Diagnostic Ultrasound [5 ed.]

Table of contents :
Cover
5TH EDITION
Physics of Ultrasound
Physics of Ultrasound Christopher R.B. Merritt
CHAPTER OUTLINE
Propagation of Sound
BASIC ACOUSTICS
Wavelength and Frequency
Distance Measurement
Acoustic Impedance
Examples of Specular Reflectors
Reflection
Attenuation
Refraction
Tissue A c 1 = 1540 m/sec
Tissue B c 2 = 1450 m/sec
Transducer
INSTRUMENTATION
Transmitter
Receiver
Image Display
Mechanical Sector Scanners
Arrays
Linear Arrays
Curved Arrays
Phased Arrays
Two-Dimensional Arrays
Transducer Selection
IMAGE DISPLAY AND STORAGE
SPECIAL IMAGING MODES
Tissue Harmonic Imaging
Spatial Compounding
Three-Dimensional Ultrasound
Ultrasound Elastography
Key Points of Ultrasound Elastography
Shear Wave Elastography
Strain Elastography
IMAGE QUALITY
Spatial Resolution
IMAGING PITFALLS
Shadowing and Enhancement
DOPPLER SONOGRAPHY
Doppler Signal Processing and Display
Doppler Instrumentation
Limitations of Color Doppler Flow Imaging
Advantages of Power Doppler
Power Doppler
Interpretation of the Doppler Spectrum
Interpretation of Color Doppler
Other Technical Considerations
Doppler Frequency
Wall Filters
Spectral Broadening
Major Sources of Doppler Imaging Artifacts
Aliasing
Doppler Angle
Sample Volume Size
Doppler Gain
OPERATING MODES: CLINICAL IMPLICATIONS
Bioeffects and User Concerns
THERAPEUTIC APPLICATIONS: HIGH INTENSITY FOCUSED ULTRASOUND
REFERENCES
Biologic Effects and Safety
J. Brian Fowlkes and Christy K. Holland
REGULATION OF ULTRASOUND OUTPUT
Factors Controlling Tissue Heating
Spatial Focusing
PHYSICAL EFFECTS OF SOUND
THERMAL EFFECTS
Ultrasound Produces Heat
Temporal Considerations
Tissue Type
TABLE 2.1 Fetal Femur Temperature Increments a at 1 W/cm 2
Bone Heating
Soft Tissue Heating
Hyperthermia and Ultrasound Safety
Thermal Index
The Thermal Index
Homogeneous Tissue Model (Soft Tissue)
Tissue Model With Bone at the Focus (Fetal Applications)
Tissue Model With Bone at the Surface (Transcranial Applications)
Estimate of Thermal Effects
Summary Statement on Thermal Effects
EFFECTS OF ACOUSTIC CAVITATION
Potential Sources for Bioeffects
The AIUM Statement on Mammalian Biological Effects of Heat 24
The AIUM Statement on Mammalian Biological Effects of Heat 24 —cont’d
Evidence of Cavitation From Lithotripters
Sonochemistry
Bioeffects in Lung and Intestine
Ultrasound Contrast Agents
The AIUM Statement on Mammalian Biological Effects in Tissues With G
Considerations for Increasing Acoustic Output
Mechanical Index
Summary Statement on Gas Body Bioeffects
OUTPUT DISPLAY STANDARD
The AIUM Statement on Mammalian Biological Effects in Tissues With
The AIUM Safety Statements on Diagnostic Ultrasound
GENERAL AIUM SAFETY STATEMENTS
EPIDEMIOLOGY
CONTROLLING ULTRASOUND OUTPUT
TABLE 2.2 Optimum Ultrasound Output: Lowest Power Output That Crea
The AIUM Statement on Keepsake Fetal Imaging 107
ULTRASOUND ENTERTAINMENT VIDEOS
Contrast Agents for Ultrasound Peter N. Burns
CHAPTER OUTLINE
REQUIREMENTS AND TYPES
Blood Pool Agents
Free Gas Bubbles
Encapsulated Air Bubbles
TABLE 3.1 Regulatory and Marketing Status of Some Current Ultrasoun
Second-Generation Agents
Selective Uptake Agents
THE NEED FOR
BUBBLE-SPECIFIC IMAGING
Bubble Behavior and Incident Pressure
TABLE 3.2 Three Types of Acoustic Behavior of a Typical Perfluoroca
The Mechanical Index (MI)
The Mechanical Index
NONLINEAR ECHOES AND HARMONIC IMAGING
Harmonic B-Mode Imaging
Harmonic Spectral and Power Doppler Imaging
Tissue Harmonic Imaging
Pulse Inversion Imaging
Pulse Inversion Doppler Imaging
Plane-Wave Contrast Imaging
Amplitude and Phase Modulation Imaging
Temporal Maximum Intensity Projection Imaging
DISRUPTING BUBBLES: INTERMITTENT IMAGING
Triggered Imaging
Intermittent Harmonic Power Doppler
Disruption-Replenishment Imaging
SAFETY CONSIDERATIONS AND REGULATORY STATUS
THE FUTURE
CONCLUSION
REFERENCES
PART TWO: Abdominal and Pelvic Sonography
The Liver
Stephanie R. Wilson and Cynthia E. Withers
SONOGRAPHIC TECHNIQUE
NORMAL ANATOMY
Couinaud Anatomy
TABLE 4.1 Structures Useful for Identifying Hepatic Segments
TABLE 4.2 Couinaud Segments and Traditional Hepatic Anatomy
Ligaments
Hepatic Circulation
Portal Veins
Arterial Circulation
Hepatic Venous System
Normal Liver Size and Echogenicity
DEVELOPMENTAL ANOMALIES
Agenesis
Anomalies of Position
Accessory Fissures
Vascular Anomalies
CONGENITAL ABNORMALITIES
Liver Cyst
Peribiliary Cysts
Autosomal Dominant Polycystic Disease
Biliary Hamartomas (von Meyenburg Complexes)
INFECTIOUS DISEASES
Viral Hepatitis
Clinical Manifestations
Bacterial Diseases
Fungal Diseases: Candidiasis
Parasitic Diseases
Amebiasis
Hydatid Disease
Schistosomiasis
Pneumocystis carinii
DISORDERS OF METABOLISM
Fatty Liver
Glycogen Storage Disease (Glycogenosis)
Cirrhosis
Elastography
Cirrhosis: Sonographic Features
Doppler Ultrasound Characteristics
VASCULAR ABNORMALITIES
Portal Hypertension
n ear the umbilicus (Cruveilhier-Baumgarten syndrome) 86
Portal Vein Thrombosis
Budd-Chiari Syndrome
Portal Vein Aneurysm
Intrahepatic Portosystemic Venous Shunts
Aneurysm, Pseudoaneurysm, and Dissection
Hereditary Hemorrhagic Telangiectasia
Peliosis Hepatis
HEPATIC MASSES
Liver Mass Characterization
Role of Microbubble Contrast Agents
Liver Mass Detection
HEPATIC NEOPLASMS
TABLE 4.3 Schematic of Algorithm for Liver Mass Diagnosis on Cont
Benign Hepatic Neoplasms
Cavernous Hemangioma
Focal Nodular Hyperplasia
Hepatic Adenoma
Fatty Tumors: Hepatic Lipomas and Angiomyolipomas
Malignant Hepatic Neoplasms
Hepatocellular Carcinoma
TABLE 4.4 Schematic of Algorithm for Diagnosis of Nodules in Cirrh
Hemangiosarcoma (Angiosarcoma)
Hepatic Epithelioid Hemangioendothelioma
Metastatic Liver Disease
a n d o varian cystadenocarcinoma a nd t e ratocarcinoma. 203
HEPATIC TRAUMA
Portosystemic Shunts
Transjugular Intrahepatic Portosystemic Shunts
Malfunction of Transjugular Intrahepatic Portosystemic Shunts: Sonograp
Sonographically detected complications include the f o llowing:
PERCUTANEOUS LIVER BIOPSY
INTRAOPERATIVE ULTRASOUND
Acknowledgment
REFERENCES
The Spleen
Patrick M. Vos, John R. Mathieson, and Peter L. Cooperberg
CHAPTER OUTLINE
EMBRYOLOGY AND ANATOMY
SONOGRAPHIC TECHNIQUE
SONOGRAPHIC APPEARANCE
PATHOLOGIC CONDITIONS
Splenomegaly
TABLE 5.1 Causes of Splenomegaly
Types of Splenic Cysts
Focal Abnormalities
Splenic Cysts
Nodular Splenic Lesions
Causes of Splenic Nodules
Focal Solid Splenic Lesions
Focal Solid Splenic Masses
Other Abnormalities
Sickle Cell Disease
Gaucher Disease
Gamna-Gandy Bodies
Splenic Trauma
CONGENITAL ANOMALIES
INTERVENTIONAL PROCEDURES
PITFALLS IN INTERPRETATION
REFERENCES
The Biliary Tree and Gallbladder Korosh Khalili and Stephanie R. Wil
CHAPTER OUTLINE
THE BILIARY TREE
Anatomy and Normal Variants
Sonographic Technique
Choledochal Cysts
Caroli Disease
Overview of Biliary Tree Obstruction
Causes of Biliary Obstruction
Choledocholithiasis
Intrahepatic Stones
Common Bile Duct Stones
Mirizzi Syndrome
Hemobilia
Pneumobilia
Biliary Tree Infection
Acute (Bacterial, Ascending) Cholangitis
Liver Flukes
Recurrent Pyogenic Cholangitis
Ascariasis
HIV Cholangiopathy
Immune-Related Diseases of the Biliary Tree
Primary Biliary Cirrhosis and Autoimmune Cholangitis
Primary Sclerosing Cholangitis
Causes of Secondary Sclerosing Cholangitis
IgG4-Related Cholangitis
Cholangiocarcinoma
Intrahepatic Cholangiocarcinoma
Hilar Cholangiocarcinoma
Criteria for Unresectable Hilar Cholangiocarcinoma
Metastases to Biliary Tree
THE GALLBLADDER
Anatomy and Normal Variants
Distal Cholangiocarcinoma
Sonographic Technique
Gallstone Disease
Biliary Sludge
Causes of Sonographic Nonvisualization of Gallbladder
Acute Cholecystitis
TABLE 6.1 Acute Calculous Cholecystitis: Pathologic-Sonographic Correl
Causes of Gallbladder Wall Thickening
o r diverticulitis, a n d even p y e lonephritis can demonstrate a
Gangrenous Cholecystitis
Perforated Gallbladder
Emphysematous Cholecystitis
Acalculous Cholecystitis
Torsion (Volvulus) of Gallbladder
Chronic Cholecystitis
Porcelain Gallbladder
Adenomyomatosis (Adenomatous Hyperplasia)
Polypoid Masses of Gallbladder
Cholesterol Polyps
Adenomas, Adenomyomas, and
Inflammatory Polyps
Common Polypoid Masses of the Gallbladder
Malignancies
Gallbladder Carcinoma
Patterns of Tumor Spread
Sonographic Appearance
REFERENCES
The Pancreas Thomas Winter and Maryellen R.M. Sun
ANATOMY AND SONOGRAPHIC TECHNIQUE
Pancreatic Head
Pancreatic Body
Pancreatic Tail
Pancreatic Parenchyma
Fatty Pancreas
Embryology and Pancreatic Duct
Imaging Anatomic Variants
Peripancreatic Structures
ACUTE PANCREATITIS
Approach to Imaging
Imaging in Acute Pancreatitis
TABLE 7.1 Causes of Acute Pancreatitis
Ultrasound Findings
TABLE 7.2 Sonographic Abnormalities in Patients With Acute Pancreat
Complications
Local Complications of Acute Pancreatitis
Acute Fluid Collections
Pseudocysts
o f “ the u s ual s u s pects”: serous cystic neoplasm (microcystic
Necrosis and Abscess
Treatment
Vascular Complications
CHRONIC PANCREATITIS
Approach to Imaging
Ultrasound Findings
Pseudocysts
Portal and Splenic Vein Thrombosis
Masses Associated With Chronic Pancreatitis
PANCREATIC NEOPLASMS
Periampullary Neoplasm
Pancreatic Carcinoma
Pancreatic Cancer Imaging: Three Key Concepts
Detection of Pancreatic Cancer
Ultrasound Findings
Resectability Imaging
Color Doppler Ultrasound
Pancreatic Cancer Imaging: Suggested Approach
TABLE 7.3 Pancreatic Color Doppler Score
CYSTIC PANCREATIC LESIONS
TABLE 7.4 Estimated Prevalence of Cystic Pancreatic Lesions a
High-Risk Features of Cystic Pancreatic Lesions
Simple Pancreatic Cysts
cysts, s uch a s a u t osomal dominant polycystic kidney disease
Cystic Neoplasms
Serous Cystic Neoplasm
Intraductal Papillary Mucinous Neoplasm
Mucinous Cystic Neoplasm
Solid-Pseudopapillary Tumor
Rare Cystic Tumors
OTHER PANCREATIC MASSES
Endocrine Tumors
Rare Cystic Pancreatic Tumors
TABLE 7.5 Pancreatic Endocrine Tumors (PETs)
Unusual and Rare Neoplasms
Lipoma
Metastatic Tumors
CONTRAST-ENHANCED ULTRASOUND
Acknowledgment
REFERENCES
The Gastrointestinal Tract Stephanie R. Wilson
Gut Wall Pathology
ANATOMY AND SONOGRAPHIC TECHNIQUE
The Gut Signature
TABLE 8.1 Gut Signature: Histologic- Sonographic Correlation
Imaging Technique
Doppler Evaluation of Gut Wall
Contrast-Enhanced Ultrasound and Elastography of the Bowel
Adenocarcinoma
GASTROINTESTINAL TRACT NEOPLASMS
Gastrointestinal Stromal Tumors
Lymphoma
Metastases
INFLAMMATORY BOWEL DISEASE: CROHN DISEASE
Crohn Disease on Sonography
TABLE 8.2 Ultrasound Global Assessment Showing Crohn Disease Activit
Classic Features
Gut Wall Thickening
Inflammatory Fat
Lymphadenopathy
Hyperemia
Mucosal Abnormalities
Conglomerate Masses
COMPLICATIONS
Strictures
Incomplete Mechanical Bowel Obstruction
Localized Perforation
Inflammatory Masses
Fistula Formation
Perianal Inflammatory Disease
ACUTE ABDOMEN
Acute Abdomen: Sonographic Approach
Right Lower Quadrant Pain
Acute Appendicitis
Acute Appendicitis: Sonographic Diagnosis
Right-Sided Diverticulitis
Sonography of Appendiceal Perforation
Crohn Appendicitis
Acute Typhlitis
Mesenteric Adenitis With Terminal Ileitis
Right-Sided Segmental Omental Infarction
Left Lower Quadrant Pain
Acute Diverticulitis
Sonography of Diverticulitis
OTHER ABNORMALITIES
Mechanical Bowel Obstruction
Paralytic Ileus
Gut Edema
Gastrointestinal Tract Infections
AIDS Patients
Pseudomembranous Colitis
Congenital Cysts
Ischemic Bowel Disease
Pneumatosis Intestinalis
Mucocele of Appendix
Gastrointestinal Tract Hematoma
Peptic Ulcer
Bezoars
Intraluminal Foreign Bodies
Celiac Disease
Cystic Fibrosis
ENDOSONOGRAPHY
Upper Gastrointestinal Tract
Rectum: Tumor Staging of Rectal Carcinoma
Anal Canal
Fecal Incontinence
Perianal Inflammatory Disease
Sonography of Perianal Inflammatory Disease
Acknowledgment
The Kidney and Urinary Tract Mitchell Tublin, Deborah Levine, Wendy
EMBRYOLOGY
Development of the Kidneys and Ureter
Development of the Bladder
Development of the Urethra
ANATOMY
Kidney
Bladder
SONOGRAPHIC TECHNIQUE
Sonographic Criteria for Hypertrophied Column of Bertin
Kidney
Ureter
Bladder and Urethra
Ureter
HYDRONEPHROSIS
Causes of Hydronephrosis
PITFALLS IN ASSESSMENT OF OBSTRUCTION
CONGENITAL ANOMALIES
Anomalies Related to Renal Growth
Hypoplasia
Fetal Lobation
Compensatory Hypertrophy
Anomalies Related to Ascent of Kidney
Ectopia
Crossed Renal Ectopia
Horseshoe Kidney
Anomalies Related to Ureteral Bud
Renal Agenesis
Supernumerary Kidney
Duplex Collecting System and Ureterocele
Ureteropelvic Junction Obstruction
Congenital Megacalices
Congenital Megaureter
Anomalies Related to Vascular Development
Aberrant Vessels
Retrocaval Ureter
Anomalies Related to Bladder Development
Bladder Agenesis
Bladder Duplication
Bladder Exstrophy
Urachal Anomalies
Anomalies Related to Urethral Development: Diverticula
GENITOURINARY INFECTIONS
Pyelonephritis
Acute Pyelonephritis
Acute Pyelonephritis on Sonography
Renal and Perinephric Abscess
Pyonephrosis
Emphysematous Pyelonephritis
Emphysematous Pyelitis
Chronic Pyelonephritis
Papillary Necrosis
Sonographic Findings of Papillary Necrosis
Tuberculosis
Fungal Infections
Candida Albicans
Parasitic Infections
Schistosomiasis
Echinococcal (Hydatid) Disease
Acquired Immunodeficiency Syndrome
Cystitis
Infectious Cystitis
Malacoplakia
Emphysematous Cystitis
Chronic Cystitis
Causes of Bladder Wall Thickening
FISTULAS, STONES (CALCULI), AND CALCIFICATION
Bladder Fistulas
Renal Calculi
Entities That Mimic Renal Calculi
Ureteral Calculi
Bladder Calculi
Nephrocalcinosis
GENITOURINARY TUMORS
Renal Cell Carcinoma
m e n a n d w o m e n equally. 1 2 2 V o n H i p pel–Lindau (VHL) di
Imaging and Treatment Approaches
Sonographic Appearance
Biopsy and Prognosis
Pitfalls in Interpretation
Transitional Cell Carcinoma
Renal Tumors
9.56 ). The differential diagnosis includes b lood clots, sloughed papillae,
Ureteral Tumors
Bladder Tumors
Squamous Cell Carcinoma
Adenocarcinoma
Oncocytoma
Angiomyolipoma
Lymphoma
Kidney
Sonographic Appearance of Renal Lymphoma
Ureter
Bladder
Leukemia
Ureter
Bladder
Metastases
Kidney
Urachal Adenocarcinoma
Rare Neoplasms
Kidney
RENAL CYSTIC DISEASE
Cortical Cysts
Approach to Complex Renal Cyst Discovered on Sonography
Parapelvic Cysts
Medullary Cysts
Medullary Sponge Kidney
Polycystic Kidney Disease
Multicystic Dysplastic Kidney
Lithium Nephropathy
Multilocular Cystic Nephroma
Localized Cystic Disease
Neoplasm-Associated Renal Cystic Disease
Acquired Cystic Kidney Disease
Tuberous Sclerosis
Von Hippel–Lindau Disease
TRAUMA
Renal Injuries
IV: U t e r o pelvic j unction a vulsion
VASCULAR ABNORMALITIES
Renal Vascular Doppler Sonography
Renal Artery Occlusion and Infarction
Arteriovenous Fistula and Malformation
Ureteral Injuries
Bladder Injuries
Renal Artery Stenosis
Renal Artery Aneurysm
Renal Vein Thrombosis
Ovarian Vein Thrombosis
MEDICAL GENITOURINARY DISEASES
Acute Tubular Necrosis
Acute Cortical Necrosis
Glomerulonephritis
Acute Interstitial Nephritis
Diabetes Mellitus
Amyloidosis
(20%-25%), t u berculosis (50%), familial Mediterranean fever
Endometriosis
Interstitial Cystitis
NEUROGENIC BLADDER
BLADDER DIVERTICULA
POSTSURGICAL EVALUATION
Nephrectomy
Urinary Diversion
CONCLUSION
Acknowledgment
REFERENCES
The Prostate and Transrectal Ultrasound
Ants Toi
SUMMARY OF KEY POINTS
CHAPTER OUTLINE
ANATOMY
Zonal Anatomy
Vascular and Neural Structures
SONOGRAPHIC APPEARANCE
EQUIPMENT AND TECHNIQUE
BENIGN CONDITIONS
Normal Variants
Benign Prostatic Hyperplasia
Chronic Prostatitis/Chronic Pelvic Pain Syndrome
Prostate Cysts
Seminal Vesicles and Vas Deferens
INFERTILITY AND TRANSRECTAL ULTRASOUND
HEMATOSPERMIA
Hematospermia
PROSTATE CANCER
Epidemiology
Prostate Cancer: Key Facts
Prostate-Specific Antigen and Variants
Role of Prostate-Specific Antigen (PSA)
Screening
Alternate Prostate Cancer Biomarkers
Clinical Staging and Histologic Grading
TABLE 10.1 Staging of Prostate Cancer, 2010
Therapy
Sonographic Appearance of Prostate Cancer
Gray-Scale Ultrasound
Transrectal Ultrasound (TRUS) Findings Suspicious for Prostate Cancer
Color Flow and Power Doppler Imaging
Contrast-Enhanced Ultrasound
Three-Dimensional Ultrasound and Transrectal Ultrasound–Magnetic Resonan
Elastography
Bowel Preparation
Analgesia
Anticoagulation
ULTRASOUND-GUIDED BIOPSY
Preparation for Biopsy
Antibiotic Prophylaxis
Technique
Side Effects and Complications
Indications and Sampling
Indications for Prostate Biopsy
mpMRI-TRUS Fusion Biopsy
Transperineal Biopsy and Template Biopsy
Biopsy After Radical Prostatectomy
Biopsy in Men With Absent Anus
OTHER APPLICATIONS OF TRANSRECTAL ULTRASOUND AND BIOPSY IN MEN AND
CONCLUSIONS
REFERENCES
The Adrenal Glands
Christina Marie Chingkoe, Olga R. Brook, and Deborah Levine
SUMMARY KEY POINTS
ANATOMY AND PHYSIOLOGY
SONOGRAPHIC IMAGING AND SCANNING TECHNIQUE
BENIGN ADRENAL MASSES
Adrenal Adenomas
Adrenal Pseudomasses
Sonographic Features
Myelolipomas
Fat-Containing Suprarenal Masses
Sonographic Features
Pheochromocytomas
Sonographic Features
Adrenal Cysts
Sonographic Features
Cystic Adrenal Lesions
Adrenal Hemorrhage
Infectious and Inflammatory Masses
Causes of Adrenal Calcification
MALIGNANT ADRENAL MASSES
Adrenocortical Carcinomas
Metastases
Sonographic Features
Lymphoma
Sonographic Features
RARE ADRENAL MASSES
INTERVENTIONS
Ultrasound-Guided Biopsy and Interventions
Endoscopic Ultrasound
MANAGEMENT OF ADRENAL LESIONS
Intraoperative Ultrasound
Acknowledgments
REFERENCES
The Retroperitoneum
Raymond E. Bertino and Elton Mustafaraj
ATHEROSCLEROSIS
ABDOMINAL AORTIC ANEURYSM
Mortality
Definition
Pathophysiology
Natural History and Medical Therapy
Screening
Recent Studies
Ultrasound Approach
Surveillance
Sonographic Technique
Computed Tomography
False-Positive/False-Negative Results
Ultrasound Versus Computed Tomography for Evaluation of Rupture
Treatment Planning
Postoperative Ultrasound Assessment
OTHER ENTITIES CAUSING ABDOMINAL AORTIC DILATION
Inflammatory Abdominal Aortic Aneurysm
Arteriomegaly and Aortic Ectasia
Penetrating Ulcer
Pseudoaneurysm
STENOTIC DISEASE OF THE ABDOMINAL AORTA
DISEASES OF ABDOMINAL AORTA BRANCHES
Renal Arteries
Anatomy
Renal Artery Stenosis and Renovascular Hypertension
Clinical Findings in Patients With Hypertension That Increase Probabi
Renal Artery Duplex Doppler Sonography
Renal Artery Aneurysm
Mesenteric Arteries
Anatomy
Mesenteric Ischemia
Median Arcuate Ligament Syndrome
Mesenteric Artery Duplex Doppler Sonography
Iliac Veins and Inferior Vena Cava
Anatomy
Anatomic Variants
Thrombosis
Nutcracker Syndrome
Pelvic Congestion Syndrome
Inferior Vena Cava Neoplasms
Other Inferior Vena Cava Findings
NONVASCULAR DISEASES OF THE RETROPERITONEUM
Solid Masses
Retroperitoneal Fibrosis
CONCLUSION
Dynamic Ultrasound of Hernias of the Groin and Anterior Abdominal
Deborah Levine, Lisa Napolitano, and A. Thomas Stavros
CHAPTER OUTLINE
TECHNICAL REQUIREMENTS
THE REPORT FOR DYNAMIC ULTRASOUND OF GROIN HERNIAS
HERNIA CONTENTS
DYNAMIC MANEUVERS
KEY SONOGRAPHIC LANDMARKS
INGUINAL AND INGUINAL REGION HERNIAS
TABLE 13.1 Types of Inguinal Hernias
Indirect Inguinal Hernias
Direct Inguinal Hernias
Femoral Hernias
Spigelian Hernias
Sports Hernias
ABDOMINAL WALL OR VENTRAL HERNIAS
Linea Alba Hernias
Umbilical Hernias
Paraumbilical or Periumbilical Hernias
Incisional Hernias
Multiple Hernias
ADDITIONAL ISSUES REGARDING HERNIAS
Recurrent Groin Hernias
Hernia Complications
Entities That Simulate Groin Hernias
TABLE 13.2 Findings of Hernia Strangulation
Entities That Simulate Anterior Abdominal Wall Hernias
SUMMARY
REFERENCES
The Peritoneum
Anthony E. Hanbidge, Korosh Khalili, and Stephanie R. Wilson
CHAPTER OUTLINE
PERITONEUM, OMENTUM, AND MESENTERY
SONOGRAPHIC TECHNIQUE
ASCITES
PERITONEAL INCLUSION CYSTS (BENIGN ENCYSTED FLUID)
MESENTERIC CYSTS
PERITONEAL TUMORS
Peritoneal Carcinomatosis
Primary Tumors of Peritoneum
O O
Pseudomyxoma Peritonei
INFLAMMATORY DISEASE OF PERITONEUM
Abscess
Tuberculous Peritonitis
Sclerosing Peritonitis
RIGHT-SIDED SEGMENTAL OMENTAL INFARCTION
ENDOMETRIOSIS
LOCALIZED INFLAMMATORY PROCESS OF PERITONEAL CAVITY
LEIOMYOMATOSIS PERITONEALIS DISSEMINATA
PNEUMOPERITONEUM
CONCLUSION
REFERENCES
The Uterus
Douglas Brown and Deborah Levine
INTRODUCTION AND SCANNING TECHNIQUES
Advantages of Transvaginal Sonography
NORMAL UTERINE FINDINGS
W h en o b taining a n e ndometrial thickness measurement,
MÜLLERIAN DUCT ANOMALIES
ABNORMALITIES OF THE MYOMETRIUM
Leiomyoma
Causes of Uterine Enlargement
Leiomyomas: Sonographic Features
Leiomyosarcoma
Adenomyosis
Adenomyosis: Sonographic Features
ABNORMALITIES OF THE CERVIX
Causes of Endometrial Thickening
ABNORMALITIES OF THE ENDOMETRIUM
Causes of Metrorrhagia
Postmenopausal Endometrium
Hormone Use
Effects of Hormones on the Postmenopausal Endometrium
Postmenopausal Bleeding
The Obstructed Uterus: Hydrometrocolpos and Hematometrocolpos
Causes of Endometrial Fluid
Endometrial Hyperplasia
Endometrial Polyps
Endometrial Carcinoma
Endometrial Sarcoma
Endometrial Adhesions
Endometrial Ablation
SONOGRAPHY OF CONTRACEPTIVE DEVICES
Intrauterine Contraceptive Devices
Tubal Occlusion Devices
Bleeding Postpartum
Retained Products of Conception
POSTPARTUM FINDINGS
Normal Findings
Endometritis
Arteriovenous Malformation
Findings After Cesarean Section
Acknowledgment
REFERENCES
The Adnexa
Rochelle Filker Andreotti and Lori A. Deitte
CHAPTER OUTLINE
NORMAL ANATOMY
Technique
Normal Sonographic Appearance of the Ovary and Fallopian Tube
Changes During the Menstrual Cycle
Postmenopausal Cysts
Postmenopausal Ovary
NONNEOPLASTIC LESIONS
Functional Cysts
Ovarian Remnant Syndrome
Pregnancy-Associated Ovarian Lesions
Surface Epithelial Inclusion Cysts
Paraovarian and Paratubal Cysts
Peritoneal Inclusion Cysts
Polycystic Ovarian Syndrome
Endometriosis
Adnexal Torsion
NEOPLASMS
Ovarian Cancer
( 1 5 % - 2 0 % ) , s e x c o r d – s t r o m a l t u m o r s ( 5 % -
TABLE 16.1 Ovarian Neoplasms
Surface Epithelial–Stromal Tumors
Serous Cystadenoma and Cystadenocarcinoma
Endometrioid Tumor
Clear Cell Tumor
Transitional Cell Tumor
Mucinous Cystadenoma and Cystadenocarcinoma
Borderline (Low Malignant Potential) Tumors
n e o p l a s m s , w i t h 9 5 % b e i n g b e n i g n cystic terat
Th e o thers, including dysgerminomas a n d e ndodermal s inus
Cystic Teratoma
Cystic Teratomas: Sonographic Features
Germ Cell Tumors
Dysgerminoma
Yolk Sac Tumor
Sex Cord–Stromal Tumors
Granulosa Cell Tumor
Sertoli-Leydig Cell Tumor
Th i s r a r e t u m o r , a l s o c a l l e d a n d r o b l a s t o
Thecoma and Fibroma
Metastatic Tumors
FALLOPIAN TUBE
Pelvic Inflammatory Disease
TABLE 16.2 Sonographic Findings of Pelvic Inflammatory Disease
Tubal Torsion
Fallopian Tube Carcinoma
VASCULAR ABNORMALITIES IN THE ADNEXA
Ovarian Vein Thrombosis or Thrombophlebitis
Pelvic Congestion Syndrome
SONOGRAPHIC EVALUATION OF AN ADNEXAL MASS IN ADULT WOMEN
TABLE 16.3 Society of Radiologists in Ultrasound Recommendations fo
TABLE 16.4 Ten Simple Rules for Identifying a Benign or Malignant
Postoperative Pelvic Masses
NONGYNECOLOGIC ADNEXAL MASSES
Gastrointestinal Tract Masses
Urinary Tract Masses
REFERENCES
Ultrasound-Guided Biopsy of Chest, Abdomen, and Pelvis
Theodora A. Potretzke, Thomas D. Atwell, J. William Charboneau, and
CHAPTER OUTLINE
PERCUTANEOUS NEEDLE BIOPSY
Indications and Contraindications
Periprocedural Antithrombotic Management
Imaging Methods
Ultrasound
Computed Tomography
Needle Selection
Biopsy Procedure
Needle Visualization
Specific Anatomic Applications
Liver
Pancreas
Kidney
Adrenal Gland
Spleen
Lung
Complications
O t h e r m a j o r c o m p l i c a t i o n s s e c o n d a ry to biopsy
ULTRASOUND-GUIDED DRAINAGE
Indications and Contraindications
Imaging Methods
Catheter Selection
Patient Preparation
Diagnostic Aspiration
Catheter Placement
Drainage Procedure
Follow-Up Care
Catheter Removal
Abdominal and Pelvic Abscesses: General
Specific Anatomic Applications
Liver
Biliary Tract
Bile Ducts. P ercutaneous t ranshepatic cholangiography
Pancreas
Spleen
PERCUTANEOUS CYST MANAGEMENT
Renal Cyst
Kidney
Liver Cyst
Ovarian Cyst
REFERENCES
Organ Transplantation
Derek Muradali and Tanya Punita Chawla
CHAPTER OUTLINE
Surgical Technique
LIVER TRANSPLANTATION
Normal Liver Transplant Ultrasound
Biliary Complications
Biliary Strictures
Bile Leaks
Recurrent Sclerosing Cholangitis
Biliary Sludge and Stones
Dysfunction of the Sphincter of Oddi
Arterial Complications
Hepatic Artery Stenosis
Hepatic Artery Thrombosis
Elevated Hepatic Arterial Resistive Index
Hepatic Artery Pseudoaneurysms
Celiac Artery Stenosis
Portal Vein Complications
Inferior Vena Cava Complications
Hepatic Vein Stenosis
Extrahepatic Fluid Collections
Adrenal Hemorrhage
Intrahepatic Fluid Collections
Abscess Versus Infarct
Intrahepatic Solid Masses
Surgical Technique
RENAL TRANSPLANTATION
Normal Renal Transplant Ultrasound
Gray-Scale Assessment
Doppler Assessment
Abnormal Renal Transplant
Parenchymal Pathology
Chronic Rejection
Infection
Prerenal Vascular Complications
Arterial Thrombosis
Renal Artery Stenosis
Doppler Criteria for Renal Artery Stenosis
Venous Thrombosis
Renal Vein Stenosis
Postrenal Collecting System Obstruction
Arteriovenous Malformations and Pseudoaneurysms
Fluid Collections
PANCREAS TRANSPLANTATION
Surgical Technique
Venous Drainage
Arterial Supply
TABLE 18.1 Surgical Techniques for Pancreatic Transplantation
Normal Pancreas Transplant Ultrasound
Role of Contrast-Enhanced Ultrasound
Abnormal Pancreas Transplant
Arteriovenous Fistula and Pseudoaneurysms
Rejection
Pancreatitis
Fluid Collections
Duodenal leaks in systemic v e nous-bladder drainage
Miscellaneous Complications
POST TRANSPLANT LYMPHOPROLIFERATIVE DISORDER
Treatment Options
REFERENCES
PART THREE: Small Parts, Carotid Artery, and
Peripheral Vessel Sonography
The Thyroid Gland
Luigi Solbiati, J. William Charboneau, Vito Cantisani, Carl Reading,
CHAPTER OUTLINE
INSTRUMENTATION AND TECHNIQUE
ANATOMY
CONGENITAL THYROID ABNORMALITIES
NODULAR THYROID DISEASE
Nodular Thyroid Disease: Sonographic Evaluation
Pathologic Features and Sonographic Correlates
Hyperplasia and Goiter
Adenoma
Carcinoma
Follicular Thyroid Carcinoma: Sonographic Features
Anaplastic Thyroid Carcinoma: Sonographic Features
Lymphoma
Thyroid Metastases
Fine-Needle Aspiration Biopsy
TABLE 19.1 Diagnostic Yield of Thyroid Fine-Needle Aspiration (FNA)
Sonographic Applications
Detection of Thyroid Masses
TABLE 19.2 Reliability of Sonographic Features in Differentiation o
Differentiation of Benign and Malignant Nodules
Thyroid Imaging Reporting and Data System
Contrast-Enhanced Ultrasound and Elastography
Guidance for Needle Biopsy
The Incidentally Detected Nodule
1. Th e epidemic of thyroid nodules has resulted mostly from ultrasound
2. The incidence o f thyroid cancer is increasing.
Evaluation of Nodules Incidentally Detected by Sonography
DIFFUSE THYROID DISEASE
4. W h i c h i n c i d e n t a lly discovered nodules should be pursued?
Diffuse Thyroid Diseases
S u b a c u t e g r a n u l o m a t o u s t h y r o i d i t i s o r D
Acknowledgment
The Parathyroid Glands
Bonnie J. Huppert and Carl Reading
EMBRYOLOGY AND ANATOMY
PRIMARY HYPERPARATHYROIDISM
Prevalence
Diagnosis
Pathology
Treatment
Causes of Primary Hyperparathyroidism
Vascularity
Size
Multiple Gland Disease
Carcinoma
SONOGRAPHIC APPEARANCE
Shape
Echogenicity and Internal Architecture
ADENOMA LOCALIZATION
Sonographic Examination and Typical Locations
Ectopic Locations
Retrotracheal/Retroesophageal Adenoma
Mediastinal Adenoma
Intrathyroid Adenoma
Carotid Sheath/Undescended Adenoma
PERSISTENT OR RECURRENT HYPERPARATHYROIDISM
S E C O N D A R Y H Y P E R P A R A T H Y R O I D I S M
PITFALLS IN INTERPRETATION
False-Positive Examination
Parathyroid Adenoma: Causes of Examination Errors
False-Negative Examination
ACCURACY IN IMAGING
Ultrasound
Other Modalities
Importance of Imaging in Primary Hyperparathyroidism
INTRAOPERATIVE SONOGRAPHY
PERCUTANEOUS BIOPSY
ETHANOL ABLATION
REFERENCES
The Breast
Jordana Phillips, Rashmi J. Mehta, and A. Thomas Stavros
CHAPTER OUTLINE
APPLICATIONS OF BREAST ULTRASOUND
BREAST ANATOMY AND PHYSIOLOGY
SONOGRAPHIC EQUIPMENT
SONOGRAPHIC TECHNIQUE
Patient Position
Annotation
Documentation of Lesions
Split-Screen Imaging
Special Breast Techniques
Doppler Sonography
Elastography
Three-Dimensional Ultrasound
Contrast-Enhanced Ultrasound
TABLE 21.1 Breast Imaging Reporting and Data System (BI-RADS) Categ
REPORTING
Normal Tissues and Variations
Cysts and Cystic Masses
Simple Cysts
SONOGRAPHIC FINDINGS
Complicated Cysts
Complex Cystic and Solid Masses
Solid Masses
TABLE 21.2 Comparison of Morphologic and Histopathologic Features o
Suspicious Findings
Indistinct Margins
Spiculation or Thick Echogenic Rim
Angular Margins
Microlobulations
Not Parallel (Not Taller-Than-Wide) Orientation
Duct Extension
Acoustic Shadowing
Hypoechogenicity
Calcifications
Associated Features
Benign Findings
Hyperechoic Tissue
Parallel (Wider-Than-Tall) Orientation
Thin Echogenic Capsule
DIAGNOSTIC ULTRASOUND INDICATIONS
Symptomatic Breast
Breast Pain
Palpable Abnormality
Nipple Discharge
Mammographic Findings
Size Correlation
Shape Correlation
Location or Position Correlation
Surrounding Tissue Density Correlation
Sonographic-Mammographic Confirmation
NICHE APPLICATIONS FOR BREAST ULTRASOUND
Infection
Implants
Breast Cancer Staging
Sonographic–Magnetic Resonance Imaging Correlation
ULTRASOUND-GUIDED INTERVENTION
REFERENCES
The Scrotum
Daniel Sommers and Thomas Winter
CHAPTER OUTLINE
SONOGRAPHIC TECHNIQUE
Scrotal Sonography: Current Uses
NORMAL ANATOMY
Pathologic Classification of Testicular Tumors 32
INTRATESTICULAR SCROTAL MASSES
Malignant Tumors
Germ Cell Tumors
Non–Germ Cell Tumors
Testicular Metastases
Lymphoma and Leukemia
Testicular Metastases
Extramedullary Myeloma
Metastatic Disease
Benign Intratesticular Lesions
Cysts
Testicular Cystic Lesions
Tubular Ectasia of Rete Testis
Cystic Dysplasia
Epidermoid Cysts
Abscess
I n patients with acquired immunodeficiency syndrome
Segmental Infarction
Adrenal Rests
Splenogonadal Fusion
Calcifications
Scrotal Calcifications
EXTRATESTICULAR PATHOLOGIC LESIONS
Tunica Vaginalis
Hydrocele, Hematocele, and Pyocele
Paratesticular Masses
Extratesticular Tumors/Masses
Hernia
Calculi
Varicocele
Fibrous Pseudotumor
Polyorchidism
Epididymal Lesions
Cystic Lesions
Tumors
Sperm Granuloma
Postvasectomy Changes in the Epididymis
Chronic Epididymitis
Sarcoidosis
ACUTE SCROTAL PAIN
Causes of Acute Scrotal Pain
Torsion
Epididymitis and Epididymo-orchitis
Fournier Gangrene
F o urnier gangrene i s a necrotizing fasciitis o f the perineum,
TRAUMA
CRYPTORCHIDISM
REFERENCES
Overview of Musculoskeletal Ultrasound Techniques and Applications
Colm McMahon and Corrie Yablon
CHAPTER OUTLINE
GENERAL CONSIDERATIONS
Doppler Imaging
Elastography
Extended Field of View Imaging
MUSCLES
TENDONS
Sonographic Signs of Tendon Tears
LIGAMENTS
NERVES
JOINT ASSESSMENT
SOFT TISSUE MASSES
TABLE 23.1 Fat-Containing Soft Tissue Lesions
FOREIGN BODIES
SOFT TISSUE INFECTION
REFERENCES
CONCLUSION
The Shoulder
Colm McMahon and Corrie Yablon
CHAPTER OUTLINE
CLINICAL PERSPECTIVE
SHOULDER ANATOMY
a n d also the coracoclavicular ligaments, which h e l p s tabilize
SCAN TECHNIQUE
TABLE 24.1 Routine Shoulder Ultrasound Protocol
Biceps Tendon Evaluation
Subscapularis Tendon Evaluation
Supraspinatus Evaluation
Infraspinatus, Teres Minor, and Posterior Shoulder Evaluation
Rotator Cuff Musculature Evaluation
ROTATOR CUFF DEGENERATION AND TEARS
Background
Tendinosis
Full-Thickness Rotator Cuff Tears
Partial-Thickness Rotator Cuff Tears
Postsurgical Rotator Cuff
Muscle Atrophy
Subacromial-Subdeltoid Bursa
Calcific Tendinitis
LONG HEAD BICEPS TENDON PATHOLOGY
ARTHROPATHY
Degenerative
Inflammatory
Th e s h o ulder can be involved in inflammatory a rthropathies, i n c
PITFALLS IN SHOULDER ULTRASOUND
CONCLUSION
REFERENCES
Musculoskeletal Interventions
Ronald S. Adler
TECHNICAL CONSIDERATIONS
INJECTION TECHNIQUE
INJECTION MATERIALS
INJECTION OF JOINTS
(MTP) o r metacarpophalangeal (MCP) a n d interphalangeal
SUPERFICIAL PERITENDINOUS AND PERIARTICULAR INJECTIONS
Foot and Ankle
Hand and Wrist
INJECTION OF DEEP TENDONS
F r equently r equested deep t endon injections include those f o r t
Biceps Tendon
Iliopsoas Tendon
Abductor and Hamstring Tendons
BURSAL, GANGLION CYST, AND PARALABRAL INJECTIONS
Calcific Tendinitis
INTRATENDINOUS INJECTIONS: PERCUTANEOUS TENOTOMY
PERINEURAL INJECTIONS
CONCLUSION
REFERENCES
The Extracranial Cerebral Vessels
Edward I. Bluth, Stephen I. Johnson, and Laurie Troxclair
CHAPTER OUTLINE
INTRODUCTION: INDICATIONS FOR CAROTID ULTRASOUND EXAMINATION
Indications for Carotid Ultrasound
CAROTID ARTERY ANATOMY
CAROTID ULTRASOUND EXAMINATION
CAROTID ULTRASOUND INTERPRETATION
Visual Inspection of Gray-Scale Images
Vessel Wall Thickness and Intima-Media Thickening
Plaque Characterization
Ultrasound Plaque Classification System
Ultrasound Types of Plaque Morphology
Plaque Ulceration
Ultrasound Features Suggestive of Plaque Ulceration
Gray-Scale Evaluation of Stenosis
Doppler Spectral Analysis
Standard Examination
Pitfalls in Interpretation
Spectral Broadening
High-Velocity Blood Flow Patterns
TABLE 26.1 Diagnostic Criteria for Carotid Ultrasound Examinations
TABLE 26.2 Alternative Diagnostic Criteria for Estimating Carotid A
Color Doppler Ultrasound
Optimal Settings for Low-Flow Vessel Evaluation
Optimization of Color Doppler Low-Flow Vessel Evaluation
Advantages and Pitfalls
Color Doppler Evolution of Carotid Stenosis
Power Doppler Ultrasound
Power Doppler Evaluation of Carotid Stenosis
Pitfalls and Adjustments
Causes of Image/Doppler Mismatch
Internal Carotid Artery Occlusion
Internal Carotid Artery Occlusion
Follow-Up of Stenosis
Preoperative Strategies for Patients With Carotid Artery Disease
Postoperative Ultrasound
Carotid Artery Stents and Revascularization
TABLE 26.3 Recommendations for Follow-Up Based on Ultrasound Assess
Grading Carotid Intrastent Restenosis
NONATHEROSCLEROTIC CAROTID DISEASE
TABLE 26.4 Carotid Artery Stenosis Grading After Stent
Internal Carotid Artery Dissection: Spectrum of Findings
Pulsatile Neck Masses in the Carotid Region
TRANSCRANIAL DOPPLER SONOGRAPHY
VERTEBRAL ARTERY
Anatomy
Sonographic Technique and Normal Examination
Subclavian Steal
Abnormal Vertebral Artery Waveforms
Stenosis and Occlusion
Thrombosis
INTERNAL JUGULAR VEINS
Sonographic Technique
Acknowledgment
REFERENCES
Peripheral Vessels
Mark E. Lockhart, Heidi R. Umphrey, Therese M. Weber, and Michelle
Sonographic Examination Technique
Stenosis Evaluation
PERIPHERAL ARTERIES
Ultrasound Examination and Imaging Protocol
Lower Extremity Arteries
Normal Anatomy
Peripheral Arterial Occlusion
Peripheral Arterial Stenosis
Aneurysm
Pseudoaneurysm
Arteriovenous Fistula
Lower Extremity Vein Bypass Grafts
Upper Extremity Arteries
Normal Anatomy
Ultrasound Examination and Imaging Protocol
Arterial Occlusion, Aneurysm, and Pseudoaneurysm
Arterial Stenosis
Subclavian Stenosis
Thoracic Outlet Syndrome
Radial Artery Evaluation for Coronary Bypass Graft
PERIPHERAL VEINS
Sonographic Examination Technique
Lower Extremity Veins
Normal Anatomy
Ultrasound Examination and Imaging Protocol
Acute Deep Venous Thrombosis
Residual (Chronic) Deep Venous Thrombosis
Potential Pitfalls
Complete Venous Doppler Versus More Limited Examinations
Recommendations for Deep Venous Thrombosis Follow-Up
Venous Insufficiency
Venous Mapping
Upper Extremity Veins
Normal Anatomy
Ultrasound Examination and Imaging Protocol
Upper Extremity Acute Deep Venous Thrombosis
Differentiation of Acute From Residual or Chronic Venous Thrombosis
Potential Pitfalls
Sonographic Examination Technique
Vascular Mapping Before Hemodialysis Access
Upper Extremity
HEMODIALYSIS
Arteriovenous Fistula and Graft
Ultrasound Examination and Imaging Protocol
Arteriovenous Fistula
Graft
Palpable Focal Masses Near Arteriovenous Fistula and Graft
Arteriovenous Fistula Maturation Evaluation
Arteriovenous Fistula and Graft Stenosis
Arterial Steal
Arm and Leg Swelling With Arteriovenous Fistula or Graft
Arteriovenous Fistula and Graft Occlusion
CONCLUSION
REFERENCES
Overview of Obstetric Imaging
Deborah Levine
TRAINING, PERSONNEL, AND EQUIPMENT
Indications for First-Trimester Ultrasound
Indications for Second- and Third-Trimester Ultrasound
ULTRASOUND GUIDELINES
First Trimester
General Survey Guidelines for First-Trimester Ultrasound
Second and Third Trimesters
Survey Guidelines for Second- and Third-Trimester Ultrasound
ROUTINE ULTRASOUND SCREENING
Estimation of Gestational Age
Indications for Detailed Fetal Anatomic Survey
Identification of Twin/Multiple Pregnancies
Screening and Perinatal Outcomes
Benefits of Routine Second-Trimester Ultrasound Screening
Three-Dimensional Ultrasound
Prudent Use of Ultrasound
Fetal Malformations: Diagnostic Accuracy
MAGNETIC RESONANCE IMAGING
CONCLUSION
REFERENCES
Bioeffects and Safety of Ultrasound in Obstetrics
Jacques S. Abramowicz
Scanning Mode
System Setup
INSTRUMENT OUTPUTS
Dwell Time
THERMAL EFFECTS
Gestational age is critical when considering heat dispersion.
BIOEFFECTS OF ULTRASOUND
Animal Research
MECHANICAL EFFECTS
Human Studies
Birth Weight
Delayed Speech
Dyslexia
Nonright-Handedness
Neurologic Development and Behavioral Issues
IS DOPPLER DIFFERENT?
Congenital Malformations
Childhood Malignancies
SAFETY GUIDELINES
CONCLUSION
TABLE 29.1 Duration of Obstetric Ultrasound as a Function of The
REFERENCES
The First Trimester
Elizabeth Lazarus and Deborah Levine
CHAPTER OUTLINE
MATERNAL PHYSIOLOGY AND EMBRYOLOGY
SONOGRAPHIC APPEARANCE OF NORMAL INTRAUTERINE PREGNANCY
Gestational Sac
β -hCG and Early Pregnancy Ultrasound
Barriers to Use of Strict β -hCG Thresholds in Determination of Pre
Embryo and Amnion
Yolk Sac
Embryonic Cardiac Activity
Umbilical Cord and Cord Cyst
ESTIMATION OF GESTATIONAL AGE
Gestational Sac Size
Crown-Rump Length
EARLY PREGNANCY FAILURE
TABLE 30.1 Rate of Spontaneous Abortion in Early Pregnancy
Diagnostic Findings of Early Pregnancy Failure
Diagnostic Findings of Early Pregnancy Failure
Gestational Sac Mean Sac Diameter 25 mm or Greater and No Embryo
Crown-Rump Length 7 mm or Greater and No Heartbeat
Worrisome Findings of Early Pregnancy Failure
Embryos With Crown-Rump Length Less Than
7 mm and No Heartbeat
Gestational Sac With Mean Sac Diameter 16 to
24 mm and No Embryo
TABLE 30.2 Worrisome Findings for Early Pregnancy Failure
Gestational Sac Appearance
Small Mean Sac Diameter in Relationship to Crown-Rump Length
Abnormally Large Amnion With Respect to Embryo Size
Yolk Sac Size and Shape
Embryonic Bradycardia
ECTOPIC PREGNANCY
Clinical Presentation
Sonographic Diagnosis
Risk of Ectopic Pregnancy
Heterotopic Gestation
Serum β -hCG Levels
Specific Sonographic Findings
Nonspecific Sonographic Findings
Adnexal Mass
Free Fluid
Endometrium
Implantation Sites
Pregnancy of Unknown Location
Management
EVALUATION OF THE EMBRYO
Normal Embryologic Findings Mimicking Pathology
Rhombencephalon
Physiologic Anterior Abdominal Wall Herniation
Abnormal Embryos
GESTATIONAL TROPHOBLASTIC DISEASE
Hydatidiform Molar Pregnancy
Complete Molar Pregnancy
Partial Molar Pregnancy
Coexistent Hydatidiform Mole and Normal Fetus
Persistent Trophoblastic Neoplasia
Invasive Mole
Choriocarcinoma
Placental-Site Trophoblastic Tumor
Sonographic Features of Persistent Trophoblastic Neoplasia
Diagnosis and Treatment
CONCLUSION
REFERENCES
Chromosomal Abnormalities
Bryann Bromley and Beryl Benacerraf
CHAPTER OUTLINE
FIRST-TRIMESTER SCREENING FOR ANEUPLOIDY
Nuchal Translucency and Trisomy 21
Serum Biochemical Markers
Combined First-Trimester Screening
Integrated and Sequential Screening
Standardization of Nuchal Translucency Measurement Technique
Fetal Nuchal Translucency (NT) Measurement Technique
Criteria for an Accurate Crown-Rump Length
Nuchal Translucency and Other Aneuploidies
Cystic Hygroma
Nasal Bone
Criteria for Nasal Bone (NB) Evaluation
IVC
Other Markers for Aneuploidy
Reversed Flow in Ductus Venosus
Tricuspid Regurgitation
Thickened Nuchal Translucency With Normal Karyotype
SECOND-TRIMESTER SCREENING FOR TRISOMY 21
Nuchal Fold
TABLE 31.1 Likelihood Ratios (LRs) of Isolated Markers for Trisomy
TABLE 31.2 Trisomy 21: Likelihood Ratios (LRs) of Cluster of Mark
Trisomy 21: Common Second-Trimester Sonographic Markers
Facial Profile (Nasal Bone)
TABLE 31.3 Pooled Estimates of Detection Rates (DRs), False-Positiv
Femur Length
Humerus Length
Urinary Tract Dilation
Echogenic Bowel
Echogenic Intracardiac Focus
Structural Anomalies
Adjunct Features of Trisomy 21
Combined Markers
Trisomy 21: Revised Risk Ratio Calculations
TRISOMY 18 (EDWARDS SYNDROME)
Trisomy 18: Common Sonographic Findings
Choroid Plexus Cysts
Trisomy 13: Common Sonographic Findings
TRIPLOIDY
Triploidy: Common Sonographic Findings
TRISOMY 13 (PATAU SYNDROME)
MONOSOMY X (TURNER SYNDROME)
PRENATAL SCREENING FOR ANEUPLOIDY WITH CELL-FREE DNA
DIAGNOSTIC TESTING
CONCLUSION
REFERENCES
Multifetal Pregnancy
Mary C. Frates
ZYGOSITY/CHORIONICITY
DETERMINATION OF CHORIONICITY
TABLE 32.1 Sonographic Findings Used to Assign Chorionicity and Am
GENERAL ISSUES
LOSS OF A TWIN
COMPLICATIONS OF MONOCHORIONICITY
Twin-Twin Transfusion Syndrome
TABLE 32.2 Complications of Twin-Twin Transfusion Syndrome
TABLE 32.3 Quintero Staging of Twin- Twin Transfusion Syndrome
Twin Anemia Polycythemia Sequence
Twin Reversed Arterial Perfusion Sequence
MONOAMNIOTIC TWINS
CONJOINED TWINS
REFERENCES
The Fetal Face and Neck
Ana P. Lourenco and Judy A. Estroff
SUMMARY KEY POINTS
CHAPTER OUTLINE
EMBRYOLOGY AND DEVELOPMENT
Face
Neck
SONOGRAPHY OF THE NORMAL FETAL FACE
ABNORMALITIES OF THE HEAD
Abnormal Size
Abnormal Shape
Craniosynostosis
Classification of Skull Deformities Based on Sutures Involved
Wormian Bones
Differential Diagnosis of Wormian Bones
Differential Diagnosis of Frontal Bossing
Forehead Abnormalities
Encephaloceles
Conditions Associated With Hypotelorism
ORBIT ABNORMALITIES
Hypotelorism
Hypertelorism
Microphthalmia and Anophthalmia
Conditions Associated With Hypertelorism
TABLE 33.1 Normal Orbital Diameters in the Fetus
Coloboma
Dacryocystocele
Congenital Cataracts
Associations With Microphthalmos
Differential Diagnosis of Congenital Cataracts
EAR ABNORMALITIES
MIDFACE ABNORMALITIES
Hypoplasia
Absent Nasal Bone
Differential Diagnosis of Cleft Lip and Palate
Other Nasal Abnormalities
Cleft Lip and Palate
Associated Signs of Cleft Palate With Cleft Lip
Bilateral Cleft Lip or Palate
Median Cleft Lip or Palate
Unusual Facial (Tessier) Clefts
Unilateral Cleft Lip or Palate
LOWER FACE ABNORMALITIES
Macroglossia and Oral Masses
Conditions Associated With Macroglossia
Isolated Cleft of Secondary Palate
Micrognathia and Retrognathia
NECK ABNORMALITIES
Nuchal Translucency and Thickening
SOFT TISSUE TUMORS
Lymphatic Malformation (Cystic Hygroma)
Cervical Teratoma
Thyromegaly and Goiter
CONCLUSION
Acknowledgments
The Fetal Brain
Ants Toi and Deborah Levine
DEVELOPMENTAL ANATOMY
Embryology
TABLE 34.1 Differentiation of Brain Regions From Primary Vesicles
Sonographic Anatomy
Cranial Structures to Note at Routine Anatomic Scan
o b literation s uggests Chiari II malformation a n d s p ina b ifida.
a n d a rachnoid cysts. 45-47
Variants (Usually Normal)
Choroid Plexus Cysts
Blake Pouch Cyst
Cavum Veli Interpositi
VENTRICULOMEGALY AND HYDROCEPHALUS
Pathogenesis of Ventriculomegaly
Examples of Conditions Associated With Ventriculomegaly
Ultrasound Evaluation of Ventriculomegaly
SPECIFIC ABNORMALITIES
ERRORS OF DORSAL INDUCTION
Anencephaly and Exencephaly
Cephalocele and Encephalocele
TABLE 34.2 Features of Some Autosomal Recessive Syndromes Associate
s yndrome, orofaciodigital syndrome, Bardet-Biedl syndrome, a u t o somal re
Joubert Syndrome
Meckel-Gruber Syndrome
Amniotic Band Sequence/Limb–Body Wall Complex
Ciliopathies
Cranial Changes in Spina Bifida
TABLE 34.3 Second-Trimester Cranial Signs Associated With Open Spina
TABLE 34.4 First-Trimester Signs of Open Spina Bifida
ERRORS OF VENTRAL INDUCTION
Holoprosencephaly
General Anatomic Classification of Holoprosencephaly 151,153
Factors Associated With Holoprosencephaly 149-151,153
Facial Changes Associated With Holoprosencephaly 155
Posterior Fossa and Cerebellum
Dandy-Walker Malformation
Vermis Hypoplasia or Dysplasia
Mega–Cisterna Magna
Rhombencephalosynapsis
Other Posterior Fossa Abnormalities
Arachnoid Cysts
Malformations of Cortical Development
Classification of Malformations of Cortical Development
Microcephaly
Hemimegalencephaly
Other Malformations of Cortical Development
Tuberous Sclerosis
Absence of Septi Pellucidi and
Septo-Optic Dysplasia
Ultrasound Findings of Agenesis or Dysgenesis of Corpus Callosum
INTRACRANIAL CALCIFICATIONS
INFECTIONS
VASCULAR MALFORMATIONS
A variety o f vascular m alformations a r e described p r enatal
Thrombosis of Dural Sinuses
Hemorrhagic Lesions
Hydranencephaly
TUMORS
Acknowledgments
REFERENCES
CONCLUSION
The Fetal Spine
Elizabeth Asch and Eric Sauerbrei
DEVELOPMENTAL ANATOMY
Embryology of the Spine
TABLE 35.1 Spine Embryology During Third and Fourth Weeks After Co
Ossification of the Fetal Spine
Normal Position of the Spinal Cord
TABLE 35.2 Timing and Pattern of Fetal Spine Ossification (10-22 We
SCANNING TECHNIQUES
Three-Dimensional Ultrasound
Protocol to Evaluate Spina Bifida With Three- Dimensional Volume Data
SPINA BIFIDA
Folic Acid Fortification
TABLE 35.3 Definition of Terms for Spinal Abnormalities
Risk Factors for Neural Tube Defect (NTD)
Pathogenesis and Pathology
Alpha-Fetoprotein and Ultrasound Screening
Causes of Elevated Maternal Serum Alpha-Fetoprotein
Sonographic Findings in the Spine
Associated Cranial Abnormalities
Anatomic Landmarks Used to Establish Level of Bony Defect
Associated Noncranial Abnormalities
Sonographic Signs of Spina Bifida
Fetal Surgery for Myelomeningocele
Prognosis
MYELOCYSTOCELE
DIASTEMATOMYELIA
SCOLIOSIS AND KYPHOSIS
Causes of Scoliosis or Kyphosis
SACRAL AGENESIS
CAUDAL REGRESSION
SACROCOCCYGEAL TERATOMA
SIRENOMELIA
Types of Sacrococcygeal Teratomas
REFERENCES
PRESACRAL FETAL MASS
Presacral Masses
The Fetal Chest
Dorothy Bulas
CHAPTER OUTLINE
DEVELOPMENT OF STRUCTURES IN THE CHEST
Pulmonary Development
Normal Sonographic Features of the Fetal Chest
Stages of Human Lung Development
PULMONARY HYPOPLASIA, APLASIA, AND AGENESIS
Normal Diaphragm
Normal Thymus
CONGENITAL PULMONARY AIRWAY MALFORMATION SPECTRUM
Congenital Pulmonary Airway Malformation
TABLE 36.1 Causes of Pulmonary Hypoplasia
TABLE 36.2 Normal Thoracic Circumference Correlated With Gestational
TABLE 36.3 Differential Diagnosis of Echogenic Lesion in Fetal Thor
Bronchopulmonary Sequestration
Congenital Lobar Overinflation
PLEUROPULMONARY BLASTOMA
P l e u r o p u l m o n a ry blastoma i s a r a r e p r i m a ry neopl
CONGENITAL HIGH AIRWAY OBSTRUCTION
BRONCHOGENIC CYST
TABLE 36.4 Differential Diagnosis of Fetal Thoracic Cystic Lesio
NEURENTERIC CYST
PLEURAL EFFUSION
Secondary p leural e ffusion occurs in a s sociation with a n e
CONGENITAL DIAPHRAGMATIC HERNIA
PERICARDIAL EFFUSION
PULMONARY LYMPHANGIECTASIA
Poor Prognostic Factors in Congenital Diaphragmatic Hernia
Predictors of Decreased Survival in Congenital Diaphragmatic Hernia
Other Hernias and Eventration
Associated Anomalies
TABLE 36.5 Sample Studies of Predictors of Survival in Left-Sided
Morbidity and Mortality
In Utero Therapy
CONCLUSION
REFERENCES
The Fetal Heart
Elizabeth R. Stamm and Julia A. Drose
TABLE 37.1 Congenital Heart Disease and Associated Risk Factors
TABLE 37.1 Congenital Heart Disease and Associated Risk Factors—cont
TABLE 37.2 Recurrence Risks in Siblings for Any Congenital Hear
TABLE 37.3 Suggested Offspring Recurrence Risk (%) for Congenital
NORMAL FETAL CARDIAC ANATOMY AND SCANNING TECHNIQUES
Common Indications for Fetal Echocardiography
STRUCTURAL ANOMALIES
Atrial Septal Defect
Ventricular Septal Defect
Atrioventricular Septal Defect
Ebstein Anomaly
A rrhythmias, particularly s u p raventricular tachycardias
Hypoplastic Right Ventricle
Hypoplastic Left Heart Syndrome
Univentricular Heart
Truncus Arteriosus
Double-Outlet Right Ventricle
Tetralogy of Fallot
Transposition of Great Arteries
Anomalous Pulmonary Venous Return
Coarctation of Aorta
Aortic Stenosis
Pulmonic Stenosis
Cardiosplenic Syndromes
Asplenia and Polysplenia: Associated Findings
Cardiac Tumors
Cardiomyopathy
A n i n c r eased incidence of a s ymmetrical septal hypertrophy
Ectopia Cordis
ARRHYTHMIAS
Premature Atrial and Ventricular Contractions
Tachycardia
Bradycardia
Congenital Heart Block
The Fetal Gastrointestinal Tract and Abdominal Wall
Nir Melamed, Anne Kennedy, and Phyllis Glanc
THE GASTROINTESTINAL TRACT
Embryology of the Digestive Tube
Esophagus
Esophageal Atresia
TABLE 38.1 Types of Esophageal Atresia
Stomach
Small or Absent Fetal Stomach
Absent Stomach
Dilated Fetal Stomach
Midline or Right-Sided Stomach
Intraluminal Gastric Masses
Small Bowel and Colon
Bowel Obstruction
Meconium Ileus
Anorectal Malformations
Enteric Duplication Cysts
TABLE 38.2 Meconium Peritonitis Findings and Likelihood of Need f
Meconium Peritonitis and Pseudocyst
3 8 . 7 ) , echogenic bowel, dilated bowel, a n d p o l y h y d r a m n
Echogenic Bowel
Conditions Associated With Echogenic Bowel
Liver
Hepatomegaly
Hepatic Calcifications
Conditions Associated With Hepatic Calcifications
Hepatic Cysts and Masses
Gallbladder and Biliary System
Nonvisualization of the Gallbladder
Fetal Gallstones
Choledochal Cyst
Pancreas
Pancreatic Cysts
Spleen
Splenomegaly
Splenic Cysts
Gastroschisis
Epidemiology
ABDOMINAL WALL
Embryology
Pathogenesis
Prenatal Diagnosis
Associated Conditions
Management
Omphalocele
Epidemiology
Prenatal Diagnosis
Associated Conditions
Management
Bladder Exstrophy
Cloacal Exstrophy
Ectopia Cordis
Other Complex Body Wall Defects
Pentalogy of Cantrell
Body Stalk Anomaly
Amniotic Band Syndrome
REFERENCES
The Fetal Urogenital Tract
Katherine W. Fong, Julia Eva Kfouri, and Kirsten L. Weind Matthews
CHAPTER OUTLINE
THE NORMAL URINARY TRACT
Embryology
Sonographic Appearance
Amniotic Fluid Volume
TABLE 39.1 Renal Lengths at 14-42 Weeks’ Gestation
Amniotic Fluid Assessment a
URINARY TRACT ABNORMALITIES
Prenatal Diagnosis of Urinary Tract Abnormalities
TABLE 39.2 Amniotic Fluid Index Values in Normal Pregnancy
Evaluation of the Fetal Urinary Tract
Bilateral Renal Agenesis
Unilateral Renal Agenesis
Renal Ectopia
Bilateral Renal Agenesis
Horseshoe Kidney
Renal Cystic Disease
Multicystic Dysplastic Kidney
Obstructive Cystic Renal Dysplasia
Autosomal Recessive Polycystic Kidney Disease
Autosomal Dominant Polycystic Kidney Disease
Syndromes Associated With Renal Cystic Disease
M eckel syndrome, a l s o k n o w n a s M eckel-Gruber syndrome,
Hyperechogenic Kidneys
Renal Neoplasm
Adrenal Mass
TABLE 39.3 Suprarenal Masses
Upper Urinary Tract Dilation
TABLE 39.4 Urinary Tract Classification System and Follow-Up
TABLE 39.5 Risk of Postnatal Pathology by Degree of Antenatal Hydr
Ureteropelvic Junction Obstruction
Vesicoureteral Junction Obstruction and Primary Megaureter
Duplication Anomalies
Duplex Kidney Findings
Lower Urinary Tract Obstruction
Vesicoureteral Reflux
be a s sociated with o ther r enal a b n o rmalities, including
Causes of Fetal Megacystis
M e g a cystis-microcolon–intestinal hypoperistalsis syndrome
In Utero Intervention: Fetal Vesicoamniotic Shunting and Cystoscopy
Antenatal Predictors of Poor Postnatal Renal Function
TABLE 39.6 Long-Term Outcomes After Prenatal Vesicoamniotic Shunting
Nonvisualized Bladder
Nonvisualization of Fetal Bladder: Etiology
Bladder Exstrophy
THE GENITAL TRACT
Normal Genitalia
Abnormal Genitalia
Hydrocolpos
CONCLUSION
Acknowledgments
REFERENCES
Ovarian Cysts
The Fetal Musculoskeletal System
Phyllis Glanc, David Chitayat, and Sheila Unger
TABLE 40.1 Major Categories of Skeletal Dysplasias 2
Resources for Molecular Tests for Diagnosis of Skeletal Dysplasias
TABLE 40.2 Birth Prevalence of Skeletal Dysplasias
NORMAL FETAL SKELETON
Development
Extremity Measurements
TABLE 40.3 Normal Extremity Long-Bone Lengths and Biparietal Diamet
Assessment of Skeletal Dysplasias: Key Features
SONOGRAPHIC EVALUATION OF FETUS WITH SKELETAL DYSPLASIA
Positive Family History
Abnormal Bone Length or Appearance
Patterns of Limb Shortening
Th e s p ine i s a s sessed f o r segmentation a nomalies, kypho scol
Additional Diagnostic Techniques
Three-Dimensional Ultrasound
Radiography
Three-Dimensional Computed Tomography
Magnetic Resonance Imaging
Molecular Diagnosis
Features Suggestive of Pulmonary Hypoplasia 52,53
Is There a Lethal Skeletal Dysplasia?
LETHAL SKELETAL DYSPLASIAS
TABLE 40.4 Severe Micromelia With Decreased Thoracic Circumference
Sonographic Assessment of Bones
Thanatophoric Dysplasia
Sonographic Assessment of Bones—cont’d
also associated with h ypochondroplasia, achondroplasia, and a c a n t h o
Other anomalies may include horseshoe kidneys, hydrone p hrosis, congenita
Achondrogenesis
Osteogenesis Imperfecta
Hypophosphatasia
TABLE 40.5 Classification of Osteogenesis Imperfecta by Type
Campomelic Dysplasia
Short-Rib Polydactyly Syndromes
T ype 1 (Saldino-Noonan) a n d type 3 (Verma-Naumoff )
Other Dysplasias
O t h e r l e t h a l s k e l e t a l d y s p l a s i a s i n c l u d
NONLETHAL OR VARIABLE PROGNOSIS SKELETAL DYSPLASIAS
Heterozygous Achondroplasia
TABLE 40.6 Rhizomelic Dysplasia: Key Features
TABLE 40.7 Micromelic Dysplasia, Mild: Key Features
TABLE 40.8 Micromelic Dysplasia, Mild and Bowed: Key Features
Diastrophic Dysplasia
Asphyxiating Thoracic Dysplasia
( 6 0 % ) w i t h r h i z o m e l i c p r e d o m i n a n c e , a l
Ellis–van Creveld Syndrome
Chondrodysplasia Punctata
Dyssegmental Dysplasia
Osteogenesis Imperfecta Types I, III, IV— Nonlethal Types
LIMB REDUCTION DEFECTS AND ASSOCIATED CONDITIONS
Proximal Focal Femoral Deficiency
Radial Ray Defects
TABLE 40.9 Nomenclature of Limb Anomalies
R o berts syndrome, o r p seudothalidomide syndrome, i s a n a u t o
Amniotic Band Sequence
Caudal Regression Syndrome and Sirenomelia
Arthrogryposis Multiplex Congenita
A symmetrical limb e nlargement m a y be caused b y hemi h ypertrophy
H e r e d i t a ry lymphedema type 1 (Nonne-Milroy lymphedema)
HAND AND FOOT MALFORMATIONS
digit. P ostaxial polydactyly (ulnar or fibular) is more common a n d i s
s u c h a s F a n c o n i s yndrome, Holt-Oram syndrome, acrocepha losy
e c t r o d a c t y l y – e c t o d e r m a l d y s p l a s i a c l e ſt i
SKELETAL FINDINGS ASSOCIATED WITH ANEUPLOIDY
Trisomy 21: Musculoskeletal Features
Trisomy 18: Musculoskeletal Features
Trisomy 13: Musculoskeletal Features
SUMMARY
Acknowledgments
REFERENCES
Fetal Hydrops
Deborah Levine
CHAPTER OUTLINE
SONOGRAPHIC FEATURES
Pleural Effusions
Ascites
TABLE 41.1 Nonimmune Hydrops: Common Causes and Associations a
Pericardial Effusions
Subcutaneous Edema
ETIOLOGY
Placentomegaly
Polyhydramnios
IMMUNE HYDROPS
Noninvasive Assessment of Alloimmunization
Measurement of Middle Cerebral Artery (MCA) Peak Systolic Velocity (
TABLE 41.2 Expected Peak Velocity of Systolic Blood Flow in the
NONIMMUNE HYDROPS
Pathophysiology
Causes and Associations
Cardiovascular Abnormalities
Neck Abnormalities
Thoracic Anomalies
Gastrointestinal Anomalies
M econium peritonitis i s a s sociated with fetal cystic fibrosis
Urinary Tract Anomalies
Lymphatic Dysplasia
Chromosomal Anomalies
Monochorionic Twins
Tumors
Anemia
Infection
Skeletal Disorders
Endocrine Disorders
Drugs
Idiopathic Disorders
DIAGNOSTIC APPROACH TO HYDROPS
Genetic Disorders
Metabolic Disorders
History
Complete Obstetric Ultrasound
TABLE 41.3 Workup of Hydrops After Fetal Echocardiogram, Maternal
Maternal Investigations
Fetal Investigations
Performing PUBS
Postnatal Investigations
FETAL WELFARE ASSESSMENT IN NONIMMUNE HYDROPS
Fetal Transfusion
OBSTETRIC PROGNOSIS
Cavity Aspiration
Maternal Complications (Mirror Syndrome)
Delivery
Predelivery Aspiration Procedures
Postnatal Outcome
REFERENCES
CONCLUSION
Fetal Measurements: Normal and Abnormal Fetal Growth and Assessment
Carol B. Benson and Peter M. Doubilet
SUMMARY OF KEY POINTS
CHAPTER OUTLINE
GESTATIONAL AGE DETERMINATION
First Trimester
TABLE 42.1 Gestational Dating by Mean Sac Diameter (MSD) in the
TABLE 42.2 Gestational Dating by Ultrasound in the First Trimester
TABLE 42.3 Gestational Age Estimation by Crown-Rump Length (CRL)
Second and Third Trimesters
Fetal Head Measurements
TABLE 42.4 Gestational Age Estimation by Biparietal Diameter (BPD)
Femur Length
Abdominal Circumference
TABLE 42.5 Gestational Age Estimation by Head Circumference (HC)
Composite Formulas
TABLE 42.6 Gestational Age Estimation by Femur Length (FL)
Gestational Age Estimation by Ultrasound: Most Accurate Approach at
TABLE 42.7 Gestational Age (GA) Assignment by Ultrasound: Most Accu
WEIGHT ESTIMATION AND ASSESSMENT
Estimation of Fetal Weight
TABLE 42.8 Accuracy of Fetal Weight Prediction Formulas
Recommended Approach
Weight Assessment in Relation to Gestational Age
TABLE 42.9 Approach to Fetal Weight Estimation
TABLE 42.10 Fetal Weight Percentiles in the Third Trimester
FETAL GROWTH ABNORMALITIES
The Large Fetus
General Population
Diabetic Mothers
TABLE 42.11 Sonographic Criteria for Large-for-Gestational Age (LGA)
The Small-for-Gestational-Age Fetus and Fetal Growth Restriction
Small-for-Gestational-Age Fetuses: Causes
ASSESSMENT OF FETAL WELL-BEING
TABLE 42.12 Sonographic Criteria for Large-for-Gestational Age (LGA)
Fetal and Placental Risk Factors Associated With Fetal Growth Restri
Maternal Risk Factors Associated With Fetal Growth Restriction
Biophysical Profile
TABLE 42.13 Biophysical Profile Parameters for 30-Minute Ultrasound E
Fetal Doppler
Ductus Venosus Doppler
Middle Cerebral Artery Doppler
Umbilical Artery Doppler
Summary of Fetal Doppler
REFERENCES
Sonographic Evaluation of the Placenta
Thomas D. Shipp
CHAPTER OUTLINE
PLACENTAL DEVELOPMENT
Placental Appearance
Placental Size
Placental Vascularity and Doppler Ultrasound
Amnion-Chorion Separation
Elastography
PLACENTA PREVIA
PLACENTA ACCRETA
PLACENTAL ABRUPTION
PLACENTAL INFARCTION
PLACENTAL MASSES
MESENCHYMAL DYSPLASIA OF THE PLACENTA
MOLAR GESTATIONS
Gestational t r o p hoblastic disease consists o f complete mole
MORPHOLOGIC PLACENTAL ABNORMALITIES
Circumvallate Placenta
Succenturiate Lobe
Bilobed Placenta
UMBILICAL CORD
Size and Appearance
Insertion Into the Placenta
Velamentous and Marginal Cord Insertions
Vasa Previa
PLACENTA DURING LABOR AND POSTPARTUM
Third Stage of Labor
Retained Products of Conception
CONCLUSION
REFERENCES
Cervical Ultrasound and Preterm Birth
Hournaz Ghandehari and Phyllis Glanc
CHAPTER OUTLINE
PRETERM BIRTH
SONOGRAPHY OF THE UTERINE CERVIX
Transabdominal Approach
Transperineal/Translabial Approach
Transvaginal Sonography
Technical Limitations and Pitfalls
Standard Technique for Cervical Measurement
Normal Cervix
“Short” Cervix
TABLE 44.1 Prediction of Spontaneous Preterm Birth Based on Gestat
PREDICTION OF SPONTANEOUS PRETERM BIRTH
Obstetric Factors
Cervical Funneling
Rate of Cervical Change
Dynamic Cervical Change
CERVICAL ASSESSMENT IN SPECIFIC CLINICAL SCENARIOS
Asymptomatic Patients
General Obstetric Population Screening
Other Sonographic Features
Cervix: Abnormal Findings on TVS a
TAS Findings That Indicate TVS Follow-Up
High-Risk Obstetric Population Screening
Risk Factors for Preterm Birth
Symptomatic Patients
Cervical Incompetence and Vaginal Pessary
Vaginal Progesterone and 17-Alpha Hydroxyprogesterone Caproate
MANAGEMENT PROTOCOLS FOR THE ABNORMAL CERVIX
CONCLUSION
Acknowledgment
REFERENCES
PART FIVE: Pediatric Sonography
Neonatal and Infant Brain Imaging
Carol M. Rumack and Amanda K. Auckland
CHAPTER OUTLINE
SONOGRAPHIC TECHNIQUE
EQUIPMENT
Coronal Imaging
Coronal Brain Scans: Normal Structures
M o v i n g p o s t e r i o r l y , t h e f r o n t a l h o r n s o
Sagittal Imaging
Sagittal Brain Scans: Normal Structures
Posterior Fontanelle Imaging
Mastoid Fontanelle Imaging
Three-Dimensional Ultrasound
STANDARDIZED REPORTS
Standardized Views for Display
Ultrasound of the Brain: Standard Report Template
DEVELOPMENTAL ANATOMY
Brain Sulcal Development and Subarachnoid Spaces
Cavum Septi Pellucidi and Cavum Vergae
Cavum Veli Interpositi
Frontal Horn Variants
Choroid Plexus and Variants
Pitfalls in Neurosonography
Germinal Matrix
Calcar Avis
Cerebellar Vermis
Cisterna Magna
CONGENITAL BRAIN MALFORMATIONS
Congenital Brain Malformations
Stages of Brain Development a
DISORDERS OF NEURAL TUBE CLOSURE
Chiari Malformations
Chiari II Malformation: Sonographic Findings
Th e r e i s u s u a l l y m a r k e d e n l a r g e m e n t o f t
Agenesis of Corpus Callosum
Agenesis of Corpus Callosum: Sonographic Findings
Corpus Callosum Lipoma
Dandy-Walker Spectrum
Dandy-Walker Malformation: Sonographic Findings
Posterior Fossa Cystic Lesions
DISORDERS OF DIVERTICULATION AND CLEAVAGE: HOLOPROSENCEPHALY
Septo-Optic Dysplasia
Alobar Holoprosencephaly: Sonographic Findings
Alobar Holoprosencephaly
Semilobar Holoprosencephaly
Lobar Holoprosencephaly
Middle Interhemispheric Form of Holoprosencephaly
DISORDERS OF SULCATION AND CELLULAR MIGRATION
Schizencephaly
Lissencephaly
DESTRUCTIVE LESIONS
Porencephalic Cyst
Hydranencephaly
Cystic Encephalomalacia
Metabolic Disorders
HYDROCEPHALUS
Cerebrospinal Fluid Production and Circulation
Causes of Hydrocephalus
Level of Obstruction
V e n t r i c u l a r e n l a r g e m e n t d o e s n o t a l w a y s
Germinal Matrix Hemorrhage
GMH m a y lead t o IVH, h y drocephalus, a n d porencephaly.
HYPOXIC-ISCHEMIC EVENTS
Arterial Watershed Determines Regional Pattern of Brain Damage
TABLE 45.1 Patterns of Hypoxic- Ischemic Injury in Newborns
Optimal Brain Ultrasound Screening in Premature Infants (Less Than 3
TABLE 45.2 Grades of Germinal Matrix Hemorrhage
Subependymal Hemorrhage (Grade I Hemorrhage)
Intraventricular Hemorrhage (Grade II Hemorrhage)
Signs of Intraventricular Hemorrhage
Intraventricular Hemorrhage With Hydrocephalus (Grade III Hemorrhage)
Intraparenchymal Hemorrhage (Grade IV Hemorrhage)
Cerebellar Hemorrhage
Subarachnoid Hemorrhage
Cerebral Edema and Infarction
White Matter Injury of Prematurity or Periventricular Leukomalacia
Term Infants With Hypoxic Ischemic Injury
Focal Infarction
Cerebral Infarction: Sonographic Signs
Lenticulostriate Vasculopathy
Hyperechoic Caudate Nuclei
POSTTRAUMATIC INJURY
Subdural and Epidural Hematomas
INFECTION
Congenital Infections
Neonatal Acquired Infections
Meningitis and Ventriculitis
INTRACRANIAL MASSES
Brain Tumors
( P N E T s ) , e p e n d y m o m a s , 2 2 4 a n d c h o r o i d p l
Common Brain Tumors in First Year of Life
Cystic Intracranial Lesions
Arachnoid Cysts
Porencephalic Cysts
Choroid Plexus Cysts
TABLE 45.3 Cystic Brain Lesions
Sites of Arachnoid Cysts a
Subependymal Cysts
Periventricular Leukomalacia
Galenic Venous Malformations
Supratentorial Periventricular Cystic Lesions
Frontal Horn Cysts
Duplex Sonography of the Neonatal and Infant Brain
Thierry A.G.M. Huisman and Andrea Poretti
Doppler Optimization
SONOGRAPHIC TECHNIQUE
Approaches
Doppler Optimization
Safety Considerations
TABLE 46.1 Factors That Change Resistive Index (RI)
Doppler Measurements and Factors That Change Resistive Index
NORMAL HEMODYNAMICS
Normal Arterial Blood Flow Patterns
TABLE 46.2 Range of Arterial Blood Flow Velocities in Full-Term In
Normal Venous Blood Flow Patterns
INTENSIVE CARE THERAPIES AND CEREBRAL HEMODYNAMICS
Mechanical Ventilation
TABLE 46.3 Mean Venous Blood Flow Velocities in Full-Term Newborns
Extracorporeal Membrane Oxygenation
Therapeutic Hypothermia and Brain Cooling
Brain Death
DIFFUSE NEURONAL INJURY
Hypoxic Ischemic Injury and Asphyxia
Cerebral Edema
INTRACRANIAL HEMORRHAGE AND STROKE
Focal Arterial Ischemic Stroke
HYDROCEPHALUS
VASCULAR MALFORMATIONS
Dural Venous Sinus Thrombosis
INTRACRANIAL TUMORS
UNCOMMON VASCULAR APPLICATIONS
PITFALLS OF DUPLEX SONOGRAPHY
NEAR-FIELD STRUCTURES
Differentiation of Subarachnoid From Subdural Fluid Collections
Doppler Sonography of the Brain in Children
Dorothy Bulas and Alexia Egloff
SUMMARY OF KEY POINTS
CHAPTER OUTLINE
SONOGRAPHIC TECHNIQUE
ULTRASOUND POWER SETTINGS
TABLE 47.1 Tips for Performing Transcranial Doppler Sonography in
LIMITATIONS AND PITFALLS IN TRANSCRANIAL DOPPLER
CONTRAST ENHANCEMENT
INDICATIONS FOR TRANSCRANIAL DOPPLER IMAGING
Indications for Transcranial Doppler in Adults
Additional Indications for Transcranial Doppler in Children
Sickle Cell Disease
Cerebrovascular Disease: Indicators in Children With Sickle Cell Dise
TABLE 47.2 STOP Stroke Risk Categories
Vasospasm
TABLE 47.3 Severity of Vasospasm With Typical Velocities 29
Evaluation of Collateral Flow
Headaches
Sleep Apnea
Hydrocephalus
TABLE 47.4 Factors That Change Cerebral Doppler Indices
Vascular Malformations
Asphyxia
Cerebral Edema and Hyperventilation Therapy
Evaluation of Right-to-Left Shunt
Brain Death
Sonographic Criteria for Brain Death After Fontanelle Closure
Neuromonitoring and Intraoperative Neuroradiologic Procedures
Transcranial Doppler and Tissue Plasminogen Activator
Functional Transcranial Doppler
Other Potential Uses
REFERENCES
The Pediatric Head and Neck
Rupa Radhakrishnan and Beth M. Kline-Fath
CHAPTER OUTLINE
NORMAL CERVICAL ANATOMY
SUPRAHYOID SPACE
Salivary Glands
Normal Anatomy
Inflammatory Lesions
Masses
Suprahyoid Cystic Lesions
Differential Diagnosis of Suprahyoid Cystic Lesions
Masticator Space
INFRAHYOID SPACE
Thyroid Gland
Normal Anatomy
TABLE 48.1 Normal Dimensions of the Thyroid Gland a
Congenital Thyroid Lesions
TABLE 48.2 Volume of Thyroid Gland and Thickness of Each Lobe a
Differential Diagnosis for Infrahyoid Cystic Lesions
Thyroid Masses
Malignant Thyroid Nodule: Sonographic Characteristics
Parathyroid Glands
Other Cystic Lesions
LACKING DEFINITION BY THE HYOID
Congenital Lesions
Branchial Anomalies
Dermoid and Epidermoid Lesions
Ectopic Thymus
Teratomas
Vascular Lesions
Vascular Anomalies
Vascular Malformations
Vascular Anomalies 162
Vascular Tumors
Other Congenital Lesions
Iatrogenic Lesions
Inflammatory Lesions
Lymph Nodes
TABLE 48.3 Age and Causes of Lymphadenopathy
TABLE 48.4 Site of Node and Causes of Lymphadenopathy
Fibromatosis Colli
Masses
Malignant Neoplasms
Congenital Infantile Myofibromatosis
REFERENCES
The Pediatric Spinal Canal
Ilse Castro-Aragon, Deborah Levine, and Carol M. Rumack
EMBRYOLOGY
SONOGRAPHIC TECHNIQUE AND NORMAL ANATOMY
SPINAL ANOMALIES
Tethered Spinal Cord
SPINAL DYSRAPHISM
Open Spinal Dysraphism
TABLE 49.1 Clinical-Radiologic Classification System for Spinal Dysra
Closed Spinal Dysraphism With a Subcutaneous Mass
A. Myelocele
B. Myelomeningocele
C. Intradural Lipoma D. Lipomyelocele E. Lipomyelomeningocele
Closed Spinal Defects Without a Subcutaneous Mass
Simple Dysraphic States
Complex Dysraphic States (Disorders of Gastrulation)
Anomalies at Risk for Spinal Dysraphism
TUMORS
TABLE 49.2 Altman’s Classification of Sacrococcygeal Teratomas
M C
HEMORRHAGE AND INFECTION
ARACHNOID CYSTS
INTRAOPERATIVE AND OTHER USES OF SPINAL SONOGRAPHY
The Pediatric Chest
Chetan Chandulal Shah and S. Bruce Greenberg
ULTRASOUND TECHNIQUE
Indications for Extracardiac Chest Sonography
PLEURAL EFFUSION AND EMPYEMA
Sonographic Signs of Pleural Fluid
Free Fluid Movement With Respiration
Fluid Color Flow Doppler Signal
Diaphragm Sign
Displaced-Crus Sign
Bare-Area Sign
Sonography Versus Computed Tomography Scan
Mass Versus Fluid
Sonographic Signs of Pleural Fluid
Parapneumonic Collections and Empyema
Lung Abscess Versus Empyema
LUNG PARENCHYMAL DISORDERS
Pneumonia
Round Pneumonia
Chest Radiograph or Ultrasound?
Atelectasis
Congenital Pulmonary Airway Malformation
Bronchopulmonary Foregut Malformation
DIAPHRAGM DISORDERS
a diaphragmatic hernia ( Fig. 50.27 ), a s u b p hrenic abscess, 34,35
VASCULAR DISORDERS
Vascular Thrombosis
Superior Vena Cava Thrombosis: Doppler Sonographic Findings
Lymphovascular Malformation
MEDIASTINAL MASSES
Thymic Index
Abnormal Location of Thymus Mimicking Mass Lesion
Anterior Mediastinal Masses
TABLE 50.1 Formula for Calculation of Thymic Index
Lymphadenopathy
Posterior Mediastinal Masses
ULTRASOUND-GUIDED INTERVENTIONAL PROCEDURES
OTHER LESS ESTABLISHED INDICATIONS
TABLE 50.2 Normal Thymic Index Values for Children Younger Than 2
REFERENCES
The Pediatric Liver and Spleen
Sara M. O’Hara
ANATOMY
Portal Vein Anatomy
Left Lobe of Liver
Right Lobe of Liver
Hepatic Vein Anatomy
NEONATAL JAUNDICE
Causes of Neonatal Jaundice
Choledochal Cyst
Spontaneous Rupture of Bile Duct
Paucity of Interlobular Bile Ducts and Alagille Syndrome
Biliary Atresia
Neonatal Hepatitis
Neonatal Jaundice and Urinary Tract Infection or Sepsis
Inborn Errors of Metabolism
Inborn Errors of Metabolism
STEATOSIS
Causes of Steatosis
Diseases Associated With Gallstones in Children
CIRRHOSIS
CHOLELITHIASIS
LIVER TUMORS
Identification
Benign Liver Tumors
Hemangiomas
Liver Masses in Children
Infantile Hemangioendotheliomas
Mesenchymal Hamartomas
Adenomas
Focal Nodular Hyperplasia
Malignant Liver Tumors
Hepatoblastoma
Hepatocellular Carcinoma
Undifferentiated Embryonal Sarcoma
Biliary Rhabdomyosarcoma
Metastases
Detection of Tumor Angiogenesis
LIVER ABSCESS AND GRANULOMAS
Pyogenic Abscess
Parasitic Abscesses
Amebiasis
Echinococcosis
Schistosomiasis
Granulomas of the Liver
DOPPLER ASSESSMENT OF LIVER DISEASE AND PORTAL HYPERTENSION IN CHIL
Basic Principles
Normal Flow Patterns in Splanchnic Vessels
Possibilities and Pitfalls
Sonographic Technique
Child With Liver Disease: Doppler Examination for Portal Hypertension
Abnormal Flow Patterns Within the Portal System
Absent Doppler Signal
Arterialized Portal Venous Flow
Causes of Absent Doppler Signal
Reversed or To-and-Fro Flow
Abnormal Hepatic Arterial Doppler Patterns
Portal Venous Hypertension
Prehepatic Portal Hypertension
Causes of Portal Vein Thrombosis
Intrahepatic Portal Hypertension
Causes of Cirrhosis in Children
Suprahepatic (Posthepatic) Portal Hypertension
Causes of Hepatic Venous Occlusive Disease
Surgical Portosystemic Shunts
Hepatic Shear Wave Elastography
DOPPLER SONOGRAPHY IN CHILDREN RECEIVING LIVER TRANSPLANT
Pretransplantation Evaluation
Posttransplantation Evaluation
Multiorgan Transplants
THE SPLEEN
Causes of Splenic Enlargement
Acknowledgment
REFERENCES
The Pediatric Urinary Tract and Adrenal Glands
Harriet J. Paltiel and Diane S. Babcock
CHAPTER OUTLINE
PEDIATRIC URINARY TRACT SONOGRAPHY
Technique
TABLE 52.1 Patient Preparation for Urinary Tract Ultrasound
TABLE 52.2 Reference Values for Infant Kidney Length (in Centimeter
TABLE 52.3 Reference Values for Infant Kidney Volume (in Milliliter
TABLE 52.4 Mean Total Renal Volumes (Values Are Mean ± Standard
TABLE 52.5 New Centiles for Renal Growth of the Solitary or Singl
TABLE 52.6 Shape and Correction Coefficient (k) for Bladder Volume
Normal Renal Anatomy
Normal Bladder Anatomy
CONGENITAL ANOMALIES OF THE URINARY TRACT
Renal Duplication
Other Renal Anomalies
CAUSES OF HYDRONEPHROSIS
Ureteropelvic Junction Obstruction
Ureteral Obstruction
PRENATAL PRESENTATION
POSTNATAL PRESENTATION
Bladder Outlet Obstruction
Vesicoureteral Reflux
Prune-Belly Syndrome
Megacystis-Microcolon-Malrotation– Intestinal Hypoperistalsis Syndrome
Bladder Exstrophy
Urachal Anomalies
URINARY TRACT INFECTION
Acute Pyelonephritis
Chronic Pyelonephritis
Neonatal Candidiasis
Cystitis
MEDICAL RENAL DISEASE
Acute Kidney Injury
Common Causes of Acute Kidney Injury
Chronic Kidney Disease
TABLE 52.7 Kidney Disease Outcomes Quality Initiative—Stages of Chr
Causes of Cortical Nephrocalcinosis
Medullary Nephrocalcinosis
URINARY TRACT CALCIFICATION
Renal Cortical Calcification
TABLE 52.8 Causes of Medullary Nephrocalcinosis 86
Urinary Stasis
Renal Vein Thrombosis Calcifications
Dystrophic Calcification
Urolithiasis
RENAL TRAUMA
RENAL VASCULAR DISEASE
Doppler Sonographic Examination Technique
Normal Vascular Anatomy and Flow Patterns
Causes of Increased Resistance to Intrarenal Arterial Flow
Causes of Increased Resistive Index in Renal Arteries
Clinical Applications
Vessel Patency
Acute Renal Vein Thrombosis
Causes of Acute Renal Vein Thrombosis
TABLE 52.9 Causes of Renovascular Hypertension 112
Renal Artery Stenosis
RENAL TRANSPLANTATION
Vascular Complications
R e nal a rtery thrombosis with associated graſt infarction
Perinephric Fluid Collections
Parenchymal Abnormalities
Urologic Complications
Tumors
RENAL CYSTIC DISEASE
Autosomal Recessive Polycystic Kidney Disease
Autosomal Dominant Polycystic Kidney Disease
Multicystic Renal Dysplasia
Nephronophthisis and Medullary Cystic Disease
Congenital Renal Cysts
Tuberous Sclerosis and Von Hippel–Lindau Disease
Acquired Cysts
Mesoblastic Nephroma
RENAL TUMORS
Wilms Tumor
Renal Cell Carcinoma
Angiomyolipoma
Multilocular Cystic Nephroma
Renal Lymphoma
Bladder Tumors
PEDIATRIC ADRENAL SONOGRAPHY
Normal Anatomy
Congenital Adrenal Hyperplasia
TABLE 52.10 Adrenal Measurements in Neonates: Mean ± SD (Mean Per
Neonatal Adrenal Hemorrhage
Neuroblastoma
Beckwith-Wiedemann syndrome, H irschsprung disease, neurofibromatosis
Pheochromocytoma
Adrenocortical Neoplasm
a n d Li-Fraumeni syndrome. 238
The Pediatric Gastrointestinal Tract
Susan D. John and Martha Mappus Munden
CHAPTER OUTLINE
ESOPHAGUS AND STOMACH
Normal Anatomy and Technique
Stomach: Optimal Measurements
Esophagus
Stomach
Hypertrophic Pyloric Stenosis
Hypertrophic Pyloric Stenosis
T C
Normal
Pseudothick
Normal
Pylorospasm and Minimal Muscular Hypertrophy
Pitfalls in Sonographic Diagnosis
Pitfalls in Diagnosis of Hypertrophic Pyloric Stenosis (HPS)
Gastric Diaphragm
Gastritis and Ulcer Disease
Bezoar
Congenital Duodenal Obstruction
DUODENUM AND SMALL BOWEL
Duodenal Hematoma
Small Bowel Obstruction
Intussusception
Sonographic Signs of Intussusception
Ectopic or Imperforate Anus
COLON
INTESTINAL INFLAMMATORY DISEASE
Causes of Intestinal Wall Thickening
Sonographic Signs of Necrotizing Enterocolitis
Appendicitis
Sonographic Signs of Appendicitis
Sonographic Signs of Appendiceal Perforation
Gastrointestinal Neoplasms and Cysts
PANCREAS
Normal Anatomy and Technique
Pancreatitis
Pancreatic Masses
p a n c r e a s i n c l u d e l ymphangioma, solid pseudopapillary tumor
Pediatric Pelvic Sonography
William L. Simpson, Jr., Humaira Chaudhry, and Henrietta Kotlus Rosen
SONOGRAPHIC TECHNIQUE
NORMAL FEMALE ANATOMY
The Uterus
TABLE 54.1 Pediatric Uterine Measurements
The Ovary
The Vagina
TABLE 54.2 Pediatric Ovarian Volume Measurements
OVARIAN ABNORMALITIES
Ovarian Cysts
Complications: Torsion, Hemorrhage, Rupture
Acute Ovarian Torsion: Sonographic Findings
Polycystic Ovarian Disease (Stein-Leventhal)
Massive Ovarian Edema
Ovarian Neoplasms
Ovarian Masses in Children
Embryonal carcinoma a n d e ndodermal s inus t umors a r e less co
UTERINE AND VAGINAL ABNORMALITIES
Congenital Anomalies
Neoplasm
Pregnancy
Infection
Pelvic Inflammatory Disease
Pelvic Inflammatory Disease: Sonographic Findings
Foreign Bodies
ENDOCRINE ABNORMALITIES
Precocious Puberty
Causes of Primary Amenorrhea
NORMAL MALE ANATOMY
The Prostate
The Scrotum
The Testes
CONGENITAL MALE ABNORMALITIES
Acute Scrotal Pain or Swelling
ACUTE SCROTAL PAIN OR SWELLING
with or without o r chitis, torsion of the testicular appendages, t e s t i
Sonographic Signs of Testicular Torsion
Color Doppler Sonography in Testicular Torsion
Epididymitis on Color Doppler Ultrasound
Torsion on Color Doppler Ultrasound
SCROTAL MASSES
Intratesticular Causes
50. Both seminomas (malignant) a n d gonadoblastomas (the m a jorit
syndrome, male pseudohermaphroditism, a n d t rue hermaphroditism.
Extratesticular Causes
Paratesticular Tumors
a n d fi b r o sarcoma. 1 7 5 , 1 8 7 , 1 8
LOWER URINARY TRACT
Congenital Anomalies
Causes of Bladder Outlet Obstruction
The Ureter
Neurogenic or Dysfunctional Bladder
Infection
Neoplasm
Trauma
Postoperative Bladder
Presacral Masses in Children
o r o bstruction, calculi, e xtravasation, a bscess, urinoma, h e
PRESACRAL MASSES
REFERENCES
The Pediatric Hip and Other Musculoskeletal Ultrasound Applications
Leslie E. Grissom and H. Theodore Harcke
DEVELOPMENT DYSPLASIA OF THE HIP
Clinical Overview
Risk Factors for Development Dysplasia of the Hip (DDH)
Indications for Hip Ultrasound 8
Dynamic Sonographic Technique: Normal and Pathologic Anatomy
History
Technical Factors
Coronal/Neutral View
Coronal/Flexion View
Transverse/Flexion View
Alternative Views
Evaluation of the Infant at Risk
Evaluation During Treatment
OTHER PEDIATRIC MUSCULOSKELETAL ULTRASOUND APPLICATIONS
Nondevelopmental Dysplasia Hip Abnormalities
Painful Hip and Hip Joint Effusion
Teratologic Hip Dislocation
Atypical Hips
Congenital Foot Deformities
Club Foot
Vertical Talus
Congenital Limb Deformities
Proximal Focal Femoral Deficiency
Tibial Hemimelia
Congenital Nonhip Dislocations
Elbow and Knee Dislocations
Brachial Plexus Injury
Patellar Dislocation
Inflammation
Infection
Noninfectious Inflammation
Trauma
Popliteal Cysts
SUMMARY
REFERENCES
Pediatric Interventional Sonography
Neil Johnson and Allison Aguado
CHAPTER OUTLINE
GENERAL PRINCIPLES
The Patient
Personnel and Equipment
TABLE 56.1 Computed Tomography (CT) Versus Ultrasound for Intervent
ULTRASOUND TECHNIQUES
Equipment and Transducers
One Operator Versus Two
GUIDANCE METHODS
Multimodality Interventional Suites
Freehand Versus Mechanical Guides
Color Doppler Ultrasound
FREEHAND TECHNIQUE
Initial Needle Placement and Localization
Locating the Needle After Insertion
Correcting the Needle Angle
Correcting the Off-Target Needle
Training Aids for Freehand Sonographic Intervention
NEEDLES, WIRES, CATHETERS, AND BIOPSY DEVICES
Chiba Needles
Drainage Catheters
Initial Puncture Device
Biopsy Devices
Colon or Bowel
ANATOMY
Diaphragm
SEDATION
LOCAL ANESTHETIC TECHNIQUE
Ultrasound-Guided Deep Local Anesthetic Administration
ANTIBIOTICS
THE TYPICAL PROCEDURE
Prior Consultation and Prior Studies
Coagulation Studies
Aims and Expectations
Initial Ultrasound Scan Should Occur Before Sedation
Pus
Catheter Fixation May Be Difficult in Infants
Postprocedure Care and Follow-Up
SPECIFIC PROCEDURES
Abscess Drainage
Transrectal Drainage
Central Venous Access
Pleural and Peritoneal Drainage
Peripherally Inserted Central Catheter Lines
Mediastinal Mass Biopsy
Appendiceal Abscess Drainage
Percutaneous Cholangiography and Drainage
Targeted Organ Lesion Biopsy
Musculoskeletal Procedures
Head and Neck Lesions
NOTE FROM THE AUTHORS
REFERENCES
Ultrasound Artifacts: A Virtual Chapter
APPENDIX
Korosh Khalili, Hojun Yu, Alexander Jesurum, and Deborah Levine
CHAPTER OUTLINE
ASSUMPTIONS IN GRAY-SCALE IMAGING
Velocity of Sound
Attenuation of Sound
Path of Sound
Beam Profile
PROPAGATION VELOCITY ARTIFACT
ATTENUATION ERRORS
Shadowing
Increased Through Transmission
PATH OF SOUND-RELATED ARTIFACTS
Mirror Image Artifact
Comet-Tail Artifact
Refraction
Anisotropy
Reverberation Artifact
GAS-RELATED ARTIFACTS
Reverberation Artifact
Ring-Down Artifact
Dirty Shadowing Artifact
Side Lobe and Grating Lobe Artifacts
BEAM PROFILE–RELATED ARTIFACTS
Partial Volume Averaging
DOPPLER IMAGING ARTIFACTS
Loss or Distortion of Doppler Information
Artifactual Vascular Flow
Tissue Vibration Artifact
Click f o r video s h o wing t issue vibration a rtifact in patient
Aliasing and Velocity Scale Errors
Spectral Broadening
Blooming Artifact
Twinkle Artifact
Acknowledgment
REFERENCES

Citation preview

DIAGNOSTIC ULTRASOUND

DIAGNOSTIC ULTRASOUND 5TH EDITION

CAROL M. RUMACK, MD, FACR Vice Chair of Education and Professional Development Professor of Radiology and Pediatrics Associate Dean for GME University of Colorado School of Medicine Denver, Colorado

DEBORAH LEVINE, MD, FACR Co-Chief of Ultrasound Director of OB/Gyn Ultrasound Vice Chair of Academic Affairs Department of Radiology Beth Israel Deaconess Medical Center Professor of Radiology Harvard Medical School Boston, Massachusetts

PART ONE: Physics CHAPTER

1

 

Physics of Ultrasound Christopher R.B. Merritt

SUMMARY OF KEY POINTS • Quality imaging requires an understanding of basic acoustic principles. • Image interpretation requires recognition and understanding of common artifacts. • Special modes of operation, including harmonic imaging, compounding, elastography, and Doppler, expand the

capabilities of conventional gray-scale imaging. • Knowledge of mechanical and thermal bioeffects of ultrasound is necessary for prudent use. • High-intensity focused ultrasound has potential therapeutic applications.

CHAPTER OUTLINE BASIC ACOUSTICS Wavelength and Frequency Propagation of Sound Distance Measurement Acoustic Impedance Reflection Refraction Attenuation INSTRUMENTATION Transmitter Transducer Receiver Image Display Mechanical Sector Scanners Arrays Linear Arrays Curved Arrays Phased Arrays

A

Two-Dimensional Arrays Transducer Selection IMAGE DISPLAY AND STORAGE SPECIAL IMAGING MODES Tissue Harmonic Imaging Spatial Compounding Three-Dimensional Ultrasound Ultrasound Elastography Strain Elastography Shear Wave Elastography IMAGE QUALITY Spatial Resolution IMAGING PITFALLS Shadowing and Enhancement DOPPLER SONOGRAPHY Doppler Signal Processing and Display Doppler Instrumentation Power Doppler

ll diagnostic ultrasound applications are based on the detection and display of acoustic energy reflected from interfaces within the body. These interactions provide the information needed to generate high-resolution, gray-scale images of the body, as well as display information related to blood flow. Its unique imaging attributes have made ultrasound an important and versatile medical imaging tool. However, expensive stateof-the-art instrumentation does not guarantee the production of high-quality studies of diagnostic value. Gaining maximum benefit from this complex technology requires a combination of skills, including knowledge of the physical principles that

Interpretation of the Doppler Spectrum Interpretation of Color Doppler Other Technical Considerations Doppler Frequency Wall Filters Spectral Broadening Aliasing Doppler Angle Sample Volume Size Doppler Gain OPERATING MODES: CLINICAL IMPLICATIONS Bioeffects and User Concerns THERAPEUTIC APPLICATIONS: HIGH-INTENSITY FOCUSED ULTRASOUND

empower ultrasound with its unique diagnostic capabilities. The user must understand the fundamentals of the interactions of acoustic energy with tissue and the methods and instruments used to produce and optimize the ultrasound display. With this knowledge the user can collect the maximum information from each examination, avoiding pitfalls and errors in diagnosis that may result from the omission of information or the misinterpretation of artifacts.1 Ultrasound imaging and Doppler ultrasound are based on the scattering of sound energy by interfaces of materials with different properties through interactions governed by acoustic

1

2

PART I

Physics

physics. The amplitude of reflected energy is used to generate ultrasound images, and frequency shifts in the backscattered ultrasound provide information relating to moving targets such as blood. To produce, detect, and process ultrasound data, users must manage numerous variables, many under their direct control. To do this, operators must understand the methods used to generate ultrasound data and the theory and operation of the instruments that detect, display, and store the acoustic information generated in clinical examinations. This chapter provides an overview of the fundamentals of acoustics, the physics of ultrasound imaging and flow detection, and ultrasound instrumentation with emphasis on points most relevant to clinical practice. A discussion of the therapeutic application of high-intensity focused ultrasound concludes the chapter.

BASIC ACOUSTICS Wavelength and Frequency Sound is the result of mechanical energy traveling through matter as a wave producing alternating compression and rarefaction. Pressure waves are propagated by limited physical displacement of the material through which the sound is being transmitted. A plot of these changes in pressure is a sinusoidal waveform (Fig. 1.1), in which the Y axis indicates the pressure at a given point and the X axis indicates time. Changes in pressure with time define the basic units of measurement for sound. The distance between corresponding points on the time-pressure curve is defined as the wavelength (λ), and the time (T) to complete a single cycle is called the period. The number of complete cycles in a unit of time is the frequency (f) of the sound. Frequency and period are inversely related. If the period (T) is expressed in seconds, f = 1/T, or f = T × sec−1. The unit of acoustic frequency

is the hertz (Hz); 1 Hz = 1 cycle per second. High frequencies are expressed in kilohertz (kHz; 1 kHz = 1000 Hz) or megahertz (MHz; 1 MHz = 1,000,000 Hz). In nature, acoustic frequencies span a range from less than 1 Hz to more than 100,000 Hz (100 kHz). Human hearing is limited to the lower part of this range, extending from 20 to 20,000 Hz. Ultrasound differs from audible sound only in its frequency, and it is 500 to 1000 times higher than the sound we normally hear. Sound frequencies used for diagnostic applications typically range from 2 to 15 MHz, although frequencies as high as 50 to 60 MHz are under investigation for certain specialized imaging applications. In general, the frequencies used for ultrasound imaging are higher than those used for Doppler. Regardless of the frequency, the same basic principles of acoustics apply.

Propagation of Sound In most clinical applications of ultrasound, brief bursts or pulses of energy are transmitted into the body and propagated through tissue. Acoustic pressure waves can travel in a direction perpendicular to the direction of the particles being displaced (transverse waves), but in tissue and fluids, sound propagation is primarily along the direction of particle movement (longitudinal waves). Longitudinal waves are important in conventional ultrasound imaging and Doppler, while transverse waves are measured in shear wave elastography. The speed at which pressure waves move through tissue varies greatly and is affected by the physical properties of the tissue. Propagation velocity is largely determined by the resistance of the medium to compression, which in turn is influenced by the density of the medium and its stiffness or elasticity. Propagation velocity is increased by increasing stiffness and reduced by decreasing density. In the body, propagation velocity of longitudinal waves may be regarded as constant for a given tissue and is not affected by the frequency or wavelength of the sound. This is in contrast to transverse (shear) waves for

FIG. 1.1  Sound Waves.  Sound is transmitted mechanically at the molecular level. In the resting state the pressure is uniform throughout the medium. Sound is propagated as a series of alternating pressure waves producing compression and rarefaction of the conducting medium. The time for a pressure wave to pass a given point is the period, T. The frequency of the wave is 1/T. The wavelength, λ, is the distance between corresponding points on the time-pressure curve.

CHAPTER 1  Physics of Ultrasound Air

330

Fat

1450

Water

1480

Soft tissue (average)

1540

Liver

1550

Kidney

1560

Blood

1570

Muscle

1580

Bone

4080

1400

1500

1600

1700

3

1800

Propagation velocity (meters/second) FIG. 1.2  Propagation Velocity.  In the body, propagation velocity of sound is determined by the physical properties of tissue. As shown, this varies considerably. Medical ultrasound devices base their measurements on an assumed average propagation velocity of soft tissue of 1540 m/sec.

which the velocity is determined by Young modulus, a measure of tissue stiffness or elasticity. Fig. 1.2 shows typical longitudinal propagation velocities for a variety of materials. In the body the propagation velocity of sound is assumed to be 1540 meters per second (m/sec). This value is the average of measurements obtained from normal soft tissue.2,3 Although this value represents most soft tissues, such tissues as aerated lung and fat have propagation velocities significantly less than 1540 m/sec, whereas tissues such as bone have greater velocities. Because a few normal tissues have propagation values significantly different from the average value assumed by the ultrasound scanner, the display of such tissues may be subject to measurement errors or artifacts (Fig. 1.3). The propagation velocity of sound (c) is related to frequency and wavelength by the following simple equation: c= fλ Thus a frequency of 5 MHz can be shown to have a wavelength of 0.308 mm in tissue: λ = c/f = 1540 m/sec × 5,000,000 sec−1 = 0.000308 m = 0.308 mm. Wavelength is an important determinant of spatial resolution in ultrasound imaging, and selection of transducer frequency for a given application is a key user decision.

Distance Measurement Propagation velocity is a particularly important value in clinical ultrasound and is critical in determining the distance of a reflecting interface from the transducer. Much of the information used to generate an ultrasound scan is based on the precise measurement of time and employs the principles of echo-ranging (Fig. 1.4). If an ultrasound pulse is transmitted into the body and the time until an echo returns is measured, it is simple to calculate the depth of the interface that generated the echo, provided the

FIG. 1.3  Propagation Velocity Artifact.  When sound passes through a lesion containing fat, echo return is delayed because fat has a propagation velocity of 1450 m/sec, which is less than the liver. Because the ultrasound scanner assumes that sound is being propagated at the average velocity of 1540 m/sec, the delay in echo return is interpreted as indicating a deeper target. Therefore the final image shows a misregistration artifact in which the diaphragm and other structures deep to the fatty lesion are shown in a deeper position than expected (simulated image).

propagation velocity of sound for the tissue is known. For example, if the time from the transmission of a pulse until the return of an echo is 0.000145 seconds and the velocity of sound is 1540 m/ sec, the distance that the sound has traveled must be 22.33 cm (1540 m/sec × 100 cm/m × 0.000145 sec = 22.33 cm). Because the time measured includes the time for sound to travel to the interface and then return along the same path to the transducer, the distance from the transducer to the reflecting interface is 22.33 cm/2 = 11.165 cm. By rapidly repeating this process, a two-dimensional (2-D) map of reflecting interfaces is created to form the ultrasound image. The accuracy of this measurement is therefore highly influenced by how closely the presumed velocity of sound corresponds to the true velocity in the tissue being observed (see Figs. 1.2 and 1.3), as well as by the important assumption that the sound pulse travels in a straight path to and from the reflecting interface.

Acoustic Impedance Current diagnostic ultrasound scanners rely on the detection and display of reflected sound or echoes. Imaging based on transmission of ultrasound is also possible, but this is not used clinically at present. To produce an echo, a reflecting interface must be present. Sound passing through a totally homogeneous medium encounters no interfaces to reflect sound, and the medium appears anechoic or cystic. The junction of tissues or materials with different physical properties produces an acoustic interface. These interfaces are responsible for the reflection of variable amounts of the incident sound energy. Thus when ultrasound passes from one tissue to another or encounters a vessel wall or circulating blood cells, some of the incident sound

4

PART I

Physics

×

×

ms

FIG. 1.4  Ultrasound Ranging.  The information used to position an echo for display is based on the precise measurement of time. Here the time for an echo to travel from the transducer to the target and return to the transducer is 0.145 ms (0.000145 seconds). Multiplying the velocity of sound in tissue (1540 m/sec) by the time shows that the sound returning from the target has traveled 22.33 cm. Therefore the target lies half this distance, or 11.165 cm, from the transducer. By rapidly repeating this process, a two-dimensional map of reflecting interfaces is created to form the ultrasound image.

energy is reflected. The amount of reflection or backscatter is determined by the difference in the acoustic impedances of the materials forming the interface. Acoustic impedance (Z) is determined by product of the density (ρ) of the medium propagating the sound and the propagation velocity (c) of sound in that medium (Z = ρc). Interfaces with large acoustic impedance differences, such as interfaces of tissue with air or bone, reflect almost all the incident energy. Interfaces composed of substances with smaller differences in acoustic impedance, such as a muscle and fat interface, reflect only part of the incident energy, permitting the remainder to continue onward. As with propagation velocity, acoustic impedance is determined by the properties of the tissues involved and is independent of frequency.

Reflection The way ultrasound is reflected when it strikes an acoustic interface is determined by the size and surface features of the interface (Fig. 1.5). If large and relatively smooth, the interface reflects sound much as a mirror reflects light. Such interfaces are called specular reflectors because they behave as “mirrors for sound.” The amount of energy reflected by an acoustic interface can be expressed as a fraction of the incident energy; this is termed the reflection coefficient (R). If a specular reflector is perpendicular to the incident sound beam, the amount of energy reflected is determined by the following relationship: R = (Z 2 − Z1 )2 (Z 2 + Z1 )2 where Z1 and Z2 are the acoustic impedances of the media forming the interface. Because ultrasound scanners only detect reflections that return to the transducer, display of specular interfaces is highly dependent

Examples of Specular Reflectors Diaphragm Vessel wall Wall of urine-filled bladder Endometrial stripe

on the angle of insonation (exposure to ultrasound waves). Specular reflectors will return echoes to the transducer only if the sound beam is perpendicular to the interface. If the interface is not at a near 90-degree angle to the sound beam, it will be reflected away from the transducer, and the echo will not be detected (see Fig. 1.5A). Most echoes in the body do not arise from specular reflectors but rather from much smaller interfaces within solid organs. In this case the acoustic interfaces involve structures with individual dimensions much smaller than the wavelength of the incident sound. The echoes from these interfaces are scattered in all directions. Such reflectors are called diffuse reflectors and account for the echoes that form the characteristic echo patterns seen in solid organs and tissues (see Fig. 1.5B). The constructive and destructive interference of sound scattered by diffuse reflectors results in the production of ultrasound speckle, a feature of tissue texture of sonograms of solid organs (Fig. 1.6). For some diagnostic applications, the nature of the reflecting structures creates important conflicts. For example, most vessel walls behave as specular reflectors that require insonation at a 90-degree angle for best imaging, whereas Doppler imaging requires an angle of less than 90 degrees between the sound beam and the vessel.

CHAPTER 1  Physics of Ultrasound

A

5

B

FIG. 1.5  Specular and Diffuse Reflectors.  (A) Specular reflector. The diaphragm is a large and relatively smooth surface that reflects sound like a mirror reflects light. Thus sound striking the diaphragm at nearly a 90-degree angle is reflected directly back to the transducer, resulting in a strong echo. Sound striking the diaphragm obliquely is reflected away from the transducer, and an echo is not displayed (yellow arrow). (B) Diffuse reflector. In contrast to the diaphragm, the liver parenchyma consists of acoustic interfaces that are small compared to the wavelength of sound used for imaging. These interfaces scatter sound in all directions, and only a portion of the energy returns to the transducer to produce the image.

propagation velocities of sound in the media forming the interface (Fig. 1.7). Refraction is important because it is one cause of misregistration of a structure in an ultrasound image (Fig. 1.8). When an ultrasound scanner detects an echo, it assumes that the source of the echo is along a fixed line of sight from the transducer. If the sound has been refracted, the echo detected may be coming from a different depth or location than the image shown in the display. If this is suspected, increasing the scan angle so that it is perpendicular to the interface minimizes the artifact.

Attenuation

FIG. 1.6  Ultrasound Speckle.  Close inspection of an ultrasound image of the breast containing a small cyst reveals it to be composed of numerous areas of varying intensity (speckle). Speckle results from the constructive (red) and destructive (green) interaction of the acoustic fields (yellow rings) generated by the scattering of ultrasound from small tissue reflectors. This interference pattern gives ultrasound images their characteristic grainy appearance and may reduce contrast. Ultrasound speckle is the basis of the texture displayed in ultrasound images of solid tissues.

Refraction When sound passes from a tissue with one acoustic propagation velocity to a tissue with a higher or lower sound velocity, there is a change in the direction of the sound wave. This change in direction of propagation is called refraction and is governed by Snell law: sin θ1 sin θ2 = c1 c2 where θ1 is the angle of incidence of the sound approaching the interface, θ2 is the angle of refraction, and c1 and c2 are the

As the acoustic energy moves through a uniform medium, work is performed and energy is ultimately transferred to the transmitting medium as heat. The capacity to perform work is determined by the quantity of acoustic energy produced. Acoustic power, expressed in watts (W) or milliwatts (mW), describes the amount of acoustic energy produced in a unit of time. Although measurement of power provides an indication of the energy as it relates to time, it does not take into account the spatial distribution of the energy. Intensity (I) is used to describe the spatial distribution of power and is calculated by dividing the power by the area over which the power is distributed, as follows: I (W/cm2 ) = Power (W) Area (cm2 ) The attenuation of sound energy as it passes through tissue is of great clinical importance because it influences the depth in tissue from which useful information can be obtained. This in turn affects transducer selection and a number of operatorcontrolled instrument settings, including time (or depth) gain compensation, power output attenuation, and system gain levels. Attenuation is measured in relative rather than absolute units. The decibel (dB) notation is generally used to compare different levels of ultrasound power or intensity. This value is 10 times the log10 of the ratio of the power or intensity values being

6

PART I

Physics

θ1 = 20°

Tissue A c1 = 1540 m/sec Tissue B c2 = 1450 m/sec

A

B

18 8 θ2 = 18.8°

FIG. 1.7  Refraction.  When sound passes from tissue A with propagation velocity (c1) to tissue B with a different propagation velocity (c2), there is a change in the direction of the sound wave because of refraction. The degree of change is related to the ratio of the propagating velocities of the media forming the interface (sinθ1/sinθ2 = c1/c2).

compared. For example, if the intensity measured at one point in tissues is 10 mW/cm2 and at a deeper point is 0.01 mW/cm2, the difference in intensity is as follows: (10)(log10 0.01 10) = (10)(log10 0.001) = (10)(− log10 1000) = (10)(−33) = −30 dB As it passes through tissue, sound loses energy, and the pressure waves decrease in amplitude as they travel farther from their source. Contributing to the attenuation of sound are the transfer of energy to tissue, resulting in heating (absorption), and the removal of energy by reflection and scattering. Attenuation is therefore the result of the combined effects of absorption, scattering, and reflection. Attenuation depends on the insonating frequency as well as the nature of the attenuating medium. High frequencies are attenuated more rapidly than lower frequencies, and transducer frequency is a major determinant of the useful depth from which information can be obtained with ultrasound. Attenuation determines the efficiency with which ultrasound

C FIG. 1.8  Refraction Artifact.  (A) and (B) Production of an artifact by refraction of sound in a transverse scan of the mid abdomen. The direct sound path properly depicts the location of the object. (B) A “ghost image” (red) produced by refraction at the edge of the rectus abdominis muscle. The transmitted and reflected sound travels along the path of the black arrows. The scanner assumes the returning signal is from a straight line (red arrow) and displays the structure at the incorrect location. (C) Axial transabdominal image of the uterus showing a small gestational sac (A) and what appears to be a second sac (B) due to refraction artifact.

CHAPTER 1  Physics of Ultrasound Water

PRF determines the time interval between ultrasound pulses and is important in determining the depth from which unambiguous data can be obtained both in imaging and Doppler modes. The ultrasound pulses must be spaced with enough time between the pulses to permit the sound to travel to the depth of interest and return before the next pulse is sent. For imaging, PRFs from 1 to 10 kHz are used, resulting in an interval of 0.1 to 1 ms between pulses. Thus a PRF of 5 kHz permits an echo to travel and return from a depth of 15.4 cm before the next pulse is sent.

0.00 0.18

Blood Fat

0.63

Soft tissue (average)

0.70

Liver

0.94

Kidney

1.00

Muscle (parallel) Muscle (transverse)

Transducer

1.30 3.30

Bone

5.00

Air

10.00 0

2

7

4

6

8

10

Attenuation (dB/cm/MHz) FIG. 1.9  Attenuation.  As sound passes through tissue, it loses energy through the transfer of energy to tissue by heating, reflection, and scattering. Attenuation is determined by the insonating frequency and the nature of the attenuating medium. Attenuation values for normal tissues show considerable variation. Attenuation also increases in proportion to insonating frequency, resulting in less penetration at higher frequencies.

penetrates a specific tissue and varies considerably in normal tissues (Fig. 1.9).

INSTRUMENTATION Ultrasound scanners are complex and sophisticated imaging devices, but all consist of the following basic components to perform key functions: • Transmitter or pulser to energize the transducer • Ultrasound transducer • Receiver and processor to detect and amplify the backscattered energy and manipulate the reflected signals for display • Display that presents the ultrasound image or data in a form suitable for analysis and interpretation • Method to record or store the ultrasound image

Transmitter Most clinical applications use pulsed ultrasound, in which brief bursts of acoustic energy are transmitted into the body. The source of these pulses, the ultrasound transducer, is energized by application of precisely timed, high-amplitude voltage. The maximum voltage that may be applied to the transducer is limited by federal regulations that restrict the acoustic output of diagnostic scanners. Most scanners provide a control that permits attenuation of the output voltage. Because the use of maximum output results in higher exposure of the patient to ultrasound energy, prudent use dictates use of the output attenuation controls to reduce power levels to the lowest levels consistent with the diagnostic problem.4 The transmitter also controls the rate of pulses emitted by the transducer, or the pulse repetition frequency (PRF). The

A transducer is any device that converts one form of energy to another. In ultrasound the transducer converts electric energy to mechanical energy, and vice versa. In diagnostic ultrasound systems the transducer serves two functions: (1) converting the electric energy provided by the transmitter to the acoustic pulses directed into the patient and (2) serving as the receiver of reflected echoes, converting weak pressure changes into electric signals for processing. Ultrasound transducers use piezoelectricity, a principle discovered by Pierre and Jacques Curie in 1880.5 Piezoelectric materials have the unique ability to respond to the action of an electric field by changing shape. They also have the property of generating electric potentials when compressed. Changing the polarity of a voltage applied to the transducer changes the thickness of the transducer, which expands and contracts as the polarity changes. This results in the generation of mechanical pressure waves that can be transmitted into the body. The piezoelectric effect also results in the generation of small potentials across the transducer when the transducer is struck by returning echoes. Positive pressures cause a small polarity to develop across the transducer; negative pressure during the rarefaction portion of the acoustic wave produces the opposite polarity across the transducer. These tiny polarity changes and the associated voltages are the source of all the information processed to generate an ultrasound image or Doppler display. When stimulated by the application of a voltage difference across its thickness, the transducer vibrates. The frequency of vibration is determined by the transducer material. When the transducer is electrically stimulated, a range or band of frequencies results. The preferential frequency produced by a transducer is determined by the propagation speed of the transducer material and its thickness. In the pulsed wave operating modes used for most clinical ultrasound applications, the ultrasound pulses contain additional frequencies that are both higher and lower than the preferential frequency. The range of frequencies produced by a given transducer is termed its bandwidth. Generally, the shorter the pulse of ultrasound produced by the transducer, the greater is the bandwidth. Most modern digital ultrasound systems employ broadbandwidth technology. Ultrasound bandwidth refers to the range of frequencies produced and detected by the ultrasound system. This is important because each tissue in the body has a characteristic response to ultrasound of a given frequency, and different tissues respond differently to different frequencies. The range of frequencies arising from a tissue exposed to ultrasound is referred to as the frequency spectrum bandwidth of the tissue, or tissue

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signature. Broad-bandwidth technology provides a means to capture the frequency spectrum of insonated tissues, preserving acoustic information and tissue signature. Broad-bandwidth beam formers reduce speckle artifact by a process of frequency compounding. This is possible because speckle patterns at different frequencies are independent of one another, and combining data from multiple frequency bands (i.e., compounding) results in a reduction of speckle in the final image, leading to improved contrast resolution. The length of an ultrasound pulse is determined by the number of alternating voltage changes applied to the transducer. For continuous wave (CW) ultrasound devices, a constant alternating current is applied to the transducer, and the alternating polarity produces a continuous ultrasound wave. For imaging, a single, brief voltage change is applied to the transducer, causing it to vibrate at its preferential frequency. Because the transducer continues to vibrate or “ring” for a short time after it is stimulated by the voltage change, the ultrasound pulse will be several cycles long. The number of cycles of sound in each pulse determines the pulse length. For imaging, short pulse lengths are desirable because longer pulses result in poorer axial resolution. To reduce the pulse length, damping materials are used in the construction of the transducer. In clinical imaging applications, very short pulses are applied to the transducer, and the transducers have highly efficient damping. This results in very short pulses of ultrasound, generally consisting of only two or three cycles of sound. The ultrasound pulse generated by a transducer must be propagated in tissue to provide clinical information. Special transducer coatings and ultrasound coupling gels are necessary to allow efficient transfer of energy from the transducer to the body. Once in the body, the ultrasound pulses are propagated, reflected, refracted, and absorbed, in accordance with the basic acoustic principles summarized earlier. The ultrasound pulses produced by the transducer result in a series of wavefronts that form a three-dimensional (3-D) beam of ultrasound. The features of this beam are influenced by

constructive and destructive interference of the pressure waves, the curvature of the transducer, and acoustic lenses used to shape the beam. Interference of pressure waves results in an area near the transducer where the pressure amplitude varies greatly. This region is termed the near field, or Fresnel zone. Farther from the transducer, at a distance determined by the radius of the transducer and the frequency, the sound field begins to diverge, and the pressure amplitude decreases at a steady rate with increasing distance from the transducer. This region is called the far field, or Fraunhofer zone. In modern multielement transducer arrays, precise timing of the firing of elements allows correction of this divergence of the ultrasound beam and focusing at selected depths. Only reflections of pulses that return to the transducer are capable of stimulating the transducer with small pressure changes, which are converted into the voltage changes that are detected, amplified, and processed to build an image based on the echo information.

Receiver When returning echoes strike the transducer face, minute voltages are produced across the piezoelectric elements. The receiver detects and amplifies these weak signals. The receiver also provides a means for compensating for the differences in echo strength, which result from attenuation by different tissue thickness by control of time gain compensation (TGC) or depth gain compensation (DGC). Sound is attenuated as it passes into the body, and additional energy is removed as echoes return through tissue to the transducer. The attenuation of sound is proportional to the frequency and is constant for specific tissues. Because echoes returning from deeper tissues are weaker than those returning from more superficial structures, they must be amplified more by the receiver to produce a uniform tissue echo appearance (Fig. 1.10). This adjustment is accomplished by TGC controls that permit the user to selectively amplify the signals from deeper structures or to suppress the signals from superficial tissues, compensating for tissue attenuation. Although many newer machines provide

FIG. 1.10  Time Gain Compensation (TGC).  Without TGC, tissue attenuation causes gradual loss of display of deeper tissues (A). In this example, tissue attenuation of 1 dB/cm/MHz is simulated for a transducer of 10 MHz. At a depth of 2 cm, the intensity is −20 dB (1% of initial value). By applying increasing amplification or gain to the backscattered signal to compensate for this attenuation, a uniform intensity is restored to the tissue at all depths (B).

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FIG. 1.11  Dynamic Range.  The ultrasound receiver must compress the wide range of amplitudes returning to the transducer into a range that can be displayed to the user. Here, compression and remapping of the data to display dynamic ranges of 35, 40, 50, and 60 dB are shown. The widest dynamic range shown (60 dB) permits the best differentiation of subtle differences in echo intensity and is preferred for most imaging applications. The narrower ranges increase conspicuity of larger echo differences.

for some means of automatic TGC, the manual adjustment of this control is one of the most important user controls and may have a profound effect on the quality of the ultrasound image provided for interpretation. Another important function of the receiver is the compression of the wide range of amplitudes returning to the transducer into a range that can be displayed to the user. The ratio of the highest to the lowest amplitudes that can be displayed may be expressed in decibels and is referred to as the dynamic range. In a typical clinical application, the range of reflected signals may vary by a factor of as much as 1 : 1012, resulting in a dynamic range of up to 120 dB. Although the amplifiers used in ultrasound machines are capable of handling this range of voltages, gray-scale displays are limited to display a signal intensity range of only 35 to 40 dB. Compression and remapping of the data are required to adapt the dynamic range of the backscattered signal intensity to the dynamic range of the display (Fig. 1.11). Compression is performed in the receiver by selective amplification of weaker signals. Additional manual postprocessing controls permit the user to map selectively the returning signal to the display. These controls affect the brightness of different echo levels in the image and therefore determine the image contrast.

Image Display Ultrasound signals may be displayed in several ways. Over the years, imaging has evolved from simple A-mode (amplitudemode) and bistable display to high-resolution, real-time, grayscale imaging. The earliest A-mode devices displayed the voltage produced across the transducer by the backscattered echo as a vertical deflection on the face of an oscilloscope. The horizontal time sweep of the oscilloscope was calibrated to indicate the distance from the transducer to the reflecting surface. In this form of display, the strength or amplitude of the reflected sound is indicated by the height of the vertical deflection displayed on the oscilloscope. With A-mode ultrasound, only the position and strength of a reflecting structure are recorded. Another simple form of imaging, M-mode (motion-mode) ultrasound, displays echo amplitude and shows the position of

A B

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FIG. 1.12  M-Mode Display.  M-mode ultrasound displays changes of echo amplitude and position with time. Display of changes in echo position is useful in the evaluation of rapidly moving structures such as cardiac valves and chamber walls. Here, the three major moving structures in the upper gray-scale image of the fetus are recorded in the corresponding M-mode image and include the near ventricular wall (A), the interventricular septum (B), and the far ventricular wall (C). The baseline is a time scale that permits the calculation of heart rate from the M-mode data.

moving reflectors (Fig. 1.12). M-mode imaging uses the brightness of the display to indicate the intensity of the reflected signal. The time base of the display can be adjusted to allow for varying degrees of temporal resolution, as dictated by clinical application. M-mode ultrasound is interpreted by assessing motion patterns of specific reflectors and determining anatomic relationships from characteristic patterns of motion. Currently, the major application of M-mode display is evaluation of embryonic and fetal heart rates, as well as in echocardiography, the rapid motion of cardiac valves and of cardiac chamber and vessel walls. M-mode imaging may play a future role in measurement of subtle changes in vessel wall elasticity accompanying atherogenesis. The mainstay of imaging with ultrasound is provided by real-time, gray-scale, B-mode display, in which variations in display intensity or brightness are used to indicate reflected signals

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FIG. 1.13  B-Mode Imaging.  A two-dimensional (2-D), real-time image is built by ultrasound pulses sent down a series of successive scan lines. Each scan line adds to the image, building a 2-D representation of echoes from the object being scanned. In real-time imaging, an entire image is created 15 to 60 times per second.

of differing amplitude. To generate a 2-D image, multiple ultrasound pulses are sent down a series of successive scan lines (Fig. 1.13), building a 2-D representation of echoes arising from the object being scanned. When an ultrasound image is displayed on a black background, signals of greatest intensity appear as white; absence of signal is shown as black; and signals of intermediate intensity appear as shades of gray. If the ultrasound beam is moved with respect to the object being examined and the position of the reflected signal is stored, the brightest portions of the resulting 2-D image indicate structures reflecting more of the transmitted sound energy back to the transducer. In most modern instruments, digital memory is used to store values that correspond to the echo intensities originating from corresponding positions in the patient. At least 28, or 256, shades of gray are possible for each pixel, in accord with the amplitude of the echo being represented. The image stored in memory in this manner can then be sent to a monitor for display. Because B-mode display relates the strength of a backscattered signal to a brightness level on the display device, it is important that the operator understand how the amplitude information in the ultrasound signal is translated into a brightness scale in the image display. Each ultrasound manufacturer offers several options

for the way the dynamic range of the target is compressed for display, as well as the transfer function that assigns a given signal amplitude to a shade of gray. Although these technical details vary among machines, the way the operator uses them may greatly affect the clinical value of the final image. In general, it is desirable to display as wide a dynamic range as possible, to identify subtle differences in tissue echogenicity (see Fig. 1.11). Real-time ultrasound produces the impression of motion by generating a series of individual 2-D images at rates of 15 to 60 frames per second. Real-time, 2-D, B-mode ultrasound is the major method for ultrasound imaging throughout the body and is the most common form of B-mode display. Real-time ultrasound permits assessment of both anatomy and motion. When images are acquired and displayed at rates of several times per second, the effect is dynamic, and because the image reflects the state and motion of the organ at the time it is examined, the information is regarded as being shown in real time. In cardiac applications the terms 2-D echocardiography and 2-D echo are used to describe real-time, B-mode imaging; in most other applications the term real-time ultrasound is used. Transducers used for real-time imaging may be classified by the method used to steer the beam in rapidly generating each

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FIG. 1.14  Beam Steering.  (A) Linear array. In a linear array transducer, individual elements or groups of elements are fired in sequence. This generates a series of parallel ultrasound beams, each perpendicular to the transducer face. As these beams move across the transducer face, they generate the lines of sight that combine to form the final image. Depending on the number of transducer elements and the sequence in which they are fired, focusing at selected depths from the surface can be achieved Small high-frequency linear arrays are well-suited for small parts scanning. (B) Curved array. A variant of the linear array, the curved array uses tranducer elements arranged in an arc, producing a pie-shaped image. These transducers are well-suited for abdominal, pelvic, and fetal examinations. (C) Phased array. A phased array transducer produces a sector field of view by firing multiple transducer elements in precise sequence to generate interference of acoustic wavefronts that steer the beam. The ultrasound beam that results generates a series of lines of sight at varying angles from one side of the transducer to the other, producing a sector image format. These transducers require a small contact area compared to most linear and curved arrays and are useful for scanning in areas where access is limited.

individual image, keeping in mind that as many as 30 to 60 complete images must be generated per second for real-time applications. Beam steering may be done through mechanical rotation or oscillation of the transducer or by electronic means (Fig. 1.14). Electronic beam steering is used in linear array and phased array transducers and permits a variety of image display formats. Most electronically steered transducers currently in use also provide electronic focusing that is adjustable for depth. Mechanical beam steering may use single-element transducers with a fixed focus or may use annular arrays of elements with electronically controlled focusing. For real-time imaging, transducers using mechanical or electronic beam steering generate displays in a rectangular or pie-shaped format. For obstetric, small parts, and peripheral vascular examinations, linear array transducers with a rectangular image format are often used. The rectangular image display has the advantage of a larger field of view near the surface but requires a large surface area for transducer contact. Sector scanners with either mechanical or electronic steering require only a small surface area for contact and are better suited for examinations in which access is limited.

transducer in a linear or circular motion. Mechanical sector scanners using one or more single-element transducers do not allow variable focusing. This problem is overcome by using annular array transducers. Although important in the early days of realtime imaging, mechanical sector scanners with fixed-focus, single-element transducers are not presently in common use.

Mechanical Sector Scanners

Linear Arrays Linear array transducers are used for small parts, vascular, and obstetric applications because the rectangular image format produced by these transducers is well suited for these applications.

Early ultrasound scanners used transducers consisting of a single piezoelectric element. To generate real-time images with these transducers, mechanical devices were required to move the

Arrays Current technology uses a transducer composed of multiple elements, usually produced by precise slicing of a piece of piezoelectric material into numerous small units, each with its own electrodes. Such transducer arrays may be formed in a variety of configurations. Typically, these are linear, curved, phased, or annular arrays. High-density 2-D arrays have also been developed. By precise timing of the firing of combinations of elements in these arrays, interference of the wavefronts generated by the individual elements can be exploited to change the direction of the ultrasound beam, and this can be used to provide a steerable beam for the generation of real-time images in a linear or sector format.

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In these transducers, individual elements are arranged in a linear fashion. By firing the transducer elements in sequence, either individually or in groups, a series of parallel pulses is generated, each forming a line of sight perpendicular to the transducer face. These individual lines of sight combine to form the image field of view (see Fig. 1.14A). Depending on the number of transducer elements and the sequence in which they are fired, focusing at selected depths from the surface can be achieved.

Curved Arrays Linear arrays that have been shaped into convex curves produce an image that combines a relatively large surface field of view with a sector display format (see Fig. 1.14B). Curved array transducers are used for a variety of applications, the larger versions serving for general abdominal, obstetric, and transabdominal pelvic scanning. Small, high-frequency, curved array scanners are often used in transvaginal and transrectal probes and for pediatric imaging. Phased Arrays In contrast to mechanical sector scanners, phased array scanners have no moving parts. A sector field of view is produced by multiple transducer elements fired in precise sequence under electronic control. By controlling the time and sequence at which the individual transducer elements are fired, the resulting ultrasound wave can be steered in different directions as well as focused at different depths (see Fig. 1.14C). By rapidly steering the beam to generate a series of lines of sight at varying angles from one side of the transducer to the other, a sector image format is produced. This allows the fabrication of transducers of relatively small size but with large fields of view at depth. These transducers are particularly useful for neonatal head ultrasound, as well as for intercostal scanning, to evaluate the heart, liver, or spleen, and for examinations in other areas where access is limited. Two-Dimensional Arrays Transducer arrays can be formed either by slicing a rectangular piece of transducer material perpendicular to its long axis to produce a number of small rectangular elements or by creating a series of concentric elements nested within one another in a circular piece of piezoelectric material to produce an annular array. The use of multiple elements permits precise focusing. A particular advantage of 2-D array construction is that the beam can be focused in both the elevation plane and the lateral plane, and a uniform and highly focused beam can be produced (Fig. 1.15). These arrays improve spatial resolution and contrast, reduce clutter, and are well suited for the collection of data from volumes of tissue for use in 3-D processing and display. Unlike linear 2-D arrays, in which delays in the firing of the individual elements may be used to steer the beam, annular arrays do not permit beam steering and, to be used for real-time imaging, must be steered mechanically.

Transducer Selection Practical considerations in the selection of the optimal transducer for a given application include not only the requirements for

FIG. 1.15  Two-Dimensional Array.  High-density, two-dimensional (2-D) arrays consist of a 2-D matrix of transducer elements, permitting acquisition of data from a volume rather than a single plane of tissue. Precise electronic control of individual elements permits adjustable focusing on both azimuth and elevation planes.

spatial resolution, but also the distance of the target object from the transducer because penetration of ultrasound diminishes as frequency increases. In general, the highest ultrasound frequency permitting penetration to the depth of interest should be selected. For superficial vessels and organs, such as the thyroid, breast, or testicle, lying within 1 to 3 cm of the surface, imaging frequencies of 7.5 to 15 MHz are typically used. These high frequencies are also ideal for intraoperative applications. If the region to be scanned is very superficial, such that the probe does not allow for focusing at the area of interest, a standoff pad can be utilized. For evaluation of deeper structures in the abdomen or pelvis more than 12 to 15 cm from the surface, frequencies as low as 2.25 to 3.5 MHz may be required. When maximal resolution is needed, a high-frequency transducer with excellent lateral and elevation resolution at the depth of interest is required.

IMAGE DISPLAY AND STORAGE With real-time ultrasound, user feedback is immediate and is provided by video display. The brightness and contrast of the image on this display are determined by the ambient lighting in the examination room, the brightness and contrast settings of the video monitor, the system gain setting, and the TGC adjustment. The factor most affecting image quality in many ultrasound departments is probably improper adjustment of the video display, with a lack of appreciation of the relationship between the video display settings and the appearance of hard copy or images viewed on a workstation. Because of the importance of the real-time video display in providing feedback to the user, it is essential that the display and the lighting conditions under which it is viewed are standardized and matched to the display used for interpretation. Interpretation of images and archival storage of images may be in the form of transparencies printed on film by optical or laser cameras and printers, videotape, or digital picture

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FIG. 1.16  Tissue Harmonics.  As sound is propagated through tissue, the high-pressure component of the wave travels more rapidly than the rarefactional component, producing distortion of the wave and generating higher-frequency components (harmonics). (A) The acoustic field of the primary frequency is represented in blue. (B) The second harmonic (twice the primary frequency) is represented in red. (C) Using a broad-bandwidth transducer, the receiver can be tuned to generate an image from the harmonic frequency rather than the primary frequency. As a result, near field clutter is reduced since the harmonic only develops at depth in the tissue and the beam profile is improved, leading to better spatial resolution.

archiving and communications system (PACS). Increasingly, digital storage is being used for archiving of ultrasound images.

SPECIAL IMAGING MODES Tissue Harmonic Imaging Variation of the propagation velocity of sound in fat and other tissues near the transducer results in a phase aberration that distorts the ultrasound field, producing noise and clutter in the ultrasound image. Tissue harmonic imaging provides an approach for reducing the effects of phase aberrations.6 Nonlinear propagation of ultrasound through tissue is associated with the more rapid propagation of the high-pressure component of the ultrasound pressure wave than its negative (rarefactional) component. This results in increasing distortion of the acoustic pulse as it travels within the tissue and causes the generation of multiples, or harmonics, of the transmitted frequency (Fig. 1.16). Tissue harmonic imaging takes advantage of the generation, at depth, of these harmonics. Because the generation of harmonics requires interaction of the transmitted field with the propagating tissue, harmonic generation is not present near the transducer/ skin interface, and it only becomes important some distance from the transducer. In most cases the near and far fields of the image are affected less by harmonics than by intermediate locations. Using broad-bandwidth transducers and signal filtration or coded pulses, the harmonic signals reflected from tissue

interfaces can be selectively displayed. Because most imaging artifacts are caused by the interaction of the ultrasound beam with superficial structures or by aberrations at the edges of the beam profile, these artifacts are eliminated using harmonic imaging because the artifact-producing signals do not consist of sufficient energy to generate harmonic frequencies and therefore are filtered out during image formation. Images generated using tissue harmonics often exhibit reduced noise and clutter (Fig. 1.17). Because harmonic beams are narrower than the originally transmitted beams, spatial resolution is improved and side lobes are reduced.

Spatial Compounding An important source of image degradation and loss of contrast is ultrasound speckle. Speckle results from the constructive and destructive interaction of the acoustic fields generated by the scattering of ultrasound from small tissue reflectors. This interference pattern gives ultrasound images their characteristic grainy appearance (see Fig. 1.6), reducing contrast (Fig. 1.18) and making the identification of subtle features more difficult. By summing images from different scanning angles through spatial compounding (Fig. 1.19), significant improvement in the contrast-to-noise ratio can be achieved (Fig. 1.20). This is because speckle is random, and the generation of an image by compounding will reduce speckle noise because only the signal is reinforced. In addition, spatial compounding may reduce artifacts that result when an ultrasound beam strikes a specular reflector at an angle

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FIG. 1.17  Tissue Harmonic Imaging.  (A) Conventional image and (B) tissue harmonic image of gallbladder of patient with acute cholecystitis. Note the reduction of noise and clutter in the tissue harmonic image. Because harmonic beams do not interact with superficial structures and are narrower than the originally transmitted beam, spatial resolution is improved and clutter and side lobes are reduced. (With permission from Merritt CR. Technology update. Radiol Clin North Am. 2001;39:385-397.7)

FIG. 1.18  Effect of Speckle on Contrast.  (A) Speckle noise partially obscures the simulated lesion. (B) The speckle has been reduced, increasing contrast resolution between the lesion and the background. (With permission from Merritt CR. Technology update. Radiol Clin North Am. 2001;39:385-397.7)

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FIG. 1.19  Spatial Compounding.  (A) Conventional imaging is limited to a fixed angle of incidence of ultrasound scan lines to tissue interfaces, resulting in poor definition of specular reflectors that are not perpendicular to the beam. (B) Spatial compounding combines images obtained by insonating the target from multiple angles. In addition to improving detection of interfaces, compounding reduces speckle noise because only the signal is reinforced; speckle is random and not reinforced. This improves contrast.

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FIG. 1.20  Spatial Compounding.  (A) Conventional image and (B) compound image of the thyroid. Note the reduced speckle as well as better definition of regions (arrows) such as superficial tissue as well as small cysts and calcifications.

greater or less than 90 degrees. In conventional real-time imaging, each scan line used to generate the image strikes the target at a constant, fixed angle. As a result, strong reflectors that are not perpendicular to the ultrasound beam scatter sound in directions that prevent their clear detection and display. This in turn results in poor margin definition and less distinct boundaries for cysts and other masses. Compounding has been found to reduce these artifacts. Limitations of compounding are diminished visibility of shadowing and enhancement; however, these are offset by the ability to evaluate lesions, both with and without compounding, preserving shadowing and enhancement when these features are important to diagnosis.7

Three-Dimensional Ultrasound Dedicated 3-D scanners used for fetal (Fig. 1.21), gynecologic, and cardiac scanning may employ hardware-based image registration, high-density 2-D arrays, or software registration of scan planes as a tissue volume is acquired. 3-D imaging permits volume

data to be viewed in multiple imaging planes and allows accurate measurement of lesion volume.

Ultrasound Elastography Palpation is an effective method for detection of tissue abnormality based on detection of changes in tissue stiffness or elasticity and may provide the earliest indication of disease, even when conventional imaging studies are normal. Ultrasound elastography provides a noninvasive method for evaluation of tissue stiffness.8 Tissue contrast in conventional ultrasound imaging is based on the bulk modulus determined by the molecular composition of tissue, whereas elastography reflects shear properties that are determined by a higher level of tissue organization, the strain modulus. This higher level of tissue organization is most likely to be altered by disease. The dynamic range of the strain modulus is several orders of magnitude greater than the bulk modulus, permitting contrast resolution far exceeding conventional ultrasound imaging.9 Elastography therefore offers the potential for a

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Physics Key Points of Ultrasound Elastography Ultrasound imaging is based on tissue bulk modulus, reflecting interactions at the molecular level. Changes in tissue stiffness based on the tissue shear modulus are important indications of disease. Ultrasound elastography provides relatative and quantitative assessment of tissue stiffness. Ultrasound elastography is based on tissue organization (strain modulus). Strain elastography provides an indication of relative tissue stiffness. Shear wave elastography provides a quantitative estimate of the tissue stiffness (strain modulus).

FIG. 1.21  Three-Dimensional Ultrasound Image, 24-Week Fetus.  Three-dimensional ultrasound permits collection and review of data obtained from a volume of tissue in multiple imaging planes, as well as a rendering of surface features.

high degree of both sensitivity and specificity in differentiating normal and abnormal tissues.8,10,11 Tissue stiffness or elasticity is expressed by Young modulus— the ratio of compression pressure (stress) and the resulting deformation (strain) E=σ ε where E is Young modulus expressed in Pa (pascals), σ is the stress, expressed in Newtons, and ε is displacement expressed in m2. Ultrasound-based elastography permits study of the elastic behavior of tissue through two general approaches (Fig. 1.22): strain elastography and shear wave elastography.

Strain Elastography Strain elastography involves measurement of longitudinal tissue displacement before and after compression, usually by manual manipulation of the ultrasound transducer (see Fig. 1.22A). Speckle tracking using radiofrequency backscatter or Doppler is then used to evaluate tissue motion. Strain elastography cannot determine the Young modulus because the compression pressure (stress) cannot be measured directly. Instead, strain ratios are estimated by comparing lesion strain to surrounding normal tissues and displayed in the image in different shades of gray or through color maps (Fig. 1.23). Strain elastography provides an indication of relative stiffness of an area of interest compared to its surroundings.

Shear Wave Elastography Longitudinal tissue compression results in the generation of transverse shear waves12,13 (see Fig. 1.22B). In shear wave elastography, shear waves are generated by repetitive compression produced by high-intensity pulses from the ultrasound transducer (see Fig. 1.22B). In contrast to longitudinal compressional waves that propagate very quickly in the human body (≈1540 m/sec), shear waves propagate slowly (≈1-50 m/sec). Shear waves are tracked with high frame rate images to determine their velocity. The propagation velocity of shear waves is directly proportional to Young modulus and provides a quantitative estimate of tissue stiffness14,15 (Fig. 1.24).

IMAGE QUALITY The key determinants of the quality of an ultrasound image are its spatial, contrast, and temporal resolution, as well as freedom from certain artifacts.

Spatial Resolution The ability to differentiate two closely situated objects as distinct structures is determined by the spatial resolution of the ultrasound device. Spatial resolution must be considered in three planes, with different determinants of resolution for each. Simplest is the resolution along the axis of the ultrasound beam, or axial resolution. With pulsed wave ultrasound, the transducer introduces a series of brief bursts of sound into the body. Each ultrasound pulse typically consists of two or three cycles of sound. The pulse length is the product of the wavelength and the number of cycles in the pulse. Axial resolution, the maximum resolution along the beam axis, is determined by the pulse length (Fig. 1.25). Because ultrasound frequency and wavelength are inversely related, the pulse length decreases as the imaging frequency increases. Because the pulse length determines the maximum resolution along the axis of the ultrasound beam, higher transducer frequencies provide higher image resolution. For example, a transducer operating at 5 MHz produces sound with a wavelength of 0.308 mm. If each pulse consists of three cycles of sound, the pulse length is slightly less than 1 mm, and this becomes the maximum resolution along the beam

CHAPTER 1  Physics of Ultrasound

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shear waves

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FIG. 1.22  Elastography.  (A) Strain elastography (SE), and (B) shear wave elastography (SWE). Strain elastograms are images of tissue stiffness generated by analysis of speckle displacements before and after mechanical compression of tissue. The precompression frame is compared to a frame obtained after compression. In this example, the lesion is compressed much less than the surrounding tissue, indicating relative stiffness. SE is not quantitative and indicates only the relative hardness or softness of lesions compared to their surroundings. In SWE (B) high-intensity compression pulses from the transducer are focused on an area of interest, resulting in the generation of low-frequency shear waves. Speckle displacement resulting from shear (transverse) waves is tracked with multiple imaging frames in order to estimate shear wave velocity. Shear wave velocity is directly related to Young modulus, permitting a quantitative estimate of tissue stiffness.

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FIG. 1.23  Strain Elastograms.  The upper frames (A) show in vivo images of swine liver containing a lesion produced by the injection of a small volume of absolute ethanol. In the precompression image (left) the lesion located within the circle is invisible. The elastogram (right) clearly delineates the lesion as an area of increased stiffness compared to the surrounding tissue. The lower frames (B) show a gray-scale image (left) and strain elastogram (right) of a mixed solid and cystic thyroid nodule. In the elastogram the color map displays relative stiffness with softer areas appearing as shades of red, orange, and yellow, and stiffer areas as dark blue. The nodule is heterogeneous with the relatively noncompressible cystic portions differentiated from more compressible surrounding tissue. (Courtesy of P. O’Kane, Thomas Jefferson University.)

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A - Normal liver v = 1.29 ± -.10 m/s

B - Cirrhotic liver

v = 4.41 ± -.17 m/s

FIG. 1.24  Shear Wave Elastograms of (A) Normal and (B) Cirrhotic Liver.  Shear wave velocities measured in liver tissue samples by shear wave elastography indicates a velocity of 1.29 ± 0.10 m/sec in the normal liver compared to a velocity of 4.41 ± 0.17 m/sec in the cirrhotic liver. Increased shear wave velocity is associated with increased tissue stiffness due to hepatic fibrosis. (Courtesy of P. O’Kane, Thomas Jefferson University.)

FIG. 1.25  Axial Resolution.  Axial resolution is the resolution along (A) the beam axis and is determined by (B) the pulse length. The pulse length is the product of the wavelength (which decreases with increasing frequency) and the number of waves (usually two to three). Because the pulse length determines axial resolution, higher transducer frequencies provide higher image resolution. In (B) for example, a transducer operating at 5 MHz produces sound with a wavelength of 0.31 mm. If each pulse consists of three cycles of sound, the pulse length is slightly less than 1 mm, and objects A and B, which are 0.5 mm apart, cannot be resolved as separate structures. If the transducer frequency is increased to 15 MHz, the pulse length is less than 0.3 mm, permitting A and B to be identified as separate structures.

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FIG. 1.26  Lateral and Elevation Resolution.  Resolution in the planes perpendicular to the beam axis is an important determinant of image quality. Lateral resolution (L) is resolution in the plane perpendicular to the beam and parallel to the transducer and is determined by the width of the ultrasound beam. Lateral resolution is controlled by focusing the beam, usually by electronic phasing to alter the beam width at a selected depth of interest. Azimuth or elevation resolution (E) is determined by the slice thickness in the plane perpendicular to the beam and the transducer. Elevation resolution is controlled by the construction of the transducer. Both lateral resolution and elevation resolution are less than the axial resolution.

axis. If the transducer frequency is increased to 15 MHz, the pulse length is less than 0.4 mm, permitting resolution of smaller details. In addition to axial resolution, resolution in the planes perpendicular to the beam axis must also be considered. Lateral resolution refers to resolution in the plane perpendicular to the beam and parallel to the transducer and is determined by the width of the ultrasound beam. Azimuth resolution, or elevation resolution, refers to the slice thickness in the plane perpendicular to the beam and to the transducer (Fig. 1.26). The width and thickness of the ultrasound beam are important determinants of image quality. Excessive beam width and thickness limit the ability to delineate small features and may obscure shadowing and enhancement from small structures, such as breast microcalcifications and small thyroid cysts. The width and thickness of the ultrasound beam determine lateral resolution and elevation resolution, respectively. Lateral and elevation resolutions are significantly poorer than the axial resolution of the beam. Lateral resolution is controlled by focusing the beam, usually by electronic phasing, to alter the beam width at a selected depth of interest. Elevation resolution is determined by the construction of the transducer and generally cannot be controlled by the user.

IMAGING PITFALLS In ultrasound, perhaps more than in any other imaging method, the quality of the information obtained is determined by the user’s ability to recognize and avoid artifacts and pitfalls. Many imaging artifacts are induced by errors in scanning technique or improper use of the instrument and therefore are preventable. Artifacts may cause misdiagnosis or may obscure important findings. Understanding artifacts is essential for correct interpretation of ultrasound examinations.

Many artifacts suggest the presence of structures not actually present. These include reverberation, refraction, and side lobes. Reverberation artifacts arise when the ultrasound signal reflects repeatedly between highly reflective interfaces that are usually, but not always, near the transducer (Fig. 1.27). Reverberations may also give the false impression of solid structures in areas where only fluid is present. Certain types of reverberation may be helpful because they allow the identification of a specific type of reflector, such as a surgical clip. Reverberation artifacts can usually be reduced or eliminated by changing the scanning angle or transducer placement to avoid the parallel interfaces that contribute to the artifact. Refraction causes bending of the sound beam so that targets not along the axis of the transducer are insonated. Their reflections are then detected and displayed in the image. This may cause structures to appear in the image that actually lie outside the volume the investigator assumes is being examined (see Fig. 1.7). Similarly, side lobes may produce confusing echoes that arise from sound beams that lie outside the main ultrasound beam (Fig. 1.28). These side lobe artifacts are of clinical importance because they may create the impression of structures or debris in fluid-filled structures (Fig. 1.29). Side lobes may also result in errors of measurement by reducing lateral resolution. As with most other artifacts, repositioning the transducer and its focal zone or using a different transducer will usually allow the differentiation of artifactual from true echoes. Artifacts may also remove real echoes from the display or obscure information, and important pathologic features may be missed. Shadowing results when there is a marked reduction in the intensity of ultrasound deep to a strong reflector or attenuator. Shadowing causes partial or complete loss of information due to attenuation of the sound by superficial structures. Another common cause of loss of image information is improper adjustment of system gain and TGC settings. Many low-level echoes

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FIG. 1.27  Reverberation Artifact.  Reverberation artifacts arise when the ultrasound signal reflects repeatedly between highly reflective interfaces near the transducer, resulting in delayed echo return to the transducer. This appears in the image as a series of regularly spaced echoes at increasing depth. The echo at depth 1 is produced by simple reflection from a strong interface. Echoes at levels 2, 3, and 4 are produced by multiple reflections between this interface and the surface (simulated image).

FIG. 1.29  Side Lobe Artifact.  Transverse image of the gallbladder reveals a bright internal echo (A) that suggests a band or septum within the gallbladder. This is a side lobe artifact related to the presence of a strong out-of-plane reflector (B) medial to the gallbladder. The low-level echoes in the dependent portion of the gallbladder (C) are also artifactual and are caused by the same phenomenon. Side lobe and slice thickness artifacts are of clinical importance because they may create the impression of debris in fluid-filled structures.

FIG. 1.28  Side Lobes.  Although most of the energy generated by a transducer is emitted in a beam along the central axis of the transducer (A), some energy is also emitted at the periphery of the primary beam (B and C). These are called side lobes and are lower in intensity than the primary beam. Side lobes may interact with strong reflectors that lie outside of the scan plane and produce artifacts that are displayed in the ultrasound image (see also Fig. 1.29).

are near the noise levels of the equipment, and considerable skill and experience are needed to adjust instrument settings to display the maximum information with the minimum noise. Poor scanning angles, inadequate penetration, and poor resolution may also result in loss of information. Careless selection of transducer frequency and lack of attention to the focal characteristics of

CHAPTER 1  Physics of Ultrasound

A

21

B

FIG. 1.30  Multipath Artifact.  (A) Mirror image of the uterus is created by reflection of sound from an interface produced by gas in the rectum. (B) Echoes reflected from the wall of an ovarian cyst create complex echo paths that delay return of echoes to the transducer. In both examples, the longer path of the reflected sound results in the display of echoes at a greater depth than they should normally appear. In (A) this results in an artifactual image of the uterus appearing in the location of the rectum. In (B) the effect is more subtle and more likely to cause misdiagnosis because the artifact suggests a mural nodule in what is actually a simple ovarian cyst.

the beam will cause loss of clinically important information from deep, low-amplitude reflectors and small targets. Ultrasound artifacts may alter the size, shape, and position of structures. For example, a multipath artifact is created when the path of the returning echo is not the one expected, resulting in display of the echo at an improper location in the image (Fig. 1.30).

Shadowing and Enhancement Although most artifacts degrade the ultrasound image and impede interpretation, two artifacts of clinical value are shadowing and enhancement. Again, shadowing results when an object (e.g., calculus) attenuates sound more rapidly than surrounding tissues. Enhancement occurs when an object (e.g., cyst) attenuates less than surrounding tissues. Failure of TGC applied to normal tissue to compensate properly for the attenuation of more highly attenuating (shadowing) or poorly attenuating (enhancing) structures produces the artifact (Fig. 1.31). Because attenuation increases with frequency, the effects of shadowing and enhancement are greater at higher than at lower frequencies. The conspicuity of shadowing and enhancement is reduced by excessive beam width, improper focal zone placement, and use of spatial compounding.

DOPPLER SONOGRAPHY Conventional B-mode ultrasound imaging uses pulse-echo transmission, detection, and display techniques. Brief pulses of ultrasound energy emitted by the transducer are reflected from acoustic interfaces within the body. Precise timing allows determination of the depth from which the echo originates. When pulsed wave ultrasound is reflected from an interface, the backscattered (reflected) signal contains amplitude, phase, and frequency information (Fig. 1.32). This information permits inference of the position, nature, and motion of the interface reflecting the pulse. B-mode ultrasound imaging uses only the amplitude information in the backscattered signal to generate the image, with differences in the strength of reflectors displayed in the image in varying shades of gray. Rapidly moving targets, such as red cells in the bloodstream, produce echoes of low

amplitude that are not usually displayed, resulting in a relatively anechoic pattern within the lumens of large vessels. Although gray-scale display relies on the amplitude of the backscattered ultrasound signal, additional information is present in the returning echoes that can be used to evaluate the motion of moving targets.16 When high-frequency sound impinges on a stationary interface, the reflected ultrasound has essentially the same frequency or wavelength as the transmitted sound. If the reflecting interface is moving with respect to the sound beam emitted from the transducer, however, there is a change in the frequency of the sound scattered by the moving object (Fig. 1.33). This change in frequency is directly proportional to the velocity of the reflecting interface relative to the transducer and is a result of the Doppler effect. The relationship of the returning ultrasound frequency to the velocity of the reflector is described by the Doppler equation, as follows: ∆F = (FR − FT ) = 2 ⋅ FT ⋅ v c The Doppler frequency shift is ΔF; FR is the frequency of sound reflected from the moving target; FT is the frequency of sound emitted from the transducer; v is the velocity of the target toward the transducer; and c is the velocity of sound in the medium. The Doppler frequency shift (ΔF) applies only if the target is moving directly toward or away from the transducer (Fig. 1.34A). In most clinical settings the direction of the ultrasound beam is seldom directly toward or away from the direction of flow, and the ultrasound beam usually approaches the moving target at an angle designated as the Doppler angle (Fig. 1.34B). In this case, ΔF is reduced in proportion to the cosine of this angle, as follows: ∆F = (FR − FT ) = 2 ⋅ FT ⋅ v ⋅ cos θ c where θ is the angle between the axis of flow and the incident ultrasound beam. If the Doppler angle can be measured, estimation of flow velocity is possible. Accurate estimation of target velocity requires precise measurement of both the Doppler frequency shift and the angle of insonation to the direction of

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Uncorrected

Gain compensated

–10 dB

–25 dB

+10 dB

+10–25 = –15 db

–20 dB

–30 dB

+20 dB

+10–35 = –15 db

A –30 dB –0 dB

–10 + 10 dB

C

–0 dB

–20 + 20 dB

B –40 dB

+30 dB

+30–5 = –15 dB

Gain compensated

+10–3 = +7 dB

+20–13 = +7 dB

FIG. 1.31  Shadowing and Enhancement.  (A) Uncorrected image of a shadowing breast mass shows that the mass attenuates 25 dB, 15 dB more than the surrounding normal tissue, which attenuates only 10 dB. (B) Application of appropriate time gain compensation (TGC) results in proper display of the normal breast tissue. However, because of the increased attenuation of the mass, a shadow results. (C) Similarly, the cyst attenuates 7 dB less than the normal tissue, and TGC correction for normal tissue results in overamplification of the signals deep to the cyst, producing enhancement of these tissues.

target movement. As the Doppler angle (θ) approaches 90 degrees, the cosine of θ approaches 0. At an angle of 90 degrees, there is no relative movement of the target toward or away from the transducer, and no Doppler frequency shift is detected (Fig. 1.35). Because the cosine of the Doppler angle changes rapidly for angles more than 60 degrees, accurate angle correction requires that Doppler measurements be made at angles of less than 60 degrees. Above 60 degrees, relatively small changes in the Doppler angle are associated with large changes in cosθ, and therefore a small error in estimation of the Doppler angle may result in a large error in the estimation of velocity. These considerations are important in using both duplex and color Doppler instruments. Optimal imaging of the vessel wall is obtained when

the axis of the transducer is perpendicular to the wall, whereas maximal Doppler frequency differences are obtained when the transducer axis and the direction of flow are at a relatively small angle. In peripheral vascular applications, it is highly desirable that measured Doppler frequencies be corrected for the Doppler angle to provide velocity measurement. This allows comparison of data from systems using different Doppler frequencies and eliminates error in interpretation of frequency data obtained at different Doppler angles. For abdominal applications, angle-corrected velocity measurements are encouraged, although qualitative assessments of flow are often made using only the Doppler frequency shift data.

CHAPTER 1  Physics of Ultrasound

FT

FIG. 1.32  Backscattered Information.  The backscattered ultrasound signal contains amplitude, phase, and frequency information. Signals B and C differ in amplitude but have the same frequency. Amplitude differences are used to generate B-mode images. Signals A and B differ in frequency but have similar amplitudes. Such frequency differences are the basis of Doppler ultrasound.

FR

v ∆F = (FR − FT) = 2 • FT • v c

A

A

Stationary target: (FR − FT) = 0

B

Target motion toward transducer: (FR − FT) > 0 FT

C

23

FR

θ Target motion away from transducer: (FR − FT) < 0

FIG. 1.33  Doppler Effect.  (A) Stationary target. If the reflecting interface is stationary, the backscattered ultrasound has the same frequency or wavelength as the transmitted sound, and there is no difference in the transmitted frequency (FT) and the reflected frequency (FR). (B) and (C) Moving targets. If the reflecting interface is moving with respect to the sound beam emitted from the transducer, there is a change in the frequency of the sound scattered by the moving object. When the interface moves toward the transducer (B), the difference in reflected and transmitted frequencies is greater than zero. When the target is moving away from the transducer (C), this difference is less than zero. The Doppler equation is used to relate this change in frequency to the velocity of the moving object.

Doppler Signal Processing and Display Several options exist for the processing of ΔF, the Doppler frequency shift, to provide useful information regarding the direction and velocity of blood. Doppler frequency shifts encountered clinically are in the audible range. This audible signal may be analyzed by ear and, with training, the operator can identify many flow characteristics. More often, the Doppler shift data are displayed in graphic form as a time-varying plot of the frequency

v

B

∆F = (FR − FT) = 2 • FT • v • cos θ c

FIG. 1.34  Doppler Equations.  The Doppler equation describes the relationship of the Doppler frequency shift to target velocity. (A) In its simplest form, it is assumed that the direction of the ultrasound beam is parallel to the direction of movement of the target. This situation is unusual in clinical practice. More often, the ultrasound impinges on the vessel at angle θ. (B) In this case the Doppler frequency shift detected is reduced in proportion to the cosine of θ. ΔF, Frequency shift; FR, reflected frequency; FT, transmitted frequency; v, velocity.

spectrum of the returning signal. A fast Fourier transformation is used to perform the frequency analysis. The resulting Doppler frequency spectrum displays the following (Fig. 1.36): • Variation with time of the Doppler frequencies present in the volume sampled

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θ = 60° cos θ = 0.5 ∆F = 0.5

Physics θ = 90° cos θ = 0.0 ∆F = 0.0

θ = 0° cos θ = 1.0 ∆F = 1.0

amplitude of each frequency component is displayed in gray scale as part of the spectrum. The presence of a large number of different frequencies at a given point in the cardiac cycle results in spectral broadening. In color Doppler imaging systems, a representation of the Doppler frequency shift is displayed as a feature of the image itself (see Fig. 1.36). In addition to the detection of Doppler frequency shift data from each pixel in the image, these systems may also provide range-gated pulsed wave Doppler with spectral analysis for display of Doppler data.

Doppler Instrumentation

FIG. 1.35  Effect of Doppler Angle on Frequency Shift.  At an angle of 60 degrees, the detected frequency shift (ΔF) detected by the transducer is only 50% of the shift detected at an angle of 0 degrees. At 90 degrees, there is no relative movement of the target toward or away from the transducer, and no frequency shift is detected. The detected Doppler frequency shift is reduced in proportion to the cosine of the Doppler angle. Because the cosine of the angle changes rapidly at angles above 60 degrees, the use of Doppler angles of less than 60 degrees is recommended in making velocity estimates.

B

A

FIG. 1.36  Doppler Display.  (A) Doppler frequency spectrum waveform shows changes in flow velocity and direction by vertical deflections of the waveform above and below the baseline. The width of the spectral waveform (spectral broadening) is determined by the range of frequencies present at any instant in time (arrow). A brightness (gray) scale is used to indicate the amplitude of each frequency component. (B) Color Doppler imaging. Amplitude data from stationary targets provide the basis for the B-mode image. Signal phase provides information about the presence and direction of motion, and changes in frequency relate to the velocity of the target. Backscattered signals from red blood cells are displayed in color as a function of their motion toward or away from the transducer, and the degree of the saturation of the color is used to indicate the frequency shift from moving red cells.

• The envelope of the spectrum, representing the maximum frequencies present at any given point in time • The width of the spectrum at any point, indicating the range of frequencies present The amplitude of the Doppler signal is related to the number of targets moving at a given velocity. In many instruments the

In contrast to A-mode, M-mode, and B-mode gray-scale ultrasonography, which display the information from tissue interfaces, Doppler ultrasound instruments are optimized to display flow information. The simplest Doppler devices use continuous wave (CW) Doppler rather than pulsed wave ultrasound, using two transducers that transmit and receive ultrasound continuously. The transmit and receive beams overlap in a sensitive volume at some distance from the transducer face (Fig. 1.37A). Although direction of flow can be determined with CW Doppler, these devices do not allow discrimination of motion coming from various depths, and the source of the signal being detected is difficult, if not impossible, to ascertain with certainty. Inexpensive and portable, CW Doppler instruments are used primarily at the bedside or intraoperatively to confirm the presence of flow in superficial vessels. Because of the limitations of CW systems, most applications use range-gated, pulsed wave Doppler. Rather than a continuous wave of ultrasound emission, pulsed wave Doppler devices emit brief pulses of ultrasound energy (see Fig. 1.37B). Using pulses of sound permits use of the time interval between the transmission of a pulse and the return of the echo as a means of determining the depth from which the Doppler shift arises. The principles are similar to the echo-ranging principles used for imaging (see Fig. 1.4). In a pulsed wave Doppler system the sensitive volume from which flow data are sampled can be controlled in terms of shape, depth, and position. When pulsed wave Doppler is combined with a 2-D, real-time, B-mode imager in the form of a duplex scanner, the position of the Doppler sample can be precisely controlled and monitored. In color Doppler imaging (Fig. 1.38A), frequency shift information determined from Doppler measurements is displayed as a feature of the image itself.17 Stationary or slowly moving targets provide the basis for the B-mode image. Signal phase provides information about the presence and direction of motion, and changes in echo signal frequency relate to the velocity of the target. Backscattered signals from red blood cells are displayed in color as a function of their motion toward or away from the transducer, and the degree of the saturation of the color is used to indicate the relative frequency shift produced by the moving red cells. Color Doppler flow imaging (CDFI) expands conventional duplex sonography by providing additional capabilities. The use of color saturation to display variations in Doppler shift frequency allows an estimation of relative velocity from the image alone, provided that variations in the Doppler angle are noted. The

CHAPTER 1  Physics of Ultrasound

A

25

B

FIG. 1.37  Continuous Wave and Pulsed Wave Doppler.  (A) Continuous wave (CW) Doppler uses separate transmit and receive crystals that continuously transmit and receive ultrasound. Although able to detect the presence and direction of flow, CW devices are unable to distinguish signals arising from vessels at different depths (green-shaded area). (B) Using the principle of ultrasound ranging (see Fig. 1.4), pulsed wave Doppler permits the sampling of flow data from selected depths by processing only the signals that return to the transducer after precisely timed intervals. The operator is able to control the position of the sample volume and, in duplex systems, to view the location from which the Doppler data are obtained.

Limitations of Color Doppler Flow Imaging

Advantages of Power Doppler

Angle dependence Aliasing Inability to display entire Doppler spectrum in the image Artifacts caused by noise

No aliasing Much less angle dependence Noise: a homogeneous background color Increased sensitivity for flow detection

display of flow throughout the image field allows the position and orientation of the vessel of interest to be observed at all times. The display of spatial information with respect to velocity is ideal for display of small, localized areas of turbulence within a vessel, which provide clues to stenosis or irregularity of the vessel wall caused by atheroma, trauma, or other disease. Flow within the vessel is observed at all points, and stenotic jets and focal areas of turbulence are displayed that might be overlooked with duplex instrumentation. The contrast of flow within the vessel lumen permits visualization of small vessels that are not visible when using conventional imagers and enhances the visibility of wall irregularity. CDFI aids in determination of the direction of flow and measurement of the Doppler angle.

Power Doppler An alternative to the display of frequency information with color Doppler imaging is to use a color map that displays the integrated power of the Doppler signal instead of its mean frequency shift18 (see Fig. 1.38B). Because frequency shift data are not displayed, there is no aliasing. The image does not provide information related to flow direction or velocity, and power Doppler imaging is much less angle dependent than frequency-based color Doppler display. In contrast to color Doppler, where noise may appear in the image as any color, power Doppler permits noise to be assigned to a homogeneous background color that does not greatly interfere with the image. This results in a significant increase in the usable

dynamic range of the scanner, permitting higher effective gain settings and increased sensitivity for flow detection (Fig. 1.39).

Interpretation of the Doppler Spectrum Doppler data components that must be evaluated both in spectral display and in color Doppler imaging include the Doppler shift frequency and amplitude, the Doppler angle, the spatial distribution of frequencies across the vessel, and the temporal variation of the signal. Because the Doppler signal itself has no anatomic significance, the examiner must interpret the Doppler signal and then determine its relevance in the context of the image. The detection of a Doppler frequency shift indicates movement of the target, which in most applications is related to the presence of flow. The sign of the frequency shift (positive or negative) indicates the direction of flow relative to the transducer. Vessel stenosis is typically associated with large Doppler frequency shifts in both systole and diastole at the site of greatest narrowing, with turbulent flow in poststenotic regions. In peripheral vessels, analysis of the Doppler changes allows accurate prediction of the degree of vessel narrowing. Information related to the resistance to flow in the distal vascular tree can be obtained by analysis of changes of blood velocity with time, as shown in the Doppler spectral display. Doppler imaging can provide information about blood flow in both large and small vessels. Small vessel impedance is reflected in the Doppler spectral waveform of afferent vessels.

26

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A

B

FIG. 1.38  Color Flow and Power Doppler.  (A) Color flow Doppler imaging uses a color map to display information based on the detection of frequency shifts from moving targets. Noise in this form of display appears across the entire frequency spectrum and limits sensitivity. (B) Power Doppler uses a color map to show the distribution of the power or amplitude of the Doppler signal. Flow direction and velocity information are not provided, but noise is reduced, allowing higher gain settings and improved sensitivity for flow detection.

A

B FIG. 1.39  Frequency and Power Mode Color Mapping.  (A) Conventional color Doppler uses the color map to show differences in flow direction and Doppler frequency shift. Because noise appears over the entire frequency spectrum, gain levels are limited to those that do not introduce excessive noise. (B) Power Doppler color map, in contrast, indicates the amplitude of the Doppler signal. Because most noise is of low amplitude, it is possible to map this to colors near the background. This permits the use of high gain settings that offer significant improvements over conventional color Doppler in flow detection.

CHAPTER 1  Physics of Ultrasound

27

FIG. 1.40  Impedance.  High-resistance waveform in brachial artery (A), produced by inflating forearm blood pressure cuff to a pressure above the systolic blood pressure. As a result of high peripheral resistance, there is low systolic amplitude and reversed diastolic flow. Low-resistance waveform in peripheral vascular bed (B), caused by vasodilation stimulated by the prior ischemia. Immediately after release of 3 minutes of occluding pressure, the Doppler waveform showed increased amplitude and rapid antegrade flow throughout diastole.

Fig. 1.40 provides a graphic example of the changes in the Doppler spectral waveform resulting from physiologic changes in the resistance of the vascular bed supplied by a normal brachial artery. A blood pressure cuff has been inflated to above systolic pressure to occlude the distal branches supplied by the brachial artery. This occlusion causes reduced systolic amplitude and cessation of diastolic flow, resulting in a waveform different than that found in the normal resting state. During the period of ischemia induced by pressure cuff occlusion of the forearm vessels, vasodilation has occurred. Immediately after release of the occluding pressure the Doppler waveform reflects a low-resistance peripheral vascular bed with increased systolic amplitude and rapid flow throughout diastole, typical for vasodilation. Doppler indices include the systolic-to-diastolic ratio (S/D ratio), resistive index (RI), and pulsatility index (PI) (Fig. 1.41). These compare blood flow in systole and diastole, show resistance to flow in the peripheral vascular bed, and help evaluate the perfusion of tumors, renal transplants, the placenta, and other organs. With Doppler ultrasound, it is therefore possible to identify vessels, determine the direction of blood flow, evaluate narrowing or occlusion, and characterize blood flow to organs and tumors. Analysis of the Doppler shift frequency with time can be used to infer both proximal stenosis and changes in distal vascular impedance. Most work using pulsed wave Doppler imaging has emphasized the detection of stenosis, thrombosis, and flow disturbances in major peripheral arteries and veins. In these applications, measurement of peak systolic and end diastolic

FIG. 1.41  Doppler Indices. Doppler flow indices used to characterize peripheral resistance are based on the peak systolic frequency or velocity (A), the minimum or end diastolic frequency or velocity (B), and the mean frequency or velocity (M). The most frequently used indices are the systolic-to-diastolic ratio (A/B); resistive index [(A-B)/A]; and pulsatility index [(A-B)/M]. In calculation of the pulsatility index, the minimum diastolic velocity or frequency is used; calculation of the systolic-to-diastolic ratio and resistive index use the end diastolic value.

frequency or velocity, analysis of the Doppler spectrum, and calculation of certain frequency or velocity ratios have been the basis of analysis. Changes in the spectral waveform measured by indices comparing flow in systole and diastole indicate the resistance of the vascular bed supplied by the vessel and the changes resulting from a variety of pathologic conditions.

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Changes in Doppler indices from normal may help in the early identification of rejection of transplanted organs, parenchymal dysfunction, and malignancy. Although useful, these measurements are influenced not only by the resistance to flow in peripheral vessels, but also by heart rate, blood pressure, vessel wall length and elasticity, extrinsic organ compression, and other factors.

Interpretation of Color Doppler Although the graphic presentation of color Doppler imaging suggests that interpretation is made easier, the complexity of the color Doppler image actually makes this a more demanding image to evaluate than the simple Doppler spectrum. Nevertheless, color Doppler imaging has important advantages over pulsed wave duplex Doppler imaging, in which flow data are obtained only from a small portion of the area being imaged. To be confident that a conventional Doppler study has achieved reasonable sensitivity and specificity in detection of flow disturbances, a methodical search and sampling of multiple sites within the field of interest must be performed. In contrast, CDFI devices permit simultaneous sampling of multiple sites and are less susceptible to this error. Although color Doppler can indicate the presence of blood flow, misinterpretation of color Doppler images may result in important errors. Each color pixel displays a representation of the Doppler frequency shift detected at that point. The frequency shift displayed is not the peak frequency present at sampling but rather a weighted mean frequency that attempts to account for the range of frequencies and their relative amplitudes at sampling. Manufacturers use different methods to derive the weighted mean frequency displayed in their systems. In addition, the pulse repetition frequency (PRF) and the color map selected to display

A

the detected range of frequencies affect the color displayed. The color assigned to each Doppler pixel is determined by the Doppler frequency shift (which in turn is determined by target velocity and Doppler angle), the PRF, and the color map selected for display; therefore the interpretation of a color Doppler image must consider each of these variables. Although most manufacturers provide on-screen indications suggesting a relationship between the color displayed and flow velocity, this is misleading because color Doppler does not show velocity and only indicates the weighted mean frequency shift measured in the vessel; without correction for the effect of the Doppler angle, velocity cannot be estimated (Fig. 1.42). Because the frequency shift at a given point is a function of velocity and the Doppler angle, depending on the frequency shift present in a given pixel and the PRF, any velocity may be represented by any color, and under certain circumstances, low-velocity flow may not be shown at all. As with spectral Doppler, aliasing is determined by PRF. With color Doppler, aliasing causes frequencies greater than twice the PRF to “wrap around” and to be displayed in the opposite colors of the color map. Inexperienced users tend to associate color Doppler aliasing with elevated velocity, but even low velocities may show marked aliasing if PRF is sufficiently low. As PRF is increased, aliasing of high Doppler frequency shifts is reduced; however, low-frequency shifts may be eliminated from the display, resulting in diagnostic error (Fig. 1.43).

Other Technical Considerations Although many problems and artifacts associated with B-mode imaging (e.g., shadowing) are encountered with Doppler sonography, the detection and display of frequency information related to moving targets present additional technical considerations. It is important to understand the source of these artifacts and

B

FIG. 1.42  Color Doppler.  Each color pixel in a color Doppler image represents the Doppler frequency shift at that point, and it cannot be used to estimate velocity. Even though the points A and B have similar color values and therefore similar Doppler frequencies, the velocity at A is much higher than at B because of the large Doppler angle at A compared to B. The velocity represented by a given Doppler frequency increases in proportion to the Doppler angle.

CHAPTER 1  Physics of Ultrasound

A (PRF = 700 Hz)

B (PRF = 4500 Hz)

FIG. 1.43  Pulse Repetition Frequency (PRF).  Depending on the color map selected, velocity of the target, Doppler velocity may appear as any color with color Doppler. (A) and (B) are sonograms of identical vessels. (A) PRF is 700 Hz, of the higher Doppler frequency shifts in the carotid artery but permits the identification of relatively slow flow in the 4500 Hz, eliminating aliasing in the artery but also suppressing the display of the low Doppler frequencies in the internal

their influence on the interpretation of the flow measurements obtained in clinical practice.

Doppler Frequency A primary objective of the Doppler examination is the accurate measurement of characteristics of flow within a vascular structure. The moving red blood cells that serve as the primary source of the Doppler signal act as point scatterers of ultrasound rather than specular reflectors. This interaction results in the intensity of the scattered sound varying in proportion to the fourth power of the frequency, which is important in selecting the Doppler frequency for a given examination. As the transducer frequency increases, Doppler sensitivity improves, but attenuation by tissue also increases, resulting in diminished penetration. Careful balancing of the requirements for sensitivity and penetration is an important responsibility of the operator during a Doppler examination. Because many abdominal vessels lie several centimeters beneath the surface, Doppler frequencies in the range of 3 to 3.5 MHz are usually required to permit adequate penetration. Wall Filters Doppler instruments detect motion not only from blood flow but also from adjacent structures. To eliminate these low-frequency signals from the display, most instruments use high pass filters, or “wall” filters, which remove signals that fall below a given frequency limit. Although effective in eliminating low-frequency noise, these filters may also remove signals from low-velocity blood flow (Fig. 1.44). In certain clinical situations the measurement of these slower flow velocities is of clinical importance, and the improper selection of the wall filter may result in serious errors of interpretation. For example, low-velocity venous flow may not be detected if an improper filter is used, and low-velocity diastolic flow in certain arteries may also be eliminated from the display, resulting in errors in the calculation of Doppler indices, such as the systolic-to-diastolic ratio or resistive index. In general, the filter should be kept at the lowest practical level, usually 50 to 100 Hz. Spectral Broadening Spectral broadening refers to the presence of a large range of flow velocities at a given point in the pulse cycle and, by indicating

29

angle, and PRF, a given which results in aliasing jugular vein. (B) PRF is jugular vein.

Major Sources of Doppler Imaging Artifacts DOPPLER FREQUENCY Higher frequencies lead to more tissue attenuation Wall filters remove signals from low-velocity blood flow INCREASE IN SPECTRAL BROADENING Excessive system gain or changes in dynamic range of the gray-scale display Excessively large sample volume Sample volume too near the vessel wall INCREASE IN ALIASING Decrease in pulse repetition frequency (PRF) Decrease in Doppler angle Higher Doppler frequency transducer DOPPLER ANGLE Relatively inaccurate above 60 degrees SAMPLE VOLUME SIZE Large sample volumes increase vessel wall noise

turbulence, is an important criterion of high-grade vessel narrowing. Excessive system gain or changes in the dynamic range of the gray-scale display of the Doppler spectrum may suggest spectral broadening; opposite settings may mask broadening of the Doppler spectrum, causing diagnostic inaccuracy. Spectral broadening may also be produced by the selection of an excessively large sample volume or by the placement of the sample volume too near the vessel wall, where slower velocities are present (Fig. 1.45).

Aliasing Aliasing is an artifact arising from ambiguity in the measurement of high Doppler frequency shifts. To ensure that samples originate from only a selected depth when using a pulsed wave Doppler system, it is necessary to wait for the echo from the area of interest before transmitting the next pulse. This limits the rate with which pulses can be generated, a lower PRF being required for greater depth. The PRF also determines the maximum depth from which unambiguous data can be obtained. If PRF is less than twice the maximum frequency shift produced by movement

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A

B

FIG. 1.44  Wall Filters.  Wall filters are used to eliminate low-frequency noise from the Doppler display, but high wall filter settings may result in interpretation errors. Here the effect on the display of low-velocity flow is shown with wall filter settings of (A) 100 Hz and (B) 400 Hz. In general, wall filters should be kept at the lowest practical level, usually in the range of 50 to 100 Hz.

of the target (Nyquist limit), aliasing results (Fig. 1.46). When PRF is less than twice the frequency shift being detected, lower frequency shifts than are actually present are displayed. Because of the need for lower PRFs to reach deep vessels, signals from deep abdominal arteries are prone to aliasing if high velocities are present. In practice, aliasing is usually readily recognized. Aliasing can be reduced by increasing the PRF, by increasing the Doppler angle (thereby decreasing the frequency shift), or by using a lower-frequency Doppler transducer.

Doppler Angle When making Doppler measurement of velocity, it is necessary to correct for the Doppler angle. The accuracy of a velocity estimate obtained with Doppler is only as great as the accuracy of the measurement of the Doppler angle. This is particularly true as the Doppler angle exceeds 60 degrees. In general, the Doppler angle is best kept at 60 degrees or less because small changes in the Doppler angle above 60 degrees result in substantial changes in the calculated velocity. Therefore measurement inaccuracies result in much greater errors in velocity estimates than do similar errors at lower Doppler angles. Angle correction is not required for the measurement of Doppler indices such as the resistive index, because these measurements are based only on the relationship of the systolic and diastolic amplitudes. Sample Volume Size With pulsed wave Doppler systems, the length of the Doppler sample volume can be controlled by the operator, and the width is determined by the beam profile. Analysis of Doppler signals requires that the sample volume be adjusted to exclude as much of the unwanted clutter as possible from near the vessel walls.

Doppler Gain As with imaging, proper gain settings are essential to achieving accurate and reproducible Doppler measurements. Excessive Doppler gain results in noise appearing at all frequencies and may result in overestimation of velocity. Conversely, insufficient gain may result in underestimation of peak velocity (Fig. 1.47). A consistent approach to setting Doppler gain should be used. After placing the sample volume in the vessel, the Doppler gain should be increased to a level where noise is visible in the image, then gradually reduced to the point at which the noise first disappears completely.

OPERATING MODES: CLINICAL IMPLICATIONS Ultrasound devices may operate in several modes, including real-time, color Doppler, spectral Doppler, and M-mode imaging. Imaging is produced in a scanned mode of operation. In scanned modes, pulses of ultrasound from the transducer are directed down lines of sight that are moved or steered in sequence to generate an image. This means that the number of ultrasound pulses arriving at a given point in the patient over a given interval is relatively small, and relatively little energy is deposited at any given location. In contrast, spectral Doppler imaging is an unscanned mode of operation in which multiple ultrasound pulses are sent in repetition along a line to collect the Doppler data. In this mode the beam is stationary, resulting in considerably greater potential for heating than in imaging modes. For imaging, PRFs are usually a few thousand hertz with very short pulses. Longer pulse durations are used with Doppler than with other imaging

CHAPTER 1  Physics of Ultrasound

31

With current devices operating in imaging modes, concerns about bioeffects are minimal because intensities sufficient to produce measurable heating are seldom used. With Doppler ultrasound, the potential for thermal effects is greater. Preliminary measurements on commercially available instruments suggest that at least some of these instruments are capable of producing temperature rises of greater than 1°C at soft tissue/bone interfaces, if the focal zone of the transducer is held stationary. Care is therefore warranted when Doppler measurements are obtained at or near soft tissue/bone interfaces, as in the second and third trimester of pregnancy. These applications require thoughtful application of the principle of ALARA (as low as reasonably achievable). Under ALARA the user should use the lowest possible acoustic exposure to obtain the necessary diagnostic information.

Bioeffects and User Concerns

FIG. 1.45  Spectral Broadening.  The range of velocities detected at a given time in the pulse cycle is reflected in the Doppler spectrum as spectral broadening. (A) Normal spectrum. Spectral broadening may arise from turbulent flow in association with vessel stenosis. (B) and (C) Artifactual spectral broadening. This may be produced by improper positioning of the sample volume near the vessel wall, use of (B) an excessively large sample volume, or (C) an excessive system gain.

modes. In addition, to avoid aliasing and other artifacts with Doppler imaging, it is often necessary to use higher PRFs than with other imaging applications. Longer pulse duration and higher PRF result in higher duty factors for Doppler modes of operation and increase the amount of energy introduced in scanning. Color Doppler, although a scanned mode, produces exposure conditions between those of real-time and Doppler imaging because color Doppler devices tend to send more pulses down each scan line and may use longer pulse durations than imaging devices. Clearly, every user needs to be aware that switching from an imaging to a Doppler mode changes the exposure conditions and the potential for biologic effects (bioeffects).

Although users of ultrasound need to be aware of bioeffects concerns, another key factor to consider in the safe use of ultrasound is the user. The knowledge and skill of the user are major determinants of the risk-to-benefit implications of the use of ultrasound in a specific clinical situation. For example, an unrealistic emphasis on risks may discourage an appropriate use of ultrasound, resulting in harm to the patient by preventing the acquisition of useful information or by subjecting the patient to another, more hazardous examination. The skill and experience of the individual performing and interpreting the examination are likely to have a major impact on the overall benefit of the examination. In view of the rapid growth of ultrasound and its proliferation into the hands of minimally trained clinicians, many more patients are likely to be harmed by misdiagnosis resulting from improper indications, poor examination technique, and errors in interpretation than from bioeffects. Misdiagnosis (e.g., of ectopic pregnancy) and failure to diagnose a clinically important anomaly are real dangers, and poorly trained users may be the greatest current hazard of diagnostic ultrasound. Understanding bioeffects is essential for the prudent use of diagnostic ultrasound and is important in ensuring that the excellent risk-to-benefit performance of diagnostic ultrasound is preserved. All users of ultrasound should be prudent, understanding as fully as possible the potential risks and obvious benefits of ultrasound examinations, as well as those of alternate diagnostic methods. With this information, operators can monitor exposure conditions and implement the principle of ALARA to keep patient (and in obstetric imaging, the fetal) exposure as low as possible while fulfilling diagnostic objectives.

THERAPEUTIC APPLICATIONS: HIGHINTENSITY FOCUSED ULTRASOUND Although the primary medical application of ultrasound has been for diagnosis, therapeutic applications are developing rapidly, particularly the use of high-intensity focused ultrasound (HIFU). HIFU is based on three important capabilities of ultrasound: (1) focusing the ultrasound beam to produce highly localized energy deposition, (2) controlling the location and size of the focal zone, and (3) using intensities sufficient to destroy tissue at the focal

32

Physics

PART I

A

C

B

D

FIG. 1.46  Aliasing.  Pulse repetition frequency (PRF) determines the sampling rate of a given Doppler frequency. (A) If PRF (arrows) is sufficient, the sampled waveform (orange curve) will accurately estimate the frequency being sampled (yellow curve). (B) If PRF is less than half the frequency being measured, undersampling will result in a lower frequency shift being displayed (orange curve). (C) In a clinical setting, aliasing appears in the spectral display as a “wraparound” of the higher frequencies to display below the baseline. (D) In color Doppler display, aliasing results in a wraparound of the frequency color map from one flow direction to the opposite direction, passing through a transition of unsaturated color. The velocity throughout the vessel is constant, but aliasing appears only in portions of the vessel because of the effect of the Doppler angle on the Doppler frequency shift. As the angle increases, the Doppler frequency shift decreases, and aliasing is no longer seen.

zone. This has led to an interest in HIFU as a means of destroying noninvasive tumor and controlling bleeding and cardiac conduction anomalies. HIFU exploits thermal (heating of tissues) and mechanical (cavitation) bioeffect mechanisms. As ultrasound passes through tissue, attenuation occurs through scattering and absorption. Scattering of ultrasound results in the return of some of the transmitted energy to the transducer, where it is detected and used to produce an image, or Doppler display. The remaining energy is transmitted to the molecules in the acoustic field and produces heating. At the spatial peak temporal average (SPTA), intensities of 50 to 500 mW/cm2 used for imaging and Doppler, heating is minimal, and no observable bioeffects related to tissue heating in humans have yet been documented with clinical devices. With higher intensities, however, tissue heating sufficient to destroy tissue may be achieved. Using HIFU at 1 to 3 MHz, focal peak intensities of 5000 to 20,000 W/cm2 may be achieved. This energy can be delivered to a small point several millimeters in

size, producing rapid temperature elevation and resulting in tissue coagulation, with little damage to adjacent tissues (Fig. 1.48). The destruction of tissue is a function of the temperature reached and the duration of the temperature elevation. In general, elevation of tissue to a temperature of 60°C for 1 second is sufficient to produce coagulation necrosis. Because of its ability to produce highly localized tissue destruction, HIFU has been investigated as a tool for noninvasive or minimally invasive treatment of bleeding sites, uterine fibroids, and tumors in the prostate, liver, and breast.19,20 As with diagnostic ultrasound, HIFU is limited by the presence of gas or bone interposed between the transducer and the target tissue. The reflection of high-energy ultrasound from strong interfaces produced by bowel gas, aerated lung, or bone may result in tissue heating along the reflected path of the sound, producing unintended tissue damage. Major challenges with HIFU include image guidance and accurate monitoring of therapy as it is being delivered. Magnetic

CHAPTER 1  Physics of Ultrasound

33

resonance imaging (MRI) provides a means of monitoring temperature elevation during treatment, which is not possible with ultrasound. Guidance of therapy may be done with ultrasound or MRI, with ultrasound guidance having the advantage of verification of the acoustic window and sound path for the delivery of HIFU. A

Excess gain PSV = 75 cm/sec

B

Proper gain PSV = 60 cm/sec

C

Insufficent gain PSV = 50 cm/sec

FIG. 1.47  Doppler Gain.  Accurate estimation of velocity requires proper Doppler gain adjustment. Excessive gain will cause an overestimation of peak velocity (A), and insufficient gain will result in underestimation of velocity (C). To adjust gain properly, the sample volume and Doppler angle are first set at the sample site. The gain is turned up until noise appears in the background (A), then is gradually reduced just to the point where the background noise disappears from the image (B). PSV, Peak systolic velocity.

FIG. 1.48  High-Intensity Focused Ultrasound (HIFU).  Local tissue destruction by heating may be achieved using HIFU delivered with focal peak intensities of several thousand W/cm2. Tissue destruction can be confined to a small area a few millimeters in size without injury to adjacent tissues. HIFU is a promising tool for minimally invasive treatment of bleeding sites, uterine fibroids, and tumors in the prostate, liver, and breast.

REFERENCES 1. Medical diagnostic ultrasound instrumentation and clinical interpretation. Report of the Ultrasonography Task Force. Council on Scientific Affairs. JAMA. 1991;265(9):1155-1159. 2. Chivers RC, Parry RJ. Ultrasonic velocity and attenuation in mammalian tissues. J Acoust Soc Am. 1978;63(3):940-953. 3. Goss SA, Johnston RL, Dunn F. Comprehensive compilation of empirical ultrasonic properties of mammalian tissues. J Acoust Soc Am. 1978;64(2):423-457. 4. Merritt CR, Kremkau FW, Hobbins JC. Diagnostic ultrasound: bioeffects and safety. Ultrasound Obstet Gynecol. 1992;2(5):366-374. 5. Curie J, Curie P. Développement par compression de l’électricité polaire dans les cristaux hémièdres à faces inclinées (Development, via compression, of electric polarization in hemihedral crystals with inclined faces). Bull Soc Minerol Fr. 1880;3:90-93. 6. Krishan S, Li PC, O’Donnell M. Adaptive compensation of phase and magnitude aberrations. IEEE Trans Ultrasonics Fer Freq Control. 1996;43. 7. Merritt CR. Technology update. Radiol Clin North Am. 2001;39(3):385-397. 8. Wells PN, Liang HD. Medical ultrasound: imaging of soft tissue strain and elasticity. J R Soc Interface. 2011;8(64):1521-1549. 9. Krouskop TA, Wheeler TM, Kallel F, et al. Elastic moduli of breast and prostate tissues under compression. Ultrason Imaging. 1998;20(4):260-274. 10. Ophir J, Cespedes I, Ponnekanti H, et al. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging. 1991; 13(2):111-134. 11. Shiina T, Nightingale KR, Palmeri ML, et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 1: basic principles and terminology. Ultrasound Med Biol. 2015;41(5):1126-1147. 12. Madsen EL, Sathoff HJ, Zagzebski JA. Ultrasonic shear wave properties of soft tissues and tissuelike materials. J Acoust Soc Am. 1983;74(5):1346-1355. 13. Sarvazyan AP, Rudenko OV, Swanson SD, et al. Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. Ultrasound Med Biol. 1998;24(9):1419-1435. 14. Ferraioli G, Parekh P, Levitov AB, Filice C. Shear wave elastography for evaluation of liver fibrosis. J Ultrasound Med. 2014;33(2):197-203. 15. Yoneda M, Suzuki K, Kato S, et al. Nonalcoholic fatty liver disease: US-based acoustic radiation force impulse elastography. Radiology. 2010;256(2):640-647. 16. Merritt CR. Doppler US: the basics. Radiographics. 1991;11(1):109-119. 17. Merritt CR. Doppler color flow imaging. J Clin Ultrasound. 1987;15(9):591-597. 18. Rubin JM, Bude RO, Carson PL, et al. Power Doppler US: a potentially useful alternative to mean frequency-based color Doppler US. Radiology. 1994; 190(3):853-856. 19. Dubinsky TJ, Cuevas C, Dighe MK, et al. High-intensity focused ultrasound: current potential and oncologic applications. AJR Am J Roentgenol. 2008; 190(1):191-199. 20. Kennedy JE, Ter Haar GR, Cranston D. High intensity focused ultrasound: surgery of the future? Br J Radiol. 2003;76(909):590-599.

CHAPTER

2

 

Biologic Effects and Safety J. Brian Fowlkes and Christy K. Holland

SUMMARY OF KEY POINTS • Clinical ultrasound has been found to be an effective imaging modality with an excellent safety profile when used appropriately. • Ultrasound can produce physical effects, which should be understood as part of the benefit-versus-risk assessment as with any medical procedure. • The thermal index (TI) and mechanical index (MI) provide feedback to the user and should be minimized while

obtaining the requisite medical benefit from the ultrasound examination. • Ultrasound exposures during clinical, research, and educational examinations should be as low as reasonably achievable (ALARA). • Users of ultrasound should be appropriately trained and familiar with the equipment operation and controls that affect ultrasound exposure.

CHAPTER OUTLINE REGULATION OF ULTRASOUND OUTPUT PHYSICAL EFFECTS OF SOUND THERMAL EFFECTS Ultrasound Produces Heat Factors Controlling Tissue Heating Spatial Focusing Temporal Considerations Tissue Type Bone Heating Soft Tissue Heating Hyperthermia and Ultrasound Safety Thermal Index Homogeneous Tissue Model (Soft Tissue)

Tissue Model With Bone at the Focus (Fetal Applications) Tissue Model With Bone at the Surface (Transcranial Applications) Estimate of Thermal Effects Summary Statement on Thermal Effects EFFECTS OF ACOUSTIC CAVITATION Potential Sources for Bioeffects Sonochemistry Evidence of Cavitation From Lithotripters Bioeffects in Lung and Intestine Ultrasound Contrast Agents

U

ltrasound has provided a wealth of knowledge in diagnostic medicine and has greatly affected medical practice, particularly in obstetrics. Millions of sonographic examinations are performed each year, and ultrasound remains one of the fastest growing imaging modalities because of its low cost, real-time interactions, portability, and apparent lack of biologic effects (bioeffects). No casual relationship has been established between clinical applications of diagnostic ultrasound and bioeffects on the patient or operator.

REGULATION OF ULTRASOUND OUTPUT The U.S. Food and Drug Administration (FDA) regulates the maximum output of ultrasound devices to an established level.

34

Considerations for Increasing Acoustic Output Mechanical Index Summary Statement on Gas Body Bioeffects OUTPUT DISPLAY STANDARD GENERAL AIUM SAFETY STATEMENTS EPIDEMIOLOGY CONTROLLING ULTRASOUND OUTPUT ULTRASOUND ENTERTAINMENT VIDEOS

The marketing approval process requires devices to be equivalent in efficacy and output to those produced before 1976. This historic regulation of sonography has provided a safety margin for ultrasound while allowing clinically useful performance. The mechanism has restricted ultrasound exposure to levels that apparently produce few, if any, obvious bioeffects based on the epidemiologic evidence, although animal studies have shown some evidence for biologic effects. In an effort to increase the efficacy of diagnostic ultrasound, the maximum acoustic output for some applications has increased through an additional FDA market approval process termed “510K Track 3.” The vast majority of ultrasound systems currently in use were approved through this process. The Track 3 process provides the potential for better imaging performance and, as discussed later, requires that additional information be reported

CHAPTER 2  Biologic Effects and Safety to the operator regarding the relative potential for bioeffects. Therefore informed decision making is important concerning the possible adverse effects of ultrasound in relation to the desired diagnostic information. Current FDA regulations that limit the maximum output are still in place, but in the future, systems might allow sonographers and physicians the discretion to increase acoustic output beyond a level that might induce a biologic response. Although the choices made during sonographic examinations may not be equivalent to the risk-versus-benefit decisions associated with imaging modalities using ionizing radiation, the operator will be increasingly responsible for determining the diagnostically required amount of ultrasound exposure. Thus the operator should know the potential bioeffects associated with ultrasound exposure. Patients also need to be reassured about the safety of a diagnostic ultrasound scan. The scientific community has identified some potential bioeffects from sonography, and although no causal relation has been established, it does not mean that no effects exist. Therefore it is important to understand the interaction of ultrasound with biologic systems.

PHYSICAL EFFECTS OF SOUND The physical effects of sound can be divided into two principal groups: thermal and nonthermal. Most medical professionals recognize the thermal effects of elevated temperature on tissue, and the effects caused by ultrasound are similar to those of any localized heat source. With ultrasound, the heating mainly results from the absorption of the sound field as it propagates through tissue. However, “nonthermal” sources can generate heat as well. Many nonthermal mechanisms for bioeffects exist. Acoustic fields can apply radiation forces (not ionizing radiation) on the structures within the body at both the macroscopic and the microscopic levels, resulting in exerted pressure and torque. The temporal average pressure in an acoustic field is different from the hydrostatic pressure of the fluid, and any object in the field is subject to this change in pressure. The effect is typically considered smaller than other effects because it relies on less significant factors in the formulation of the acoustic field. Acoustic fields can also cause motion of fluids. Such acoustically induced flow is called streaming. Acoustic cavitation is the action of acoustic fields within a fluid to generate bubbles and cause volume pulsation or even collapse in response to the acoustic field. The result can be heat generation and associated free radical formation, microstreaming of fluid around the bubble, radiation forces generated by the scattered acoustic field from the bubble, and mechanical actions from bubble collapse. The interaction of acoustic fields with bubbles or “gas bodies” (as they are generally called) has been a significant area of bioeffects research for many years.

THERMAL EFFECTS Ultrasound Produces Heat As ultrasound propagates through the body, energy is lost through attenuation. Attenuation causes loss of penetration and the

35

inability to image deeper tissues. Attenuation is the result of two processes, scattering and absorption. Scattering of the ultrasound results from the redirection of the acoustic energy by tissue encountered during propagation. With diagnostic ultrasound, some of the acoustic energy transmitted into the tissue is scattered back in the direction of the transducer, termed backscatter, which allows a signal to be detected and images to be made. Energy also is lost along the propagation path of the ultrasound by absorption. Absorption loss occurs substantially through the conversion of the ultrasound energy into heat. This heating provides a mechanism for ultrasound-induced bioeffects.

Factors Controlling Tissue Heating The rate of temperature increase in tissues exposed to ultrasound depends on several factors, including spatial focusing, ultrasound frequency, exposure duration, and tissue type.

Spatial Focusing Ultrasound systems use multiple techniques to concentrate or focus ultrasound energy and improve the quality of measured signals. The analogy for light is that of a magnifying glass. The glass collects all the light striking its surface and concentrates it into a small region. In sonography and acoustics in general, the term intensity is used to describe the spatial distribution of ultrasonic power (energy per unit time), where intensity = power/ area and the area refers to the cross-sectional area of the ultrasound beam. Another common beam dimension is the beam width at a specified location of the field. If the same ultrasonic power is concentrated into a smaller area, the intensity will increase. Focusing occurs on both transmission of the ultrasound and when receiving the backscattered signals used to form the image. The transmit focusing is of importance in terms of potential biologic effects because this phenomenon controls the applied energy to the tissue. There are ultrasound imaging systems that use plane wave transmission or limited transmit focusing, which may reduce the local intensity, but all ultrasound systems must still operate under the FDA limits. Focusing in an ultrasound system can be used to improve the spatial resolution of the images. The side effect is an increased potential for bioeffects caused by heating and cavitation. In general, the greatest heating potential is between the scanhead and the focus, but the exact position depends on the focal distance, tissue properties, and heat generated within the scanhead itself. Returning to the magnifying glass analogy, most children learn that the secret to incineration is a steady hand. Movement distributes the power of the light beam over a larger area, thereby reducing its intensity. The same is true in ultrasound imaging. Thus imaging systems that scan a beam through tissue reduce the spatial average intensity. Spectral Doppler and M-mode ultrasound imaging maintain the ultrasound beam in a stationary position (both considered unscanned modes) and therefore provide no opportunity to distribute the ultrasonic power spatially, whereas color flow Doppler, power mode Doppler, and B-mode (also called gray-scale) ultrasound imaging require that the beam be moved to new locations (scanned modes) at a rate sufficient to produce the real-time nature of these imaging modes.

Physics

PART I

TISSUE ATTENUATION

p+ Attenuation (dB/cm-MHz)

25

p–

TP

10 5 0

ni o flu tic id Bl oo d Br ai n Li ve M r us cl e Fa Te t nd on

PA

15

Am

Instantaneous intensity

Pulse length (temporal duration)

20

TA

Time

FIG. 2.1  Pressure and Intensity Parameters Measured in Medical Ultrasound.  The variables are defined as follows: p+, peak positive pressure in waveform; p−, peak rarefactional pressure in waveform; PA, pulse average; TA, temporal average; TP, temporal peak.

Temporal Considerations The ultrasound power is the temporal rate at which ultrasound energy is produced. Therefore controlling how ultrasound is produced in time seems a reasonable method for limiting its effects. Ultrasound can be produced in bursts rather than continuously. Ultrasound imaging systems operate on the principle of pulseecho, in which a burst of ultrasound is emitted, followed by a quiescent period listening for echoes to return. This pulsed wave ultrasound may be swept through the image plane numerous times during an imaging sequence. On the other hand, ultrasound may be transmitted in a continuous wave (CW) mode, in which the ultrasound transmission is not interrupted. The temporal peak intensity refers to the largest intensity at any time during ultrasound exposure (Fig. 2.1). The pulse average intensity is the average value over the duration of the ultrasound pulse. The temporal average intensity is the average over the entire pulse repetition period (elapsed time between onset of ultrasound bursts). The duty factor is defined as the fraction of time the ultrasound field is “on.” With significant time “off ” between pulses (small duty factor), the temporal average value will be significantly smaller. For example, a duty factor of 10% will reduce the temporal average intensity by a factor of 10 compared with the pulse average. The time-averaged quantities are the variables most related to the potential for thermal bioeffects. Combining temporal and spatial information results in common terms such as the spatial peak, temporal average intensity (ISPTA) and spatial average, temporal average intensity (ISATA). The overall duration, or dwell time, of the ultrasound exposure to a particular tissue is important because longer exposure of

Sk ar in t In ilag fa nt e sk ul l Sk ul l

Pressure

Pulse repetition period

C

36

Tissue Type FIG. 2.2  Tissue Attenuation.  Values for types of human tissue at body temperature. (Data from Duck FA, Starritt HC, Anderson SP. A survey of the acoustic output of ultrasonic Doppler equipment. Clin Phys Physiol Meas. 1987;8[1]:39-49.47)

the tissue may increase the risk of bioeffects. The motion of the scanhead during an examination reduces the dwell time within a particular region of the body and can minimize the potential for bioeffects of ultrasound. Therefore performing an efficient scan, spending only the time required for diagnosis, is a simple way to reduce exposure.

Tissue Type Numerous physical and biologic parameters control heating of tissues. Absorption is normally the dominant contributor to attenuation in soft tissue. The attenuation coefficient is the attenuation per unit length of sound travel and is usually given in decibels per centimeters-megahertz (dB/cm-MHz). The attenuation typically increases with increasing ultrasound frequency. The attenuation ranges from a negligible amount for fluids (e.g., amniotic fluid, blood, urine) to the highest value for bone, with some variation among different soft tissue types (Fig. 2.2). Another important factor is the body’s ability to cool tissue through blood perfusion. Well-perfused tissue will more effectively regulate its temperature by carrying away the excess heat produced by ultrasound. The exception is when heat is deposited too rapidly, as in therapeutic thermal ablation.1 Bone and soft tissue are two specific areas of interest based on the differences in heating phenomena. Bone has high attenuation of incident acoustic energy. In examinations during pregnancy, calcified bone is typically subjected to ultrasound, as in measurement of the biparietal diameter (BPD) of the skull. Fetal bone contains increasing degrees of mineralization as gestation progresses, thereby increasing risk of localized heating. Special heating situations relevant to obstetric ultrasound examinations may also occur in soft tissue, where overlying structures provide little attenuation of the field, such as the fluid-filled amniotic sac.

CHAPTER 2  Biologic Effects and Safety 8

TABLE 2.1  Fetal Femur Temperature Incrementsa at 1 W/cm2

7 Temperature increment (°C)

37

6

Gestational Age (days)

5

Diameter (mm)

Temperature Increments (°C)

0.5 1.2 3.3

0.10 0.69 2.92

59 78 108

4 3 a

2 1 0 0.0

0.5

1.0

1.5

Temperature increments in human fetal femur exposed for 20 seconds were found to be approximately proportional to incident intensity. With permission from Drewniak JL, Carnes KI, Dunn F. In vitro ultrasonic heating of fetal bone. J Acoust Soc Am. 1989;86(4):1254-1258.4

Exposure time (minutes)

Pressure

+

Shocked Normal

|

FIG. 2.3  Heating of Mouse Skull in a Focused Sound Field.  For these experiments, frequency was 3.6 MHz, and temporal average focal intensity was 1.5 W/cm2. Solid circles, Young (6 mo) mice (n = 4); vertical bars, two standard errors in height; top curves, theoretical estimation of the temperature increases by Nyborg.3 (With permission from Carstensen EL, Child SZ, Norton S, Nyborg W. Ultrasonic heating of the skull. J Acoust Soc Am. 1990;87[3]: 1310-1317.2)

Bone Heating The absorption of ultrasound at the bone surface allows for rapid deposition of energy from the field into a limited volume of tissue. The result can be a significant temperature rise. For example, Carstensen and colleagues2 combined an analytic approach and experimental measurements of the temperature rise in mouse skull exposed to CW ultrasound to estimate the temperature increments in bone exposures. Because bone has a large absorption coefficient, the incident ultrasonic energy is assumed to be absorbed in a thin planar sheet at the bone surface. The temperature rise of mouse skull has been studied in a 3.6-MHz focused beam with a beam width of 2.75 mm (Fig. 2.3). The temporal average intensity in the focal region was 1.5 W/cm.2 One of two models (upper curve in Fig. 2.3) in common use3 predicts values for the temperature rise about 20% greater than that actually measured in this experiment.2 Thus the theoretical model is conservative in nature. Similarly for the fetal femur, Drewniak and colleagues4 indicated that the size and calcification state of the bone contributed to the ex vivo heating of bone (Table 2.1). To put this in perspective and to illustrate the operator’s role in controlling potential heating, consider the following scenario. By reducing the output power of an ultrasound scanner by 10 dB, the predicted temperature rise would be reduced by a factor of 10, making the increase of 3°C seen by these researchers (see Table 2.1) virtually nonexistent. This strongly suggests the use of maximum receive gain and reduction in output power during ultrasound examinations (see section on considerations for controlling ultrasound output). In fetal examinations an attempt should be made to maximize receive gain because this comes at no cost

Time FIG. 2.4  Effect of Finite Amplitude Distortion on a Propagating Ultrasound Pulse.  Note the increasing steepness in the pulse, which contains higher frequency components.

to the patient in terms of exposure. Distinctions are often made between bone positioned deep to the skin at the focal plane of the transducer and bone near the skin surface, as when considering transcranial applications. This distinction is discussed later with regard to the thermal index (TI).

Soft Tissue Heating Two clinical situations for ultrasound exposure in soft tissue are particularly relevant to obstetric and gynecologic applications. First, a common scenario involves scanning through a full bladder. The urine is a fluid with a relatively low ultrasound attenuation coefficient. The reduced attenuation allows larger acoustic amplitudes to be applied deeper within the body. Second, the propagating wave may experience finite amplitude distortion, resulting in energy being shifted by a nonlinear process from lower to higher frequencies. The result is a shockwave—a gradual wave steepening results in a waveform composed of higher frequency components (Fig. 2.4). Attenuation increases with increasing frequency; therefore the absorption of a large portion of the energy in such a wave occurs over a much shorter distance, concentrating the energy deposition in the first tissue encountered, which may include the fetus.

PART I

Physics

Ultrasound imaging systems include specific modalities that rely on nonlinear effects. In tissue harmonic imaging, or native harmonic imaging, the image is created using the backscatter of harmonic components induced by nonlinear propagation of the ultrasound field. This has distinct advantages in terms of reducing image artifacts and improving lateral resolution in particular. In these nonlinear imaging modes the acoustic output must be sufficiently high to produce the effect. The acoustic power currently used is still within the FDA limits, but improvements in image quality using such modes may create the need to modify or relax the regulatory restrictions. Similarly, in elasticity or shear wave imaging, the acoustic pressure may need to be increased to provide sufficient acoustic radiation force for imaging tissue stiffness. This detail will be discussed in the section on considerations for increasing acoustic output. Transvaginal ultrasound is important to note because of the proximity of the transducer to sensitive tissues such as the ovaries. As discussed later, temperature increases near the transducer may provide a heat source at sites other than the focus of the transducer. In addition, the transducer face itself may be a significant heat source because of inefficiencies in its conversion of electric to acoustic energy. Such factors must be considered in the estimation of potential thermal effects in transvaginal ultrasound and other endocavitary applications.

Hyperthermia and Ultrasound Safety Knowledge of the bioeffects of ultrasound heating is in part based on the experience available from other, more common forms of hyperthermia, which serve as a basis for safety criteria. Extensive data exist on the effects of short-term and extended temperature increases, or hyperthermia. Teratogenic effects from hyperthermia have been demonstrated in birds, all the common laboratory animals, farm animals, and nonhuman primates.5 The wide range of observed bioeffects, from subcellular chemical alterations to gross congenital abnormalities and fetal death, is an indication of the effectiveness or universality of hyperthermic conditions for perturbing living systems.6 The National Council on Radiation Protection and Measurements (NCRP) Scientific Committee on Biological Effects of Ultrasound compiled a comprehensive list of the lowest reported thermal exposures producing teratogenic effects.7,8 Examination of these data indicated a lower boundary for observed thermally induced bioeffects. Questions remain, however, about the relevance of this analysis of hyperthermia to the application of diagnostic ultrasound.9 After a careful literature review, O’Brien and colleagues10 suggested a more detailed consideration of thermal effects with regard to short-duration exposures. Fig. 2.5 shows the recommended approach to addressing the combination of temperature and duration of exposure. Note that the tolerance of shorter durations and higher temperatures suggests a substantial safety margin for diagnostic ultrasound. Regardless, it is beneficial to provide feedback to the ultrasound operator as to the relative potential for a temperature rise in a given acoustic field under conditions associated with a particular examination. This will allow an informed decision as to the exposure needed to obtain diagnostically relevant information.

58 55 Temperature (°C)

38

52 49 46 43 40 37 0.1

1

10

100

1000

Time (s) FIG. 2.5  Conservative Boundary Curve for Nonfetal Bioeffects Caused by a Thermal Mechanism.  Note the increase in temperature tolerance associated with shorter durations of exposures, a modification to the earlier American Institute of Ultrasound in Medicine (AIUM) Conclusions Regarding Heat statement (March 26, 1997). The AIUM approved a revised thermal statement on April 6, 2009. For a complete description of the origins of this curve, see O’Brien and colleagues.10 (With permission from O’Brien Jr WD, Deng CX, Harris GR, et al. The risk of exposure to diagnostic ultrasound in postnatal subjects: thermal effects. J Ultrasound Med. 2008;27[4]:517-535.10)

Thermal Index Based on analysis of hyperthermia data, the NCRP proposed a general statement concerning the safety of ultrasound examinations in which no temperature rise greater than 1°C is expected. In an afebrile patient within this limit, the NCRP concluded that there was no basis for expecting an adverse effect. In cases where the temperature rise might be greater, the operator should weigh the benefit against the potential risk. To assist in this decision, given the range of different imaging conditions seen in practice, a thermal index (TI) was approved as part of the Standard for Real-Time Display of Thermal and Mechanical Acoustical Output Indices on Diagnostic Ultrasound Equipment of the American Institute of Ultrasound in Medicine (AIUM).11 This standard provides the operator with an indication of the relative potential risk of heating tissue, with calculations based on the imaging conditions and an on-screen display showing the TI. This standard was subsequently adopted as an international standard through the International Electrotechnical Commission (IEC).12

The Thermal Index To more easily inform the physician of the operating conditions that could, in some cases, lead to a temperature elevation of 1°C, a thermal index is defined as TI =

W0 Wdeg

where Wdeg is the ultrasonic source power (in watts) calculated as capable of producing a 1°C temperature elevation under specific conditions. W0 is the ultrasonic source power (in watts) being used during the current exam. Reproduced with permission of American Institute of Ultrasound in Medicine (AIUM).

CHAPTER 2  Biologic Effects and Safety The NCRP ultrasound committee introduced the TI concept.8 The purpose of the TI is to provide an indication of the relative potential for increasing tissue temperature, but it is not meant to provide the actual temperature rise. The NCRP recommended two tissue models to aid in the calculation of the ultrasound power that could raise the temperature in tissue by 1°C: (1) a homogeneous model in which the attenuation coefficient is uniform throughout the region of interest, and (2) a fixedattenuation model in which the minimum attenuation along the path from transducer to a distant anatomic structure is independent of the distance because of a low-attenuation fluid path (e.g., amniotic fluid).8,13,14 Because of concern for the patient, it was recommended that “reasonable worst case” assumptions be made with respect to estimation of temperature elevations in vivo. The FDA, AIUM, and National Electrical Manufacturers Association (NEMA) adopted the TI as part of the output display standard. They advocate estimating the effect of attenuation in the body by reducing the acoustic power/output of the scanner (W0) by a derating factor equal to 0.3 dB/cm-MHz for the soft tissue model.11 The AIUM Thermal Index Working Group considered three tissue models: (1) the homogeneous tissue or soft tissue model, (2) a tissue model with bone at the focus, and (3) a tissue model with bone at the surface, or transcranial model.11 The TI takes on three different forms for these tissue models.

Homogeneous Tissue Model (Soft Tissue) The assumption of homogeneity helps simplify the determination of the effects of acoustic propagation and attenuation, as well as the heat transfer characteristics of the tissue. Providing one of the most common applications for ultrasound imaging, this model applies to situations where bone is not present and can generally be used for fetal examinations during the first trimester (low calcification in bone). In the estimation of potential heating, many assumptions and compromises had to be made to calculate a single quantity that would guide the operator. Calculations of the temperature rise along the axis of a focused beam for a simple, spherically curved, single-element transducer result in two thermal peaks. The first is in the near field (between the transducer and the focus), and the second appears close to the focal region.15,16 The first thermal peak occurs in a region with low ultrasound intensity and wide beam width. When the beam width is large, cooling will occur mainly because of perfusion. In the near field the magnitude of the local intensity is the chief determinant of the degree of heating. The second thermal peak occurs at the location of high intensity and narrow beam width at or near the focal plane. Here the cooling is dominated by conduction, and the total acoustic power is the chief determinant of the degree of heating. Given the thermal “twin peaks” dilemma, the AIUM Thermal Index Working Group compromised in creating a TI that included contributions from both heating domains.11 Their rationale was based on the need to minimize the acoustic measurement load for manufacturers of ultrasound systems. In addition, adjustments had to be made to compensate for effects of the large range of potential apertures. The result is a complicated series of calculations and measurements that must be performed, and to the

39

credit of the many manufacturers, there has been considerable effort in implementing a display standard to provide user feedback. Different approaches to these calculations were considered,10 but changes will require that the currently accepted implementation be reexamined and approved for use by the FDA and considered by the IEC.

Tissue Model With Bone at the Focus (Fetal Applications) Applications of ultrasound in which the acoustic beam travels through soft tissue for a fixed distance and impinges on bone occur most often in obstetric scanning during the second and third trimesters. Carson and colleagues13 recorded sonographic measurements of the maternal abdominal wall thickness in various stages of pregnancy. Based on their results, the NCRP recommended that the attenuation coefficients for the first, second, and third trimesters be 1.0, 0.75, and 0.5 dB/MHz, respectively.7 These values represent “worst case” estimates. In addition, Siddiqi and colleagues17 determined the average tissue attenuation coefficient for transabdominal insonification (exposure to ultrasound waves) in a patient population of nonpregnant, healthy volunteers was 2.98 dB/MHz. This value represents an average measured value and is much different from the worst-case estimates previously listed. This leads to considerable debate on how such parameters should be included in an index. In addition, bone is a complex, hard connective tissue with a calcified collagenous intercellular structure. Its absorption coefficient for longitudinal waves is a factor of 10 greater than that for most soft tissues (see Fig. 2.2). Shear waves are also created in bone as sound waves strike bone at oblique incidence. The absorption coefficients for shear waves are even greater than those for longitudinal waves.18-20 Based on the data of Carstensen and colleagues2 described earlier, the NCRP proposed a thermal model for bone heating. Using this model, the Bone Thermal Index (TIB) is estimated for conditions in which the focus of the beam is at or near bone. Again, assumptions and compromises had to be made to develop a functional TI for the case of bone exposure, as follows: • For unscanned mode transducers (operating in a fixed position) with bone in the focal region, the location of the maximum temperature increase is at the surface of the bone. Therefore the TIB is calculated at the distance along the beam from the transducer where it is maximized, a worst-case assumption. • For scanned modes, the Soft Tissue Thermal Index (TIS) is used because the temperature increase at the surface is either greater than or approximately equal to the temperature increase with bone in the focus. Tissue Model With Bone at the Surface (Transcranial Applications) For adult cranial applications, the same model as that with bone at the focus is used to estimate the temperature distribution in situ. However, because the bone is located at the surface, immediately after the acoustic beam enters the body, attenuation of the acoustic power output is not included.11 In this situation the equivalent beam diameter at the surface is used to calculate the

40

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Physics

acoustic power and derive the Cranial Bone Thermal Index (TIC).

Estimate of Thermal Effects Ultrasound users should keep in mind several points when referring to the TI as a means of estimating the potential for thermal effects. First, the TI is not synonymous with temperature rise. A TI equal to 1 does not mean the temperature will rise 1°C. An increased potential for thermal effects can be expected as TI increases. Second, a high TI does not mean that bioeffects are occurring, but only that the potential exists. The thermal models employed for TI calculation may not consider factors that may reduce the actual temperature rise. However, TI should be monitored during examinations and minimized when possible. Finally, there is no consideration in the TI for the duration of the scan, so minimizing the overall examination time will reduce the potential for effects. There have been proposals suggesting the inclusion of such a dwell time effect,21 but these have not been adopted.

Summary Statement on Thermal Effects The AIUM statement concerning thermal effects of ultrasound includes several conclusions that can be summarized as follows22: • Adult examinations resulting in a temperature rise of up to 2°C are not expected to cause bioeffects. (Many ultrasound examinations fall within these parameters.) • A significant number of factors control heat production by diagnostic ultrasound. • Ossified bone is a particularly important concern for ultrasound exposure.

• A labeling standard now provides information concerning potential heating in soft tissue and bone. • Even though an FDA limit exists for fetal exposures, predicted temperature rises can exceed 2°C. • Thermal indices are expected to track temperature increases better than any single ultrasonic field parameter.

EFFECTS OF ACOUSTIC CAVITATION Potential Sources for Bioeffects Knowledge concerning the interaction of ultrasound with gas bodies (which many term “cavitation”) has significantly increased over time, although it is not as extensive as that for ultrasound thermal effects and other sources of hyperthermia. Acoustic cavitation inception is demarcated by a specific threshold value: the minimum acoustic pressure necessary to initiate the growth of a cavity in a fluid during the rarefaction phase of the cycle. Several parameters affect this threshold, including initial bubble or cavitation nucleus size, acoustic pulse characteristics (e.g., center frequency, pulse repetition frequency [PRF], pulse duration), ambient hydrostatic pressure, and host fluid parameters (e.g., density, viscosity, compressibility, heat conductivity, surface tension). Inertial cavitation refers to bubbles that undergo large variations from their equilibrium sizes in a few acoustic cycles. Specifically during contraction, the surrounding fluid inertia controls the bubble motion.23 Large acoustic pressures are necessary to generate inertial cavitation, and the collapse of these cavities is often violent.

The AIUM Statement on Mammalian Biological Effects of Heat24 APPROVED MARCH 25, 2015 1. An excessive temperature increase can result in toxic effects in mammalian systems. The biological effects observed depend on many factors, such as the exposure duration, the type of tissue exposed, its cellular proliferation rate, and its potential for regeneration. Age and stage of development are important factors when considering fetal and neonatal safety. Temperature increases of several degrees Celsius above the normal core range can occur naturally. The probability of an adverse biological effect increases with both the duration and the magnitude of the temperature rise.

2. In general, adult tissues are more tolerant of temperature increases than fetal and neonatal tissues. Therefore, higher temperatures and/or longer exposure durations would be required for thermal damage. The considerable data available on the thermal sensitivity of adult tissues support the following inferences10: a. For exposure durations up to 50 hours, there have been no significant adverse biological effects observed due to temperature increases less than or equal to 1.5°C above normal.25 b. For temperature increases between 1.5°C and 6°C above normal, there have been no significant adverse biological effects observed due to temperature increases less than or equal to 6 − [log10(t/60)]/0.6 where t is the exposure duration in seconds. For

example, for temperature increases of 4°C and 6°C, the corresponding limits for the exposure durations t are 16 minutes and 1 minute, respectively. c. For temperature increases greater than 6°C above normal, there have been no significant adverse biological effects observed due to temperature increases less than or equal to 6 − [log10(t/60)]/0.3 where t is the exposure duration in seconds. For example, for temperature increases of 9.6°C and 6.0°C, the corresponding limits for the exposure durations t are 5 and 60 seconds, respectively. d. For exposure durations less than 5 seconds, there have been no significant, adverse biological effects observed due to temperature increases less than or equal to 9 − [log10(t/60)]/0.3 where t is the exposure duration in seconds. For example, for temperature increases of 18.3°C, 14.9°C, and 12.6°C, the corresponding limits for the exposure durations t are 0.1, 1, and 5 seconds, respectively. 3. Acoustic output from diagnostic ultrasound devices is sufficient to cause temperature elevations in fetal tissue. Although fewer data are available for fetal tissues, the following conclusions are justified10,26: a. In general, temperature elevations become progressively greater from B-mode to color Doppler to spectral Doppler applications.

CHAPTER 2  Biologic Effects and Safety

41

The AIUM Statement on Mammalian Biological Effects of Heat24—cont’d











b. For identical exposure conditions, the potential for thermal bioeffects increases with the dwell time during examination. c. For identical exposure conditions, the temperature rise near bone is significantly greater than in soft tissues, and it increases with ossification development throughout gestation. For this reason, conditions in which an acoustic beam impinges on ossifying fetal bone deserve special attention due to its close proximity to other developing tissues. d. The current U.S. Food and Drug Administration regulatory limit for the derated spatial-peak temporalaverage intensity (ISPTA.3) is 720 mW/cm2. For this exposure, the theoretical estimate of the maximum temperature increase in the conceptus may exceed 1.5°C. e. Although an adverse fetal outcome is possible at any time during gestation, most severe and detectable effects of thermal exposure in animals have been observed during the period of organogenesis. For this reason, exposures during the first trimester should be restricted to the lowest outputs consistent with obtaining the necessary diagnostic information. f. Ultrasound exposures that elevate fetal temperature by 4°C above normal for 5 minutes or more have the potential to induce severe developmental defects. Thermally induced congenital anomalies have been observed in a large variety of animal species. In current clinical practice, using commercially available equipment, it is unlikely that such thermal exposure would occur at a specific fetal anatomic site provided that the thermal index (TI) is less than 2.0 and the dwell time on that site does not exceed 4 minutes. g. Transducer self-heating is a significant component of the temperature rise of tissues close to the transducer. This may be of significance in transvaginal

scanning, but no data for the fetal temperature rise are available. 4. The temperature increase during exposure of tissues to diagnostic ultrasound fields is dependent on: (1) output characteristics of the acoustic source, such as frequency, source dimensions, scan rate, output power, pulse repetition frequency, pulse duration, transducer selfheating, exposure time, and wave shape; and (2) tissue properties, such as attenuation, absorption, speed of sound, acoustic impedance, perfusion, thermal conductivity, thermal diffusivity, anatomic structure, and the nonlinearity parameter. 5. Calculations of the maximum temperature increase resulting from ultrasound exposure are not exact because of the uncertainties and approximations associated with the thermal, acoustic, and structural characteristics of the tissues involved. However, experimental evidence shows that calculations are generally capable of predicting measured values within a factor of 2. Thus, such calculations are used to obtain safety guidelines for clinical exposures in which direct temperature measurements are not feasible. These guidelines, called thermal indices,a provide a real-time display of the relative probability that a diagnostic system could induce thermal injury in the exposed subject. Under most clinically relevant conditions, the soft tissue thermal index (TIS) and the bone thermal index (TIB) either overestimate or closely approximate the best available estimate of the maximum temperature increase (ΔTmax). For example, if TIS = 2, then ΔTmax ≤ 2°C; actual temperature increases are also dependent on dwell time.

However, in some applications, such as fetal examinations in which the ultrasound beam passes through a layer of relatively unattenuating liquid, such as urine or amniotic fluid, the TI can underestimate ΔTmax by up to a factor of 2.27,28

a

The thermal indices are the nondimensional ratios of attenuated acoustic power at a specific point to the attenuated acoustic power required to raise the temperature at that point in a specific tissue model by 1°C.29 AIUM, American Institute of Ultrasound in Medicine. Reproduced with permission from American Institute of Ultrasound in Medicine (AIUM). Statement on mammalian biological effects of heat. Laurel, MD: AIUM; 2015. Available from: http://www.aium.org/officialStatements/17. Updated March 25, 2015. Cited October 7, 2016.24

The effect of preexisting cavitation nuclei may be one of the principal controlling factors in mechanical effects that result in biologic effects. The body is such an excellent filter that these nucleation sites may be found only in small numbers and at selected sites. For example, if water is filtered down to 2 µm, the cavitation threshold doubles.30 Theoretically, the tensile strength of water that is devoid of cavitation nuclei is about 100 megapascals (MPa).31 Various models have been suggested to explain bubble formation in animals,32,33 and these models have been used extensively in cavitation threshold determination. One model is used in the prediction of SCUBA diving tables and may also have applicability

to patients.34 It remains to be seen how well such models will predict the nucleation of bubbles from diagnostic ultrasound in the body. Fig. 2.6 shows a 1-MHz therapeutic ultrasound unit generating bubbles in gas-saturated water. The particular medium and ultrasound parameters were chosen to optimize the conditions for cavitation. Using CW ultrasound and many preexisting gas pockets in the water set the stage for the production of cavitation. Even though these acoustic pulses are longer than those typically used in diagnostic ultrasound, cavitation effects have also been observed with diagnostic pulses in fluids.35 Ultrasound contrast agents composed

42

PART I

Physics

FIG. 2.6  Acoustic Cavitation Bubbles.  This cavitation activity is being generated in water using a common therapeutic ultrasound device. (Courtesy of National Center for Physical Acoustics, University of Mississippi.)

FIG. 2.8  Collapsing Bubble Near a Boundary.  When cavitation is produced near boundaries, a liquid jet may form through the center of a bubble and strike the boundary surface. (Courtesy of Lawrence A. Crum.)

a therapeutic ultrasound device; the setup is backlighted (in red) to show the bubbles and experimental apparatus. The chemiluminescence emissions are the blue bands seen through the middle of the liquid sample holder. The light emitted is sufficient to be seen by simply adapting one’s eyes to darkness. Electron spin resonance can also be used with molecules that trap free radicals to detect cavitation activity capable of free radical production.38 A number of other chemical detection schemes are presently employed to detect cavitation from diagnostic devices in vitro.

Evidence of Cavitation From Lithotripters

FIG. 2.7  Chemical Reaction Induced by Cavitation Producing Visible Light.  The reaction is the result of free radical production. (Courtesy of National Center for Physical Acoustics, University of Mississippi.)

of stabilized gas bubbles should provide a source of cavitation nuclei, as discussed later in the section on ultrasound contrast agents.

Sonochemistry Free radical generation and detection provide a means to observe cavitation and to gauge its strength and potential for damage. The sonochemistry of free radicals is the result of very high temperatures and pressures within the rapidly collapsing bubble. These conditions can even generate light, or sonoluminescence.36 With the addition of the correct compounds, chemical luminescence can also be used for free radical detection and can be generated with short pulses similar to those used in diagnostic ultrasound.37 Fig. 2.7 shows chemiluminescence generated by

It is possible to generate bubbles in vivo using short pulses with high amplitudes of extracorporeal shockwave lithotripsy (ESWL). The peak positive pressure for lithotripsy pulses can be as high as 50 MPa, with a rarefactional pressure of about 20 MPa. Finite amplitude distortion causes high frequencies to appear in high-amplitude ultrasound fields. Although ESWL pulses have significant energy at high frequencies because of finite amplitude distortion, a large portion of the energy is actually in the 100-kHz range, much lower than frequencies in diagnostic scanners. The lower frequency makes cavitation more likely. Aymé and Carstensen39 showed that the higher frequency components in nonlinearly distorted pulses contributed little to the killing of Drosophila larvae. Interestingly, evidence indicates that collapsing bubbles play a role in stone disruption.40-42 A bubble collapsing near a surface may form a liquid jet through its center, which strikes the surface (Fig. 2.8). Placing a sheet of aluminum foil at the focus of a lithotripter generates small pinholes.40 The impact is even sufficient to pit solid brass and aluminum plates. At very high acoustic amplitudes, tissue can be disrupted and even emulsified using ultrasound in a process termed “histotripsy.”43-45 Peak rarefactional pressures used in this form of therapeutic ultrasound can be as high as 25 to

CHAPTER 2  Biologic Effects and Safety 30 MPa, at which point gas bubbles form spontaneously in a very consistent controlled fashion that allows for therapeutic applications. Clearly, lithotripsy and histotripsy differ greatly from diagnostic ultrasound in the acoustic power generated and are not comparable in the bioeffects produced. However, some diagnostic devices produce peak rarefactional pressures greater than 3 MPa, which is in the lower range of lithotripter outputs.46-48 Lung damage and surface petechiae have been noted as side effects of ESWL in clinical cases.49 Inertial cavitation was suspected as the cause, prompting several researchers to study the effects of diagnostic ultrasound exposure on the lung parenchyma.50,51

Bioeffects in Lung and Intestine Lung tissue and intestinal tissue are key locations for examining for bioeffects of diagnostic ultrasound.50 The presence of air in the alveolar spaces constitutes a significant source of gas bodies. Child and colleagues51 measured threshold pressures for hemorrhage in mouse lung exposed to 1- to 4-MHz short-pulse diagnostic ultrasound (i.e., 10- and 1-µm pulse durations). The threshold of damage in murine lung at these frequencies was 1.4 MPa. Pathologic features of this damage included extravasation of blood cells into the alveolar spaces.52 The authors hypothesized that cavitation, originating from gas-filled alveoli, was responsible for the damage. Their data provided the first direct evidence that clinically relevant, pulsed ultrasound exposures produce deleterious effects in mammalian tissue in the absence of significant heating. Hemorrhagic foci induced by 4-MHz pulsed Doppler ultrasound have also been reported in the monkey.53 Damage in the monkey lung was of a significantly lesser degree than that in the mouse. In these studies it was impossible to show categorically that bubbles induced these effects because the cavitation-induced bubbles were not observed. Thresholds for petechial hemorrhage in the lung caused by ultrasound have been measured in mouse, rat, rabbit and pig.54-56 Direct mechanical stresses associated with propagation of ultrasound in the lung were believed to contribute to the damage observed.50,57 Thresholds for hemorrhage in the murine intestine exposed to pulsed ultrasound have also been determined.58 Kramer and colleagues59 assessed cardiopulmonary function in rats exposed to pulsed ultrasound well above the acoustic output threshold of damage, at a mechanical index (MI) of 9.7. Measurements of cardiopulmonary function included arterial blood pressure, heart rate, respiratory rate, and arterial blood gases (Pco2 and Po2). If only one side of the rat lung was exposed, the cardiopulmonary measurements did not change significantly between baseline and postexposure values because of the functional respiratory reserve in the unexposed lobes. However, when both sides of the lung had significant ultrasound-induced lesions, the rats were unable to maintain systemic arterial pressure or resting levels of arterial Po2. Further studies are required to determine the relevance of these findings to humans. In general, tissues containing air (or stabilized gas) are more susceptible to damage than are

43

tissues without gas. Also, no confirmed reports of petechial hemorrhage below an MI of 0.4 have been noted in animal studies. As recently as 2012, this threshold in lungs was confirmed in a small animal model.60 However, it should be noted that the mechanism for pulmonary effects might not follow the functional frequency dependence embedded in the MI.61

Ultrasound Contrast Agents The apparent absence of cavitation in many locations in the body can result from the lack of available cavitation nuclei. Based on evidence in the lung and intestine in mammalian models described earlier, the presence of gas bodies clearly reduces the requisite acoustic field for producing bioeffects. Many ultrasound contrast agents are composed of stabilized gas bubbles, so they could provide readily available nuclei for potential cavitation activity. This makes the investigation of bioeffects in the presence of ultrasound contrast agents an important area of research.62-64 Studies have also shown that ultrasound exposure in the presence of contrast agents produces small vascular petechiae and endothelial damage in mammalian systems.65-70 Acoustic emissions from activated microbubbles correlate with the degree of vascular damage.67,68 As a result, the AIUM has a safety statement on the bioeffects of diagnostic ultrasound with gas body contrast agents. This bioeffect may occur, but the issue remains whether it constitutes a significant physiologic risk. The safety statement is designed to make sonographers and physicians aware of the potential for bioeffects in the presence of gas contrast agents and allow them to make an informed decision based on a risk-versus-benefit assessment. Some research also indicates the production of premature ventricular contractions (PVCs) during cardiac scanning in the presence of ultrasound contrast agents. At least one human study indicated an increase in PVCs only when ultrasound imaging was performed with a contrast agent, and not with ultrasound imaging alone or during injection of the agent without imaging.71 Another study72 revealed that oscillating microbubbles affect stretch activation channels73,74 in cardiac cells, which generates membrane depolarization and triggers action potentials and thus PVCs. The importance of this bioeffect is also being debated because there is a naturally occurring rate of PVCs, and a small increase may not be considered clinically important, particularly if the patient benefits from using the agent. Additional consideration might be given to patients with specific conditions in whom additional PVCs should be avoided. The consequences of the ultrasound contrast agent bioeffects reported thus far require more study. Although the potential exists for a bioeffect, its scale and influence on human physiology remain unclear. Contrast agents have demonstrated efficacy for specific indications, facilitating patient management.75 In addition, clinical trials and marketing follow-up of many patients receiving ultrasound and contrast agents have reported few effects. Several publications provide evidence confirming the safety of ultrasound contrast agent use.76-79

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The AIUM Statement on Mammalian Biological Effects in Tissues With Gas Body Contrast Agents80 APPROVED MARCH 25, 2015 Presently available ultrasound contrast agents consist of suspensions of gas bodies (stabilized gaseous microbubbles). The gas bodies have the correct size for strong echogenicity with diagnostic ultrasound and also for passage through the microcirculation. Commercial agents undergo rigorous clinical testing for safety and efficacy before Food and Drug Administration approval is granted, and they have been in clinical use in the United States since 1994. Detailed information on the composition and use of these agents is included in the package inserts. In the United States, contrast agents have been approved for opacification of the left ventricular chamber and delineation of the left ventricular endocardial border. Outside the United States, additional approved indications include imaging lesions of the breast and liver, portal vein, and extracranial carotid and peripheral arteries. Many other diagnostic applications are under development or clinical testing. Contrast agents carry some potential for nonthermal bioeffects when ultrasound interacts with the gas bodies. The mechanism for such effects is related to the physical phenomenon of acoustic cavitation. Several published reports describe adverse bioeffects in mammalian tissue in vivo resulting from exposure to diagnostic ultrasound with gas body contrast agents in the circulation. Induction of premature ventricular contractions by triggered contrast echocardiography in humans has been reported for a noncommercial agent and in laboratory animals for commercial agents. Microvascular leakage, killing of cardiomyocytes, and glomerular capillary hemorrhage, among other bioeffects, have been reported in animal studies. Two medical ultrasound societies have examined this potential risk of bioeffects in diagnostic ultrasound with contrast agents and provide extensive reviews of the topic: the World Federation for

Ultrasound in Medicine and Biology Contrast Agent Safety Symposium81 and the American Institute of Ultrasound in Medicine 2005 Bioeffects Consensus Conference.62 More recently, the British Medical Ultrasound Society issued a detailed assessment of methods for the safe use of diagnostic ultrasound, including use of contrast agents.82 Based on a review of these reports and recent literature, the Bioeffects Committee has issued the following statement. STATEMENT ON MAMMALIAN BIOLOGICAL EFFECTS OF DIAGNOSTIC ULTRASOUND WITH GAS BODY CONTRAST AGENTS Induction of premature ventricular contractions, microvascular leakage with petechiae, glomerular capillary hemorrhage, local cell killing, and other effects in mammalian tissue in vivo have been reported and independently confirmed for diagnostic ultrasound exposure with a mechanical index (MI) above about 0.4 and a gas body contrast agent present in the circulation. Although the medical significance of such microscale bioeffects is uncertain, minimizing the potential for such effects represents prudent use of diagnostic ultrasound. In general, for imaging with contrast agents at an MI above 0.4, practitioners should use the minimal agent dose, MI, and examination time consistent with efficacious acquisition of diagnostic information. In addition, the echocardiogram should be monitored during high-MI contrast cardiac-gated perfusion echocardiography, particularly in patients with a history of myocardial infarction or unstable cardiovascular disease. Furthermore, physicians and sonographers should follow all guidance provided in the package inserts of these drugs, including precautions, warnings, and contraindications.

AIUM, American Institute of Ultrasound in Medicine. Reproduced with permission from American Institute of Ultrasound in Medicine (AIUM). Statement on mammalian biological effects in tissues with gas body contrast agents. Laurel, MD: AIUM; 2015. Available from: http://www.aium.org/officialStatements/25. Approved March 25, 2015. Cited October 7, 2016.80

Considerations for Increasing Acoustic Output Situations arise where increasing acoustic output in ultrasound imaging could provide improved performance, particularly at significant depths. The desire to increase acoustic output was the original impetus for the development of the FDA 510K Track 3 mechanism in situations in which imaging was challenging for deep tissue structures, particularly in obstetrics. Modes such as tissue harmonic imaging and elasticity and shear wave imaging may also benefit from similar considerations. A working group of the Output Standards Subcommittee of the AIUM Technical Standards Committee examined on the potential benefits and risks of conditionally increased acoustic pressure. The resulting white paper83 provides a rationale for a three-tiered approach for conditionally increased acoustic output that follows the model employed for elevated output in magnetic resonance imaging, and concludes with summary

recommendations to facilitate clinical studies monitored by an institutional review board to investigate the benefits of an increased acoustic output in specific tissues. One of the fundamental assumptions in the MI calculation is the presence of a preexisting gas body. Based on theoretical predictions and experimentally reported cavitation thresholds for tissues that do not contain preexisting gas bodies, the working group found this assumption to be overly conservative and concluded that exceeding the recommended maximum MI given in the FDA guidance could be warranted without concern for increased risk of cavitation in these tissues. In the future, the ultrasound research community will need examine how much improvement in diagnostic ultrasound imaging might be achieved with increased acoustic output.

Mechanical Index Calculations for cavitation prediction have yielded a trade-off between peak rarefactional pressure and frequency.84 This

CHAPTER 2  Biologic Effects and Safety

45

10 MI=2 5

Threshold pressure (MPa)

MI=1 190 W

cm–2

2 1 MI=0.3 10 W cm–2

5

2

0.1 5

1

2

5

10

Frequency (MHz) Adult mouse lung (10 µs) Adult mouse lung (1 µs) Neonatal mouse lung (10 µs) Fruit fly larvae (10 µs) Elodea leaves (5 µs) FIG. 2.9  Threshold for Bioeffects From Pulsed Ultrasound Scan Using Low Temporal Average Intensity.  Data shown are the threshold for effects measured in peak rarefactional pressures (p− in Fig. 2.1) as a function of ultrasound frequency used in the exposure. Pulse durations are shown in parentheses in the key below the graph. Also shown for reference purposes are the values for the mechanical index (MI) and the local spatial peak, pulse average intensity (ISPPA). (With permission from American Institute of Ultrasound in Medicine. Consensus Report on Potential Bioeffects of Diagnostic Ultrasound. J Ultrasound Med. 2008;27:503-515.22)

predicted trade-off assumes short-pulse (a few acoustic cycles) and low–duty cycle ultrasound (0.7 cm) is associated with severe portal hypertension (portohepatic gradient >10 mm Hg)82 (Fig. 4.31C and D). • Paraumbilical vein: Runs in the falciform ligament and connects the left portal vein to the systemic epigastric veins

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near the umbilicus (Cruveilhier-Baumgarten syndrome)86 (Fig. 4.31A). Some studies suggest that, if the hepatofugal flow in the patent paraumbilical vein exceeds the hepatopetal flow in the portal vein, patients may be protected from developing esophageal varices.87,88 • Splenorenal and gastrorenal: Tortuous veins may be seen in the region of the splenic and left renal hilus (Fig. 4.31E and F), which represent collaterals between the splenic, coronary, and short gastric veins and the left adrenal or renal veins. • Intestinal: Regions in which the gastrointestinal tract becomes retroperitoneal so that the veins of the ascending and descending colon, duodenum, pancreas, and liver may anastomose with the renal, phrenic, and lumbar veins (systemic tributaries). • Hemorrhoidal: The perianal region where the superior rectal veins, which extend from the inferior mesenteric vein, anastomose with the systemic middle and inferior rectal veins. Duplex Doppler sonography provides additional information regarding direction of portal flow. False results may occur, however, when sampling is obtained from periportal collaterals in patients with portal vein thrombosis or hepatofugal portal flow.89 Normal portal venous flow rates vary in the same individual, increasing postprandially and during inspiration75,90 and decreasing after exercise or in the upright position.91 An increase of less than 20% in the diameter of the portal vein with deep inspiration indicates portal hypertension with 81% sensitivity and 100% specificity.92 The normal portal vein demonstrates an undulating hepatopetal (toward the liver) flow. Mean portal venous flow velocity is 15 to 18 cm/sec and varies with respiration and cardiac pulsation. As portal hypertension develops, the flow in the portal vein loses its undulatory pattern and becomes monophasic. As the severity of portal hypertension increases, flow becomes biphasic and finally hepatofugal (away from the liver). Intrahepatic arterial-portal venous shunting may also be seen. Chronic liver disease is also associated with increased splanchnic blood flow. Evidence suggests that portal hypertension is partly caused by the hyperdynamic flow state of cirrhosis. Zwiebel et al.93 found that blood flow was increased in the superior mesenteric arteries and splenic arteries of patients with cirrhosis and splenomegaly, compared with normal controls. Of interest, in patients with cirrhosis and normal-sized livers, splanchnic blood flow was not increased. Patients with isolated splenomegaly and normal livers were not included in this study. The limitations of Doppler sonography in the evaluation of portal hypertension include the inability to determine vascular pressures and flow rates accurately. Patients with portal hypertension are often ill, with contracted livers, abundant ascites, and floating bowel, all of which create a technical challenge. In a comparison of duplex Doppler sonography with magnetic resonance angiography, MRI imaging was superior in the assessment of patency of the portal vein and surgical shunts, as well as in detection of varices.94 However, when technically adequate, the Doppler study was accurate in the assessment of normal portal anatomy and flow direction. Duplex Doppler sonography has

the added advantages of decreased cost and portability of the equipment and therefore should be used as the initial screening method for portal hypertension.

Portal Vein Thrombosis Portal vein thrombosis has been associated with malignancy, including HCC, metastatic liver disease, carcinoma of the pancreas, and primary leiomyosarcoma of the portal vein,95 as well as with chronic pancreatitis, hepatitis, septicemia, trauma, splenectomy, portacaval shunts, hypercoagulable states such as pregnancy and in neonates, omphalitis, umbilical vein catheterization, and acute dehydration.96 Sonographic findings of portal vein thrombosis include echogenic thrombus within the lumen of the vein, portal vein collaterals, expansion of the caliber of the vein, and cavernous transformation96 (Figs. 4.32 and 4.33). Cavernous transformation of the portal vein refers to numerous wormlike vessels at the porta hepatis, which represent periportal collateral circulation.97 This pattern is observed in long-standing thrombosis, requiring up to 12 months to occur, and thus is more likely to develop with benign disease.98 Acute thrombus may appear relatively anechoic and thus may be overlooked unless Doppler ultrasound interrogation is performed. Malignant thrombosis of the portal vein has a high association with HCC and is often expansive, as is malignant occlusion from other primary or secondary disease (Fig. 4.32A and B and Fig. 4.34). Doppler sonography is useful in distinguishing between benign and malignant portal vein thrombi in patients with cirrhosis. Both bland and malignant thrombi may demonstrate venous blood flow. Pulsatile (arterial) flow, however, has been found to be 95% specific for the diagnosis of malignant portal vein thrombosis (see Fig. 4.32). The sensitivity was only 62% because many malignant thrombi are hypovascular.99

Budd-Chiari Syndrome The Budd-Chiari syndrome is a relatively rare disorder characterized by occlusion of the lumens of the hepatic veins with or without occlusion of the IVC lumen. The degree of occlusion and presence of collateral circulation predict the clinical course. Some patients die in the acute phase of liver failure. Causes of Budd-Chiari syndrome include coagulation abnormalities such as polycythemia rubra vera, chronic leukemia, and paroxysmal nocturnal hemoglobinuria; trauma; tumor extension from primary HCC, renal carcinoma, and adrenocortical carcinoma; pregnancy; congenital abnormalities; and obstructing membranes. The classic patient in North America is a young adult woman taking oral contraceptives who presents with an acute onset of ascites, right upper quadrant pain, hepatomegaly, and, to a lesser extent, splenomegaly. In some cases, no causal factor is found. The syndrome is more common in other geographic areas, including India, South Africa, and Asia. Sonographic evaluation of the patient with Budd-Chiari syndrome includes gray-scale and Doppler features.100-111 Ascites is invariably seen. The liver is typically large and bulbous in the acute phase (Fig. 4.35A). Hemorrhagic infarction may produce significant altered regional echogenicity. As infarcted areas become more fibrotic, echogenicity increases.109 The caudate lobe is often

CHAPTER 4  The Liver

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FIG. 4.32  Portal Vein Thrombosis: Benign and Malignant.  Malignant thrombus: transverse views of (A) the vein at the porta hepatis and (B) left ascending left portal vein. Both are distended with occlusive thrombus. Benign thrombus: (C) transverse and (D) sagittal images of simple, bland nonocclusive thrombus in the left portal vein at the porta hepatis.

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FIG. 4.33  Cavernous Transformation of Portal Vein.  (A) Gray-scale image. (B) Color Doppler image. Numerous periportal collateral vessels are present.

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FIG. 4.34  Metastasis to the Portal Vein From Colon Cancer.  (A) Sagittal view of the main portal vein at the porta hepatis and (B) subcostal oblique sonogram of the left ascending branch of the portal vein show the portal vein is distended and highly echogenic (arrows). There is also evidence of cavernous transformation, an uncommon accompaniment of malignant portal vein occlusion.

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FIG. 4.35  Acute Budd-Chiari Syndrome.  (A) Transverse view of liver shows a large, bulbous caudate lobe. (B) Sagittal view of right hepatic vein shows echoes within the vein lumen consistent with thrombosis, with absence of the vessel toward the inferior vena cava. Doppler ultrasound showed no flow in this vessel.

spared in Budd-Chiari syndrome because the emissary veins drain directly into the IVC at a lower level than the involved main hepatic veins. Increased blood flow through the caudate lobe leads to relative caudate enlargement. Real-time scanning allows the radiologist to evaluate the IVC and hepatic veins noninvasively. Sonographic features include evidence of the hepatic vein occlusion (Fig. 4.35B and Fig. 4.36) and the development of abnormal intrahepatic collaterals (Fig. 4.37). The extent of hepatic venous involvement in Budd-Chiari

syndrome includes partial or complete inability to see the hepatic veins, stenosis with proximal dilation, intraluminal echogenicity, thickened walls, thrombosis (Figs. 4.38 and 4.39), and extensive intrahepatic collaterals107,108 (see Fig. 4.37). Membranous “webs” may be identified as echogenic or focal obliterations of the lumen.107 Real-time ultrasonography, however, underestimates the presence of thrombosis and webs and may be inconclusive in a cirrhotic patient with hepatic veins that are difficult to image.108 Intrahepatic collaterals, on gray-scale images, show as

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FIG. 4.36  Budd-Chiari Syndrome.  Abnormal hepatic vein appearance in three patients on transverse images of intrahepatic inferior vena cava. (A) Right hepatic vein is not seen at all. Middle and left hepatic veins show tight strictures just proximal to the inferior vena cava. (B) Right hepatic vein is seen as a thrombosed cord. Middle hepatic vein does not reach the inferior vena cava. Left hepatic vein is not seen. (C) Only a single hepatic vein, the middle hepatic vein, can be seen as a thrombosed cord.

FIG. 4.37  Budd-Chiari Syndrome.  Abnormal intrahepatic collaterals on gray-scale sonograms in two patients. Both images show vessels with abnormal locations and increased tortuosity compared with the normal intrahepatic vasculature.

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FIG. 4.38  Budd-Chiari Syndrome.  (A) Gray-scale transverse image of hepatic venous confluence shows complete absence of the right hepatic vein with obliteration of the lumen of a common trunk for the middle and left hepatic veins. (B) Color Doppler image shows that blood flow in the middle hepatic vein (blue) is normally directed toward the inferior vena cava. As the trunk is obliterated, all the blood is flowing out of the left hepatic vein (red), which is abnormal. Other images showed anastomoses of the left hepatic vein with surface collaterals. (C) Color Doppler image shows an anomalous left hepatic vein with flow to the inferior vena cava (normal direction) and aliasing from a long stricture. (D) Spectral Doppler waveform of the anomalous left hepatic vein shows a very high abnormal velocity of approximately 140 cm/sec, confirming the tight stricture.

tubular vascular structures in an abnormal location and typically are seen extending from a hepatic vein to the liver surface, where they anastomose with systemic capsular vessels. Duplex Doppler ultrasound and color Doppler flow imaging (CDFI) can help determine both the presence and the direction of hepatic venous flow in the evaluation of patients with suspected Budd-Chiari syndrome. The middle and left hepatic veins are best scanned in the transverse plane at the level of the xiphoid process. The right hepatic vein is best evaluated from a right intercostal approach.105 The intricate pathways of blood flow out of the liver in the patient with Budd-Chiari syndrome can be mapped with documentation of hepatic venous occlusions,

hepatic-systemic collaterals, hepatic venous–portal venous collaterals, and increased caliber of anomalous or accessory hepatic veins. The normal blood flow in the IVC and hepatic veins is phasic in response to both the cardiac and respiratory cycles.100 In Budd-Chiari syndrome, flow in the IVC, hepatic veins, or both, changes from phasic to absent, reversed, turbulent, or continuous.104,112 Continuous flow has been called the pseudoportal Doppler signal and appears to reflect either partial IVC obstruction or extrinsic IVC compression.103 The portal blood flow also may be affected and is characteristically either slowed or reversed.104

CHAPTER 4  The Liver

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IVC

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FIG. 4.39  Budd-Chiari Syndrome With Extensive Inferior Vena Cava Thrombosis.  (A) Sagittal image of the inferior vena cava (IVC) shows that it is distended with echogenic thrombus. (B) Middle hepatic vein as a thrombosed cord. (C) Gray-scale image of right hepatic vein (RHV) and (D) color Doppler image show that anomalous right hepatic vein is distended with thrombus. There is flow in the vein proximal to the thrombus.

The use of Doppler in the patient with suspected Budd-Chiari syndrome lends strong supportive evidence to the gray-scale impression of missing, compressed, or otherwise abnormal hepatic veins and IVC.102,112 Associated reversal of flow in the portal vein and epigastric collaterals is also optimally assessed with this technique.112 Hepatic veno-occlusive disease causes progressive occlusion of the small hepatic venules. The disease is endemic in Jamaica, secondary to alkaloid toxicity from bush tea. In North America, most cases are iatrogenic, secondary to hepatic irradiation and chemotherapy used in bone marrow transplantation.101 Patients with hepatic veno-occlusive disease are clinically indistinguishable from those with Budd-Chiari syndrome. Duplex Doppler

sonography demonstrates normal caliber, patency, and phasic forward (toward the heart) flow of the main hepatic veins and IVC.101 Flow in the portal vein, however, may be abnormal, showing either reversed or “to and fro” flow.101,113 In addition, the diagnosis of hepatic veno-occlusive disease may be suggested in a patient with decreased portal blood flow (compared with baseline measurement before ablative therapy).101

Portal Vein Aneurysm Aneurysms of the portal vein are rare. Their origin is either congenital or acquired secondary to portal hypertension. Portal vein aneurysms have been described proximally at the junction of the superior mesenteric and splenic veins and distally involving

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the portal venous radicles. The sonographic appearance is that of a vascular mass connected to the portal system with turbulent flow.

Intrahepatic Portosystemic Venous Shunts Intrahepatic arterial-portal fistulas are well-recognized complications of large-gauge percutaneous liver biopsy and trauma. Conversely, intrahepatic portohepatic venous shunts are rare. Their cause is controversial and believed to be either congenital or related to portal hypertension.114,115 Patients typically are middle aged and present with hepatic encephalopathy. Anatomically, portohepatic venous shunts are more common in the right lobe. Sonography demonstrates a tortuous tubular vessel or complex vascular channels, which connect a branch of the portal vein to a hepatic vein or the IVC.114-116 The diagnosis is confirmed angiographically.

Aneurysm, Pseudoaneurysm, and Dissection The hepatic artery is the fourth most common site of an intraabdominal aneurysm, following the infrarenal aorta, iliac, and splenic arteries. Eighty percent of patients with a hepatic artery aneurysm experience catastrophic rupture into the peritoneum, biliary tree, gastrointestinal tract, or portal vein.117 Hepatic artery pseudoaneurysm secondary to chronic pancreatitis has been described. The duplex Doppler sonographic examination revealed turbulent arterial flow within a sonolucent mass.117 Primary dissection of the hepatic artery is rare and in most cases leads to death before diagnosis.118 Sonography may show the intimal flap with the true and false channels.

Hereditary Hemorrhagic Telangiectasia Hereditary hemorrhagic telangiectasia, or Osler-Weber-Rendu, is an autosomal dominant disorder that causes arteriovenous (AV) malformations in the liver, hepatic fibrosis, and cirrhosis. Patients present with multiple telangiectasias and recurrent

A

episodes of bleeding. Sonographic findings include a large feeding common hepatic artery up to 10 mm, multiple dilated tubular structures representing AV malformations, and large draining hepatic veins secondary to AV shunting.119

Peliosis Hepatis Peliosis hepatis is a rare liver disorder characterized by blood-filled cavities ranging from less than a millimeter to many centimeters in diameter. It can be distinguished from hemangioma by the presence of portal tracts within the fibrous stroma of the blood spaces. The pathogenesis of peliosis hepatis involves rupture of the reticulin fibers that support the sinusoidal walls, secondary to cell injury or nonspecific hepatocellular necrosis. The diagnosis of peliosis can be made with certainty only by histologic examination. Most cases of peliosis affect the liver, although other solid internal organs and lymph nodes may be involved in the process as well. Although early reports described incidental detection of peliosis hepatis at autopsy in patients with chronic wasting disorders, it has now been seen following renal and liver transplantation, in association with a multitude of drugs, especially anabolic steroids, and with an increased incidence in patients with HIV.119 The HIV association may occur alone or as part of bacillary angiomatosis in the spectrum of opportunistic infections of AIDS.120 Peliosis hepatis has the potential to be aggressive and lethal. The imaging features of peliosis hepatis have been described in single case reports,121-123 although often without adequate histologic confirmation. Angiographically, the peliotic lesions have been described as accumulations of contrast detected late in the arterial phase and becoming more distinct in the parenchymal phase.124 On sonography, described lesions are nonspecific and have shown single or multiple masses of heterogeneous echogenicity.119,120,125 Calcifications have been reported125 (Fig. 4.40). Peliosis hepatis is difficult to diagnose both clinically and radiologically and must be suspected in a susceptible individual with a liver mass.

B

FIG. 4.40  Peliosis Hepatis.  Peliosis hepatis in 34-year-old woman with deteriorating liver function necessitating transplantation. (A) Sagittal right lobe and (B) sagittal left lobe scans show multiple large liver masses with innumerable tiny punctate calcifications. (With permission from Muradali D, Wilson SR, Wanless IR, et al. Peliosis hepatis with intrahepatic calcifications. J Ultrasound Med. 1996;15[3]:257-260.125)

CHAPTER 4  The Liver

HEPATIC MASSES Focal liver masses include a variety of malignant and benign neoplasms, as well as masses with developmental, inflammatory, and traumatic causes. In cross-sectional imaging, two basic issues relate to a focal liver lesion: characterization of a known liver lesion (what is it?) and detection (is it there?). The answer to either question requires a focused examination, often adjusted according to the clinical situation.

Liver Mass Characterization Characterization of a liver mass on conventional sonography is based on the appearance of the mass on gray-scale imaging and vascular information derived from spectral, color, and power Doppler sonography. With excellent spatial and contrast resolution, the gray-scale morphology of a mass allows for the differentiation of cystic and solid masses, and characteristic appearances may suggest the correct diagnosis without further evaluation. Often, however, definitive diagnosis is not based on gray-scale information alone, but on vascular information obtained on conventional Doppler ultrasound examination. However, conventional Doppler often fails in the evaluation of a focal liver mass, particularly in a large patient or on a small or deep liver lesion, or on a mass with inherent weak Doppler signals. Motion artifact is also highly problematic for abdominal Doppler ultrasound studies, and a left lobe liver mass close to the pulsation of the cardiac apex, for example, can limit assessment by conventional Doppler. For these reasons, conventional ultrasound is not regarded highly for characterization of focal liver masses, and a mass detected on ultrasound is historically evaluated further with CECT or MRI for definitive characterization.

Role of Microbubble Contrast Agents Worldwide, noninvasive diagnosis of focal liver masses is achieved with CECT and MRI based on recognized enhancement patterns in the arterial and portal venous phases. These noninvasive methods of characterization have become so accurate that excisional and percutaneous biopsy for diagnosis of liver masses is now rarely performed. In recent years, however, CEUS has joined the ranks of CT and MRI in providing similar diagnostic information as well as information unique to CEUS.126 Injection of a microbubble contrast agent to enhance the Doppler signal from blood and imaging with a specialized imaging technique such as pulse inversion sonography allow for preferential detection of the signal from the contrast agent while suppressing the signal from background tissue. Ultrasound contrast agents currently in use are secondgeneration agents comprising tiny bubbles of a perfluorocarbon gas contained within a stabilizing shell. Microbubble contrast agents are blood pool agents that do not diffuse through the vascular endothelium. This is of potential importance when imaging the liver because comparable contrast agents for CT and MRI may diffuse into the interstitium of a tumor. Our personal experience with perfluorocarbon microbubble agents is largely based on the use of Definity (Lantheus Medical Imaging, Billerica, MA) and brief exposure to Optison (GE Healthcare,

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Milwaukee, WI).127,128 We routinely perform CEUS for characterization of incidentally detected liver masses, those found on surveillance scans of patients at risk for HCC, and any focal mass referred by our clinicians found on outside imaging or indeterminate on CT and MRI.129 Microbubble contrast agents for ultrasound are unique in that they interact with the imaging process.127 The major determinant of this interaction is the peak negative pressure of the transmitted ultrasound pulse, reflected by the mechanical index (MI). The bubbles show stable, nonlinear oscillation when exposed to an ultrasound field with a low MI, with the production of harmonics of the transmitted frequency, including the frequency double that of the sound emitted by the transducer, the second harmonic. When the MI is raised sufficiently, the bubbles undergo irreversible disruption, with the production of a brief but bright, high-intensity ultrasound signal (see Chapter 3). Liver lesion characterization with microbubble contrast agents is based on lesional vascularity and lesional enhancement in the arterial phase (10-40 sec), portal venous phase (40-90 sec), and late phase (up to 5 minutes). Lesional vascularity assessment depends on continuous imaging of the agents while they are within the vascular pool. We document the presence, number, distribution, and morphology of any lesional vessels. A low MI is essential because it will preserve the contrast agent population without destruction of the bubbles in the imaging field, allowing for prolonged periods of real-time observation. The morphology of the lesional vessels is discriminatory and facilitates the diagnosis of liver lesions (Fig. 4.41). Lesional enhancement is best determined by comparing the echogenicity of the lesion to the echogenicity of the liver at a similar depth on the same frame and requires knowledge of liver blood flow. The liver has a dual blood supply from the hepatic artery and portal vein. The liver derives a larger proportion of its blood from the portal vein, whereas most liver tumors derive their blood supply from the hepatic artery. At the initiation of the injection, the low-MI technique will cause the entire field of view (FOV) to appear virtually black, regardless of the baseline appearance of the liver and the lesion in question. In fact, a known mass may be invisible at this point. As the microbubbles arrive in the FOV, the discrete vessels in the liver and then those within a liver lesion will be visualized, followed by increasing generalized enhancement as the microvascular volume of liver and lesion fills with the contrast agent. The liver parenchyma will appear more echogenic in the arterial phase than at baseline, and even more enhanced in the portal venous phase, as a reflection of its blood flow. Vascularity and enhancement patterns of a liver lesion, by comparison, will therefore reflect the actual blood flow and hemodynamics of the lesion in question, such that a hyperarterialized mass will appear more enhanced against a less enhanced liver on an arterial phase sequence. Conversely, a hypoperfused lesion will appear as a dark or hypoechoic region within the enhanced liver on an arterial phase sequence. Currently, evaluation of lesional enhancement is usually performed with the low-MI technique just described. However, details of vessel morphology and lesional enhancement are even more sensitively assessed using a bubble-tracking technique called maximum-intensity projection (MIP) imaging.130 In this

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FIG. 4.41  Early Arterial Phase Vascular Morphology.  Shown on real-time dynamic ultrasound, this is contributory to diagnosis of focal liver masses. (A) Stellate vessels are highly suggestive of focal nodular hyperplasia. (B) Peripheral discontinuous nodular enhancement without linear vascularity suggests hemangioma. (C) Rim enhancement has a high association with malignant disease, especially metastases and cholangiocarcinoma. (D) Dysmorphic tortuous vessels are suggestive of malignant tumors, in this case a hepatocellular carcinoma. The filling from the periphery, as here, is common for this diagnosis.

technique, performed either at wash-in of contrast or at the peak of arterial phase enhancement, a brief high-MI exposure will destroy all the bubbles within the FOV. Sequential frames, as the lesion and liver are reperfused, will track the bubble course providing exquisite resolution (Fig. 4.42, Videos 4.5 and 4.6). There are established algorithms for the diagnosis of focal liver masses with CEUS, with similarities to CT and MRI algorithms but also important differences131-133 (Table 4.3). Diagnosis of benign liver masses, hemangioma, and focal nodular hyperplasia (FNH) is extremely accurate showing characteristic features of enhancement in the arterial phase and sustained enhancement in the portal venous phase (Fig. 4.43),

such that their enhancement equals or exceeds the enhancement of the adjacent liver. Malignant tumors, by comparison, tend to show washout, such that the tumor appears unenhanced in the portal venous phase of enhancement (Fig. 4.44). Exceptions to this general rule include frequent washout of benign hepatic adenoma and delayed or no washout of HCC. Discrimination of benign and malignant liver masses has similar high accuracy.134

Liver Mass Detection Excellent spatial resolution allows small lesions to be well seen on sonography. Therefore it is not size but echogenicity that

CHAPTER 4  The Liver

FIG. 4.42  Normal Liver Vasculature.  Temporal maximum-intensity projection image shows accumulated enhancement in 11 seconds after contrast material arrives in liver. Depiction of vessel structure to fifth-order branching is evident. Focal unenhanced region (arrow) is slowly perfusing hemangioma. (With permission from Wilson S, Jang H, Kim T, et al. Real-time temporal maximum-intensity-projection imaging of hepatic lesions with contrast-enhanced sonography. AJR Am J Roentgenol. 2008;190[3]:691-695.130)

determines lesion conspicuity on a sonogram. That is, a tiny mass of only a few millimeters will be easily seen if it is increased or decreased in echogenicity compared with the adjacent liver parenchyma. Because many metastases are either hypoechoic or hyperechoic relative to the liver, a careful examination should allow for their detection. Nonetheless, many metastatic lesions are of similar echogenicity to the background liver, making their detection difficult or impossible, even if they are of a substantial size. This occurs when the backscatter from the lesion is virtually identical to the backscatter from the liver parenchyma. To combat this inherent problem of lack of contrast between many metastatic liver lesions and the background liver on conventional sonography, contrast-enhanced liver ultrasound is helpful (Fig. 4.45). CEUS increases the backscatter from the liver compared with the liver lesions, thereby improving their detection. This occurs rapidly following the arterial phase of enhancement and generally lasts for several minutes beginning in the portal venous and persisting for the late phase. Of historic interest is the use of the first-generation contrast agent Levovist (Schering AG, Berlin). After clearance of the contrast agent from the vascular pool, the microbubble persisted in the liver, probably within the Kupffer cells on the basis of phagocytosis. A high-MI sweep through the liver produced bright enhancement in the distribution of the bubbles. Therefore all normal liver enhances. Liver metastases, lacking Kupffer cells,

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do not enhance and therefore show as black or hypoechoic holes within the enhanced parenchyma135 (Fig. 4.45A and B). In a multicenter study conducted in Europe and Canada, more and smaller lesions were seen than on baseline scan.136 Overall, lesion detection was equivalent to that of CT and MRI. The decibel difference between the lesions and the liver parenchyma is increased many fold because of increased backscatter from contrast agent within the normal liver tissue. Although many results were compelling, these first-generation contrast agents are no longer marketed. Today, current requirements for improved lesion detection use a similar technique of CEUS with a perfluorocarbon contrast agent and low-MI scanning in both the arterial and the portal venous phase. The use of a low-MI imaging technique for lesion detection has advantages in terms of scanning because the microbubble population is preserved and timing is not so critical. Virtually all metastases will be unenhanced relative to the liver in the portal and the late phase and the liver parenchyma will remain optimally enhanced. Therefore malignant lesions tend to appear hypoechoic in the portal phase, allowing for improved lesion detection (Fig. 4.45C and D). This observation, that malignant lesions tend to be hypoechoic in the portal venous phase of perfluorocarbon liver enhancement, is helpful for both lesion detection and lesion characterization. Enhancement of benign lesions, FNH, and hemangioma generally equals or exceeds liver enhancement in the portal venous phase. Detection of hypervascular liver masses (e.g., HCC, metastases) is also improved by scanning with perfluorocarbon agents in the arterial phase. These lesions will generally show as hyperechoic masses relative to the liver parenchyma in the arterial phase because they are predominantly supplied by hepatic arterial flow.

HEPATIC NEOPLASMS Sonographic visualization of a focal liver mass may occur in a variety of clinical scenarios, ranging from incidental detection to identification in a symptomatic patient or as part of a focused search in a patient at risk for hepatic neoplasm. Hemangiomas, FNH, and adenomas are the benign neoplasms typically encountered in the liver, whereas HCC and metastases account for the majority of malignant tumors. The role of imaging in the evaluation of an identified focal liver mass is to determine which masses are potentially clinically important, requiring confirmations of their diagnoses, and which masses are likely to be insignificant and benign, not requiring further evaluation to confirm their nature. On a sonographic study, there is considerable overlap in the appearances of focal liver masses. Once a liver mass is seen, however, the excellent contrast and spatial resolution of state-of-the-art ultrasound equipment have provided guidelines for the initial management of patients, which include recognition of the following features: • A hypoechoic halo identified around an echogenic or isoechoic liver mass is an ominous sonographic sign necessitating definitive diagnosis. • A hypoechoic and solid liver mass is highly likely to be significant and also requires definitive diagnosis.

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TABLE 4.3  Schematic of Algorithm for Liver Mass Diagnosis on Contrast-Enhanced Ultrasound

Hemangioma

or

AP Peripheral nodular enhancement Centripetal progression of enhancement PVP Complete or partial fill-in AP Centrifugal hypervascular enhancement Stellate arteries PVP Sustained enhancement Hypoechoic central scar

FNH

AP Diffuse or centripetal hypervascular enhancement Dysmorphic arteries

Adenoma

or

AP Rim enhancement Diffuse hypervascular Hypovascular

or

Metastases

or

Arterial phase (AP) (+) Enhancement

PVP Sustained enhancement Soft wash out

PVP Fast washout

Portal venous phase (PVP) Soft wash out

(–) enhancement (wash out)

AP, Arterial phase; FNH, focal nodular hyperplasia; PVP, portal venous phase. With permission from Wilson SR, Burns PN. Microbubble-enhanced US in body imaging: what role? Radiology. 2010;257(1):24-39.148

• Multiple solid liver masses may be significant and suggest possible metastatic or multifocal malignant liver disease. However, hemangiomas are also frequently multiple. • Clinical history of malignancy, chronic liver disease or hepatitis, and symptoms referable to the liver are requisite information for interpretation of a focal liver lesion.

Benign Hepatic Neoplasms Cavernous Hemangioma Cavernous hemangiomas are the most common benign tumors of the liver, occurring in approximately 4% of the population. They occur in all age groups but are more common in adults, particularly women, with a female-to-male ratio of approximately 5:1. Histologically, hemangiomas consist of multiple vascular channels that are lined by a single layer of endothelium and

separated and supported by fibrous septa. The vascular spaces may contain thrombi. The vast majority of hemangiomas are small, asymptomatic, and discovered incidentally. Large lesions may, in rare cases, produce symptoms of acute abdominal pain, caused by hemorrhage or thrombosis within the tumor. Thrombocytopenia, caused by sequestration and destruction of platelets within a large cavernous hemangioma (Kasabach-Merritt syndrome), occasionally occurs in infants and is rare in adults. Traditional teaching suggests that once identified in the adult, hemangiomas usually have reached a stable size, rarely changing in appearance or size.137,138 In our practice, however, we have documented substantial growth of some lesions over many years of follow-up. Hemangiomas may enlarge during pregnancy or with the administration of estrogens, suggesting the tumor is hormone dependent.

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FIG. 4.43  Sustained enhancement in the portal venous phase, on contrast-enhanced ultrasound (CEUS) and contrast-enhanced computed tomography (CECT) scan, suggestive of a benign mass. (A) and (C) are arterial phase images on CT and CEUS, respectively, both showing arterial phase hyperenhancement. (B) and (D) are portal venous phase images on CT and CEUS, respectively, both showing sustained enhancement and a nonenhanced scar. This sustained enhancement is concordant on the two scans and suggests a benign tumor. This is a confirmed FNH. See also Video 4.5. (With permission from Wilson S, Greenbaum L, Goldberg B. Contrast-enhanced ultrasound: what is the evidence and what are the obstacles? AJR Am J Roentgenol. 2009;193[1]:55-60.129)

The sonographic appearance of cavernous hemangioma varies. Typically the lesion is small ( 3 cm Internal soft tissue Mural or septal thickening

including symptomatic patients, growth of the cyst on serial studies, tumor greater than 3 cm in diameter, internal soft tissue, and mural or septal thickening. Multiple societies have proposed algorithms to follow incidentally detected pancreatic cysts,155 but there is a great deal of uncertainty in this process,156,157 and future assessment may rely on novel tumor markers and molecular analysis rather than cross-sectional imaging morphology.158 Data from 2015 suggest that pancreatic cysts found incidentally by using CT or MRI may be associated with increased mortality for patients younger than 65 years and an overall increased risk of pancreatic adenocarcinoma.159

Simple Pancreatic Cysts Simple pancreatic cysts are rare in the general population, with a prevalence of 0.2%160 to 1.2%.151 These low percentages may underestimate true prevalence because imaging161 and autopsy162 studies have recorded a substantially higher prevalence, about 20% and 24.3%, respectively. Our experience suggests that the lower prevalence rates are closer to the actual experience in clinical imaging. Detecting a simple pancreatic cyst should raise suspicion of an inherited disease that has a high prevalence of

cysts, such as autosomal dominant polycystic kidney disease (ADPKD)163 or von Hippel–Lindau (VHL) disease.164 Multiple pancreatic cysts can also occur in individuals with cystic fibrosis.165 Multiple pancreatic cysts are more common in VHL disease than in ADPKD. Prevalence of pancreatic cysts in patients with VHL ranges from 50% to 90%, making pancreatic cysts the most common type of lesion in VHL disease.164 Thus multiple simple pancreatic cysts should suggest the diagnosis of VHL (Fig. 7.75). In addition to simple cysts, other pancreatic lesions associated with VHL include serous cystic neoplasm and pancreatic endocrine tumors, with a slightly increased risk of ductal adenocarcinoma.164

Cystic Neoplasms Cystic tumors of the pancreas account for about 10% of cystic pancreatic lesions. Although most solid tumors are ductal adenocarcinomas with a poor prognosis, cystic tumors are usually either benign lesions or low-grade malignancies. Malignant cystic tumors account for about 1% of all pancreatic malignancies.73 Mucinous tumors such as intraductal papillary mucinous neoplasm and mucinous cystic neoplasm are often malignant. The risk of malignancy is greater in older individuals. Reliable prevalence data are difficult to find166 but are estimated in Table 7.4.

Serous Cystic Neoplasm Serous cystic neoplasm, previously known as microcystic adenoma, is typically a benign tumor, although a few invasive, malignant examples have been reported.73,166 Serous cystic neoplasm occurs more frequently in women and is most often found in the pancreatic head.154 These lesions are composed of myriad tiny cysts, generally too small to be individually resolved sonographically (Fig. 7.76). The multiple reflective interfaces caused by the walls of the tiny cysts leads to an echogenic appearance, analogous to that of autosomal recessive polycystic kidney disease. Through transmission is usual. Larger cysts (1-3 cm in diameter) often are present at the periphery of the lesion. A radially oriented, fibrous pattern occurs in a minority of patients,149 and a central calcification is often present (30%50%) (Fig. 7.77). Small lesions (5 cm

10%

90% 100% 50%-60% 100% Nonhyperfunctioning

All tumors VIP, Vasoactive intestinal polypeptide.

SMA SMV

Ao

Stent

IVC

FIG. 7.84  Pancreatic Endocrine Tumor, Nonhyperfunctioning.  Longitudinal oblique color Doppler sonogram shows 5-cm, hypoechoic malignant tumor large enough to cause bile duct obstruction, requiring stenting. Internal color flow is typical with pancreatic endocrine tumors. Ao, Aorta; IVC, interior vena cava; SMA, superior mesenteric artery; SMV, superior mesenteric vein.

Unusual and Rare Neoplasms FIG. 7.83  Insulinoma on Intraoperative Ultrasound.  This 10-mm lesion was discovered because of hyperinsulinism. (Courtesy of Dr. Hisham Tchelepi.)

clinically—because of pain,185 mass effect, or, if malignant, invasion and metastasis119 (Fig. 7.84). Incidental detection of smaller, nonhyperfunctioning tumors is becoming more frequent (Fig. 7.85). These tumors are usually well defined and round or oval. They generally appear hypoechoic compared to the normal parenchyma. These tumors may have cystic changes and calcification.187 The larger, nonhyperfunctioning pancreatic endocrine tumors may be difficult to differentiate from the more common pancreatic ductal adenocarcinoma. Sonographic findings that suggest the diagnosis are (1) prominent internal color flow (rare in carcinoma), (2) lack of biliary or pancreatic ductal dilation in a pancreatic head lesion, and (3) lack of progression or metastasis on serial imaging.

On ultrasound, many histologic variants of pancreatic ductal adenocarcinoma are indistinguishable from tumors with the usual histologic features. These include adenosquamous cell carcinoma, anaplastic carcinoma, and pleomorphic giant cell carcinoma. Acinar cell carcinoma and pleomorphic giant cell carcinoma, although often indistinguishable from ductal adenocarcinoma, may be larger and may exhibit central necrosis. Primary pancreatic lymphoma is prohibitively rare, although adenopathy or diffuse involvement from more generalized disease occurs with some frequency.120 Other rare pancreatic tumors include connective tissue–origin tumors (sarcomas), pancreaticoblastomas, dysontogenetic cysts, and metastases.190,191

Lipoma In contrast to the usual echogenic appearance of fat and fatty lesions, pancreatic lipomas are usually hypoechoic192,193 (Fig. 7.86). Other lipomas may have a mixed appearance, with a variable amount of internal echoes, or they may appear hyperechoic. The cause of hypoechoic fat is not known but may involve the number

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Stomach

LK

Spleen

A

Pancreas tail

B

C

D

FIG. 7.85  Small, Nonhyperfunctioning Pancreatic Endocrine Tumors.  (A) Transverse sonogram shows 9-mm hypoechoic nonhyperfunctioning pancreatic endocrine tumor (arrow) discovered incidentally during an abdominal ultrasound. The pancreatic tail was removed. (B) and (C) In another patient, gray-scale (B) and color Doppler (C) sonograms show 2-cm hypervascular pancreatic endocrine tumor indenting the superior mesenteric artery (arrow). (D) In another patient, intraoperative ultrasound shows a 9-mm lesion (arrows) that was discovered incidentally. Marked dilation of the pancreatic duct is noted and can be a hallmark of serotonin-secreting pancreatic endocrine tumors. Intraoperative ultrasound is considered essential in many institutions for the surgical management of pancreatic endocrine tumors. PD, Pancreatic duct.

L L

A

B

FIG. 7.86  Pancreatic Lipoma.  (A) Transverse sonogram of almost anechoic pancreatic lipoma (L). In contrast to the usual echogenic appearance of fat and fatty lesions, pancreatic lipomas are usually hypoechoic. (B) Computed tomography image confirms the fatty nature of the lesion. (Courtesy of Dr. Vinay Duddlewar.)

CHAPTER 7  The Pancreas

FIG. 7.87  Lung Carcinoma Metastasis to Pancreas.  Longitudinal sonogram shows typical hypoechoic metastasis (arrow). Pancreatic metastases are the most common pancreatic neoplasm in autopsy series but are rarely found clinically because they generally occur late with widespread metastatic disease.

of blood vessels, amount and thickness of connective tissue stroma, number of fibrous septae that separate fat lobules, and amount of water content in the fat.192,194

Metastatic Tumors In autopsy series, metastasis is the most common pancreatic neoplasm, found about four times as often as pancreatic cancer.191 Clinical discovery of metastasis was rare until the advent of modern imaging.195 Pancreatic metastases are rarely clinically significant because they generally occur late in patients with widespread metastatic disease. Primary tumors that most often metastasize to the pancreas include renal cell carcinoma, breast carcinoma, lung carcinoma (Fig. 7.87), melanoma, colon carcinoma, and stomach carcinoma.120,191,195 With metastasis to the pancreas, there may be a long interval between initial diagnosis of the primary lesion and discovery of the metastasis. This is especially true of renal cell carcinoma and, to a lesser degree, melanoma. Klein et al.195 found that the mean delay between discovery of the primary renal cell carcinoma and metastasis was 10 years; the longest interval was more than 24 years. A classic scenario is the discovery of a hypervascular mass (or masses) in the pancreas of a patient who had a remote, presumably cured renal cell carcinoma (Fig. 7.88). Differential diagnosis from a hypervascular pancreatic endocrine tumor may be difficult in such cases.

CONTRAST-ENHANCED ULTRASOUND Contrast-enhanced ultrasound (CEUS) shows promise as a technique that will be beneficial in both endoscopic ultrasound and transabdominal ultrasound of the pancreas. Historically, CEUS was best considered an experimental technique.98,196

251

FIG. 7.88  Renal Cell Carcinoma Metastasis to Pancreas.  Longitudinal color Doppler sonogram shows hypervascular metastasis. Differentiation from a hypervascular pancreatic endocrine tumor may be difficult in these cases.

However, more recent data suggest that CEUS may become much more routine.197-199 Fan states, “CEUS has obvious superiority over conventional US in the general diagnostic accuracy of solid pancreatic lesions and in the diagnostic consistency among doctors. The performances of CEUS are similar to that of CECT in the diagnosis of pancreatic carcinoma and focal pancreatitis.”200 CEUS might be helpful in diagnosing pancreatic necrosis in patients with severe acute pancreatitis.147

Acknowledgment The authors would like to acknowledge Dr. Philip Ralls, the prior author of this chapter. His supreme dedication and passion for quality ultrasound practice and education in all areas was exemplary, and his images and text form the backbone of this updated version. REFERENCES 1. Harisinghani MG, Saini S, Schima W, et al. Simethicone coated cellulose as an oral contrast agent for ultrasound of the upper abdomen. Clin Radiol. 1997;52(3):224-226. 2. Lev-Toaff AS, Langer JE, Rubin DL, et al. Safety and efficacy of a new oral contrast agent for sonography: a phase II trial. AJR Am J Roentgenol. 1999;173(2):431-436. 3. Abu-Yousef MM, El-Zein Y. Improved US visualization of the pancreatic tail with simethicone, water, and patient rotation. Radiology. 2000;217(3):780-785. 4. Mori H, McGrath FP, Malone DE, Stevenson GW. The gastrocolic trunk and its tributaries: CT evaluation. Radiology. 1992;182(3):871-877. 5. Winter 3rd TC. “Proximal” versus “distal” in the pancreas. Radiographics. 2013;33(2):622-623. 6. Glaser J, Stienecker K. Pancreas and aging: a study using ultrasonography. Gerontology. 2000;46(2):93-96. 7. Guerra M, Gutiérrez L, Carrasco R, Arroyo A. Size and echogenicity of the pancreas in Chilean adults: echotomography study in 261 patients]. Rev Med Chil. 1995;123(6):720-726.

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117. Lowenfels AB, Maisonneuve P, Cavallini G, et al. Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N Engl J Med. 1993;328(20):1433-1437. 118. Lowenfels AB, Maisonneuve P. Risk factors for pancreatic cancer. J Cell Biochem. 2005;95(4):649-656. 119. Ross WA, Bismar MM. Evaluation and management of periampullary tumors. Curr Gastroenterol Rep. 2004;6(5):362-370. 120. Faria SC, Tamm EP, Loyer EM, et al. Diagnosis and staging of pancreatic tumors. Semin Roentgenol. 2004;39(3):397-411. 121. Elsayes KM, Narra VR, Abou El Abbass HA, et al. Pancreatic tumors: diagnostic patterns by 3D gradient-echo post contrast magnetic resonance imaging with pathologic correlation. Curr Probl Diagn Radiol. 2006;35(4):125-139. 122. American Cancer Society. Cancer facts & figures. Atlanta: ACS; 2008. 123. Canto MI, Goggins M, Hruban RH, et al. Screening for early pancreatic neoplasia in high-risk individuals: a prospective controlled study. Clin Gastroenterol Hepatol. 2006;4(6):766-781. 124. Klein AP, Hruban RH, Brune KA, et al. Familial pancreatic cancer. Cancer J. 2001;7(4):266-273. 125. Wilkowski R, Thoma M, Bruns C, et al. Chemoradiotherapy with gemcitabine and continuous 5-FU in patients with primary inoperable pancreatic cancer. JOP. 2006;7(4):349-360. 126. Conlon KC, Klimstra DS, Brennan MF. Long-term survival after curative resection for pancreatic ductal adenocarcinoma. Clinicopathologic analysis of 5-year survivors. Ann Surg. 1996;223(3):273-279. 127. Klek S, Kulig J, Popiela T, et al. The value of modern ultrasonographic techniques and computed tomography in detecting and staging of pancreatic carcinoma. Acta Chir Belg. 2004;104(6):659-667. 128. Gudjonsson B. Carcinoma of the pancreas: critical analysis of costs, results of resections, and the need for standardized reporting. J Am Coll Surg. 1995;181:483-503. 129. Gudjonsson B. Survival statistics gone awry: pancreatic cancer, a case in point. J Clin Gastroenterol. 2002;35(2):180-184. 130. Wade TP, el-Ghazzawy AG, Virgo KS, Johnson FE. The Whipple resection for cancer in U.S. Department of Veterans Affairs Hospitals. Ann Surg. 1995;221(3):241-248. 131. Farnell MB, Nagorney DM, Sarr MG. The Mayo clinic approach to the surgical treatment of adenocarcinoma of the pancreas. Surg Clin North Am. 2001;81(3):611-623. 132. Tamm EP, Bhosale PR, Lee JH. Pancreatic ductal adenocarcinoma: ultrasound, computed tomography, and magnetic resonance imaging features. Semin Ultrasound CT MR. 2007;28(5):330-338. 133. Karlson BM, Ekbom A, Lindgren PG, et al. Abdominal US for diagnosis of pancreatic tumor: prospective cohort analysis. Radiology. 1999;213(1):107-111. 134. Campbell JP, Wilson SR. Pancreatic neoplasms: how useful is evaluation with US? Radiology. 1988;167(2):341-344. 135. Kosmahl M, Pauser U, Anlauf M, Kloppel G. Pancreatic ductal adenocarcinomas with cystic features: neither rare nor uniform. Mod Pathol. 2005;18(9):1157-1164. 136. Pappas S, Federle MP, Lokshin AE, Zeh 3rd HJ. Early detection and staging of adenocarcinoma of the pancreas. Gastroenterol Clin North Am. 2007;36(2):413-429, x. 137. Gress FG, Hawes RH, Savides TJ, et al. Role of EUS in the preoperative staging of pancreatic cancer: a large single-center experience. Gastrointest Endosc. 1999;50(6):786-791. 138. Boujaoude J. Role of endoscopic ultrasound in diagnosis and therapy of pancreatic adenocarcinoma. World J Gastroenterol. 2007;13(27):3662-3666. 139. Kalra MK, Maher MM, Mueller PR, Saini S. State-of-the-art imaging of pancreatic neoplasms. Br J Radiol. 2003;76(912):857-865. 140. Nino-Murcia M, Tamm EP, Charnsangavej C, Jeffrey Jr RB. Multidetector-row helical CT and advanced postprocessing techniques for the evaluation of pancreatic neoplasms. Abdom Imaging. 2003;28(3):366-377. 141. Vargas R, Nino-Murcia M, Trueblood W, Jeffrey Jr RB. MDCT in pancreatic adenocarcinoma: prediction of vascular invasion and resectability using a multiphasic technique with curved planar reformations. AJR Am J Roentgenol. 2004;182(2):419-425. 142. Angeli E, Venturini M, Vanzulli A, et al. Color Doppler imaging in the assessment of vascular involvement by pancreatic carcinoma. AJR Am J Roentgenol. 1997;168(1):193-197.

143. Ralls PW, Wren SM, Radin R, et al. Color flow sonography in evaluating the resectability of periampullary and pancreatic tumors. J Ultrasound Med. 1997;16(2):131-140. 144. Tomiyama T, Ueno N, Tano S, et al. Assessment of arterial invasion in pancreatic cancer using color Doppler ultrasonography. Am J Gastroenterol. 1996;91(7):1410-1416. 145. Wren SM, Ralls PW, Stain SC, et al. Assessment of resectability of pancreatic head and periampullary tumors by color flow Doppler sonography. Arch Surg. 1996;131(8):812-817. 146. Ishida H, Konno K, Hamashima Y, et al. Assessment of resectability of pancreatic carcinoma by color Doppler sonography. Abdom Imaging. 1999;24(3):295-298. 147. Rickes S, Malfertheiner P. Echo-enhanced sonography—an increasingly used procedure for the differentiation of pancreatic tumors. Dig Dis. 2004;22(1):32-38. 148. Fernández-del Castillo C, Targarona J, Thayer SP, et al. Incidental pancreatic cysts: clinicopathologic characteristics and comparison with symptomatic patients. Arch Surg. 2003;138(4):427-434. 149. Edirimanne S, Connor SJ. Incidental pancreatic cystic lesions. World J Surg. 2008;32(9):2028-2037. 150. Sahani DV, Saokar A, Hahn PF, et al. Pancreatic cysts 3 cm or smaller: how aggressive should treatment be? Radiology. 2006;238(3):912-919. 151. Spinelli KS, Fromwiller TE, Daniel RA, et al. Cystic pancreatic neoplasms: observe or operate. Ann Surg. 2004;239(5):651-657. 152. Maker AV, Lee LS, Raut CP, et al. Cytology from pancreatic cysts has marginal utility in surgical decision-making. Ann Surg Oncol. 2008;15(11):3187-3192. 153. Belsley NA, Pitman MB, Lauwers GY, et al. Serous cystadenoma of the pancreas: limitations and pitfalls of endoscopic ultrasound-guided fine-needle aspiration biopsy. Cancer. 2008;114(2):102-110. 154. Megibow AJ. Update in imaging of cystic pancreatic masses for gastroenterologists. Clin Gastroenterol Hepatol. 2008;6(11):1194-1197. 155. Berland LL, Silverman SG, Gore RM, et al. Managing incidental findings on abdominal CT: white paper of the ACR incidental findings committee. J Am Coll Radiol. 2010;7(10):754-773. 156. Johnson PT, Horton KM, Megibow AJ, et al. Common incidental findings on MDCT: survey of radiologist recommendations for patient management. J Am Coll Radiol. 2011;8(11):762-767. 157. Brook OR, Beddy P, Pahade J, et al. Delayed growth in incidental pancreatic cysts: are the Current American College of Radiology recommendations for follow-up appropriate? Radiology. 2015;140972. 158. Freeny PC, Saunders MD. Moving beyond morphology: new insights into the characterization and management of cystic pancreatic lesions. Radiology. 2014;272(2):345-363. 159. Chernyak V, Flusberg M, Haramati LB, et al. Incidental pancreatic cystic lesions: is there a relationship with the development of pancreatic adenocarcinoma and all-cause mortality? Radiology. 2015;274(1):161-169. 160. Ikeda M, Sato T, Morozumi A, et al. Morphologic changes in the pancreas detected by screening ultrasonography in a mass survey, with special reference to main duct dilatation, cyst formation, and calcification. Pancreas. 1994;9(4):508-512. 161. Zhang XM, Mitchell DG, Dohke M, et al. Pancreatic cysts: depiction on single-shot fast spin-echo MR images. Radiology. 2002;223(2):547-553. 162. Kimura W, Nagai H, Kuroda A, et al. Analysis of small cystic lesions of the pancreas. Int J Pancreatol. 1995;18(3):197-206. 163. Chang MY, Ong AC. Autosomal dominant polycystic kidney disease: recent advances in pathogenesis and treatment. Nephron Physiol. 2008;108(1):p1-p7. 164. Leung RS, Biswas SV, Duncan M, Rankin S. Imaging features of von HippelLindau disease. Radiographics. 2008;28(1):65-79. 165. Cahill ME, Parmentier JM, Van Ruyssevelt C, Pauls CH. Pancreatic cystosis in cystic fibrosis. Abdom Imaging. 1997;22(3):313-314. 166. Adsay NV. Cystic neoplasia of the pancreas: pathology and biology. J Gastrointest Surg. 2008;12(3):401-404. 167. Ohashi KM, Maruyama Y. Four cases of mucin-producing cancer of the pancreas: specific findings in the ampulla of Vater [Japanese]. Prog Dig Endosc. 1982;20:348-351. 168. Zamora C, Sahel J, Cantu DG, et al. Intraductal papillary or mucinous tumors (IPMT) of the pancreas: report of a case series and review of the literature. Am J Gastroenterol. 2001;96(5):1441-1447.

CHAPTER 7  The Pancreas 169. Sarr MG, Kendrick ML, Nagorney DM, et al. Cystic neoplasms of the pancreas: benign to malignant epithelial neoplasms. Surg Clin North Am. 2001;81(3):497-509. 170. Lim JH, Lee G, Oh YL. Radiologic spectrum of intraductal papillary mucinous tumor of the pancreas. Radiographics. 2001;21(2):323-337. 171. Suzuki M, Fujita N, Onodera H, et al. Mucinous cystic neoplasm in a young male patient. J Gastroenterol. 2005;40(11):1070-1074. 172. Klimstra DS, Wenig BM, Heffess CS. Solid-pseudopapillary tumor of the pancreas: a typically cystic carcinoma of low malignant potential. Semin Diagn Pathol. 2000;17(1):66-80. 173. Shuja A, Alkimawi KA. Solid pseudopapillary tumor: a rare neoplasm of the pancreas. Gastroenterol Rep (Oxf). 2014;2(2):145-149. 174. Sidden CR, Mortele KJ. Cystic tumors of the pancreas: ultrasound, computed tomography, and magnetic resonance imaging features. Semin Ultrasound CT MR. 2007;28(5):339-356. 175. Buetow PC, Buck JL, Pantongrag-Brown L, et al. Solid and papillary epithelial neoplasm of the pancreas: imaging-pathologic correlation on 56 cases. Radiology. 1996;199(3):707-711. 176. Tucci G, Muzi MG, Nigro C, et al. Dermoid cyst of the pancreas: presentation and management. World J Surg Oncol. 2007;5:85. 177. Demos TC, Posniak HV, Harmath C, et al. Cystic lesions of the pancreas. AJR Am J Roentgenol. 2002;179(6):1375-1388. 178. Koenig TR, Loyer EM, Whitman GJ, et al. Cystic lymphangioma of the pancreas. AJR Am J Roentgenol. 2001;177(5):1090. 179. Cives M, Strosberg J. An update on gastroenteropancreatic neuroendocrine tumors. Oncology (Williston Park). 2014;28(9):749-756, 758. 180. Kloppel G, Heitz PU. Pancreatic endocrine tumors. Pathol Res Pract. 1988;183(2):155-168. 181. Phan GQ, Yeo CJ, Hruban RH, et al. Surgical experience with pancreatic and peripancreatic neuroendocrine tumors: Review of 125 patients. J Gastrointest Surg. 1998;2(5):473-482. 182. Shah S, Mortele KJ. Uncommon solid pancreatic neoplasms: ultrasound, computed tomography, and magnetic resonance imaging features. Semin Ultrasound CT MR. 2007;28(5):357-370. 183. O’Grady HL, Conlon KC. Pancreatic neuroendocrine tumours. Eur J Surg Oncol. 2008;34(3):324-332. 184. Grant CS. Insulinoma. Best Pract Res Clin Gastroenterol. 2005;19(5): 783-798.

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185. Horton KM, Hruban RH, Yeo C, Fishman EK. Multi-detector row CT of pancreatic islet cell tumors. Radiographics. 2006;26(2):453-464. 186. Doppman JL, Chang R, Fraker DL, et al. Localization of insulinomas to regions of the pancreas by intra-arterial stimulation with calcium. Ann Intern Med. 1995;123(4):269-273. 187. Buetow PC, Miller DL, Parrino TV, Buck JL. Islet cell tumors of the pancreas: clinical, radiologic, and pathologic correlation in diagnosis and localization. Radiographics. 1997;17(2):453-472. 188. Kawamoto S, Shi C, Hruban RH, et al. Small serotonin-producing neuroendocrine tumor of the pancreas associated with pancreatic duct obstruction. AJR Am J Roentgenol. 2011;197(3):W482-W488. 189. Shi C, Siegelman SS, Kawamoto S, et al. Pancreatic duct stenosis secondary to small endocrine neoplasms: a manifestation of serotonin production? Radiology. 2010;257(1):107-114. 190. Degen L, Wiesner W, Beglinger C. Cystic and solid lesions of the pancreas. Best Pract Res Clin Gastroenterol. 2008;22(1):91-103. 191. Cubilla AL, Fitzgerald PJ. Cancer of the exocrine pancreas: the pathologic aspects. CA Cancer J Clin. 1985;35(1):2-18. 192. Ryan MF, Hamilton PA, Smith AJ, Khalifa M. Radiologic features of pancreatic lipoma. Can Assoc Radiol J. 2003;54(1):41-44. 193. Barutcu O, Cihangiroglu M, Yildirim T, et al. Fat containing unusual tumor of the pancreas. Eur Radiol. 2002;12(4):770-773. 194. Spencer GM, Rubens DJ, Roach DJ. Hypoechoic fat: a sonographic pitfall. AJR Am J Roentgenol. 1995;164(5):1277-1280. 195. Klein KA, Stephens DH, Welch TJ. CT characteristics of metastatic disease of the pancreas. Radiographics. 1998;18(2):369-378. 196. D’Onofrio M, Zamboni G, Faccioli N, et al. Ultrasonography of the pancreas. 4. Contrast-enhanced imaging. Abdom Imaging. 2007;32(2):171-181. 197. Ardelean M, Sirli R, Sporea I, et al. Contrast enhanced ultrasound in the pathology of the pancreas—a monocentric experience. Med Ultrason. 2014;16(4):325-331. 198. Grossjohann HS. Contrast-enhanced ultrasound for diagnosing, staging and assessment of operability of pancreatic cancer. Dan Med J. 2012;59(12):B4536. 199. D’Onofrio M, Gallotti A, Principe F, Mucelli RP. Contrast-enhanced ultrasound of the pancreas. World J Radiol. 2010;2(3):97-102. 200. Fan Z, Li Y, Yan K, et al. Application of contrast-enhanced ultrasound in the diagnosis of solid pancreatic lesions—a comparison of conventional ultrasound and contrast-enhanced CT. Eur J Radiol. 2013;82(9):1385-1390.

CHAPTER

8

 

The Gastrointestinal Tract Stephanie R. Wilson

SUMMARY OF KEY POINTS • High-resolution ultrasound allows for excellent depiction of the bowel, including the normal multilayered appearance of the bowel wall and many pathologic features. • Ultrasound is a safe, objective, and accurate method for measuring the severity of inflammatory activity in inflammatory bowel disease, an essential requirement considering the young population most often affected by this chronic and often debilitating disease. • Contrast-enhanced ultrasound is an objective biomarker that may accurately evaluate disease activity in those with bowel wall inflammation. • Elastography measures bowel wall stiffness, increasing in those with chronic disease, helping to differentiate

patients amenable to medical therapy from those requiring surgical intervention. • Transrectal ultrasound (TRUS) is an excellent noninvasive and well-tolerated procedure for staging of rectal tumors. • Transvaginal ultrasound increases accuracy of bowel ultrasound in many women as pathologic features located deep in the pelvis may only be visible with this technique. • Transperineal scan allows for accurate depiction of perianal inflammatory masses without necessity of performing often painful scans with endoanal or endorectal placement of the transducer.

CHAPTER OUTLINE ANATOMY AND SONOGRAPHIC TECHNIQUE The Gut Signature Gut Wall Pathology Imaging Technique Doppler Evaluation of Gut Wall Contrast-Enhanced Ultrasound and Elastography of the Bowel GASTROINTESTINAL TRACT NEOPLASMS Adenocarcinoma Gastrointestinal Stromal Tumors Lymphoma Metastases INFLAMMATORY BOWEL DISEASE: CROHN DISEASE Classic Features Gut Wall Thickening Inflammatory Fat Lymphadenopathy Hyperemia Mucosal Abnormalities Conglomerate Masses

G

COMPLICATIONS Strictures Incomplete Mechanical Bowel Obstruction Localized Perforation Inflammatory Masses Fistula Formation Perianal Inflammatory Disease ACUTE ABDOMEN Right Lower Quadrant Pain Acute Appendicitis Crohn Appendicitis Right-Sided Diverticulitis Acute Typhlitis Mesenteric Adenitis With Terminal Ileitis Right-Sided Segmental Omental Infarction Left Lower Quadrant Pain Acute Diverticulitis OTHER ABNORMALITIES Mechanical Bowel Obstruction Paralytic Ileus

astrointestinal (GI) tract sonography is frequently frustrating and always challenging. Gas content within the gut lumen can make visibility difficult or even impossible; intraluminal fluid may mimic cystic masses; and fecal material can create a variety of artifacts and pseudotumors. Nevertheless, normal gut

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Gut Edema Gastrointestinal Tract Infections AIDS Patients Pseudomembranous Colitis Congenital Cysts Ischemic Bowel Disease Pneumatosis Intestinalis Mucocele of Appendix Gastrointestinal Tract Hematoma Peptic Ulcer Bezoars Intraluminal Foreign Bodies Celiac Disease Cystic Fibrosis ENDOSONOGRAPHY Upper Gastrointestinal Tract Rectum: Tumor Staging of Rectal Carcinoma Anal Canal Fecal Incontinence Perianal Inflammatory Disease Acknowledgment

has a reproducible pattern, or gut signature, and a variety of gut diseases create recognizable sonographic abnormalities. Therefore ultrasound may play a valuable role in the evaluation of patients in a variety of clinical situations, including suspicion of acute conditions of the GI tract, especially appendicitis and diverticulitis.

CHAPTER 8  The Gastrointestinal Tract Recent years have shown growing interest in the use of ultrasound for surveillance of patients with inflammatory bowel disease. Further, endosonography, performed with high-frequency transducers in the gut lumen, is an increasingly popular technique for assessing the esophagus, stomach, and rectum.

ANATOMY AND SONOGRAPHIC TECHNIQUE The Gut Signature The gut is a continuous hollow tube with four concentric layers (Fig. 8.1). From the lumen outward, these layers are (1) mucosa, which consists of an epithelial lining, loose connective tissue (or lamina propria), and muscularis mucosa; (2) submucosa; (3) muscularis propria, with inner circular and outer longitudinal fibers; and (4) serosa or adventitia. These histologic layers correspond with the sonographic appearance1-3 (Table 8.1) and are referred to as the gut signature, where up to five layers may be visualized (Fig. 8.2). The sonographic layers appear alternately echogenic and hypoechoic; the first, third, and fifth layers are echogenic, and the second and fourth layers are hypoechoic. This relationship

TABLE 8.1  Gut Signature: HistologicSonographic Correlation Histology

Sonography

Superficial mucosa/interface (epithelium and lamina propria) Muscularis mucosa Submucosa Muscularis propria (inner circular and outer longitudinal fibers) Serosa/interface

Echogenic Hypoechoic Echogenic Hypoechoic Echogenic

Submucosa Mucosa Epithelium Lamina propria Muscularis mucosa

Muscularis propria FIG. 8.1  Schematic Depiction of the Histologic Layers of the Gut Wall.

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of the histologic layering with the sonographic layering is best remembered by recognition that the muscular components of the gut wall—the muscularis mucosa and the muscularis propria—constitute the hypoechoic layers on sonography. On routine sonograms, the gut signature may vary from a “bull’s-eye” in cross section, with an echogenic central area and a hypoechoic rim, to full depiction of the five sonographic layers. The quality of the scan and the resolution of the transducer determine the degree of layer differentiation. Ultrasound is superior to both computed tomography (CT) and magnetic resonance imaging (MRI) for resolution of the gut wall layers. The normal gut wall is uniform and compliant, with an average thickness of 3 mm if distended and 5 mm if not. Other morphologic features that allow recognition of specific portions of the gut include the gastric rugae (in the stomach), valvulae conniventes (plicae circulares in the small intestines), and haustra (in the colon) (Fig. 8.3). Real-time sonography allows assessment of the content and diameter of the GI lumen and the motility of the gut. Hypersecretion, mechanical obstruction, and ileus are implicated when gut fluid is excessive. Peristalsis is normally seen in the small bowel and stomach. Activity may be increased with mechanical obstruction and inflammatory enteritides. Decreased activity is seen with paralytic ileus and in the end stages of mechanical bowel obstruction.

Gut Wall Pathology Evaluation of thickened gut on sonography is far superior to the evaluation of normal gut for two important reasons. Thick gut, particularly if associated with abnormality of the perienteric soft tissues, creates a mass effect, which is easily seen on sonography. In addition, thickened gut is frequently relatively gasless, improving its sonographic evaluation. Gut wall pathology creates characteristic sonographic patterns (Fig. 8.4). The most familiar, the target pattern, was first described by Lutz and Petzoldt4 in 1976 and later by Bluth et al.,5 who referred to the pattern as a “pseudokidney,” noting that a pathologically significant lesion was found in more than 90% of patients with this pattern. In both descriptions the hypoechoic external rim corresponds to thickened gut wall, whereas the echogenic center relates to residual gut lumen or mucosal ulceration. Identification of thickened gut on sonographic examination may be related to a variety of diseases. Diagnostic possibilities are predicted by determining the (1) extent and location of disease, (2) preservation or destruction of wall layering, and (3) concentricity or eccentricity of wall involvement. Benignancy is favored by long segment involvement with concentric thickening and wall layer preservation. The classic benign pathology showing gut wall thickening is Crohn disease. Malignancy is favored by short segment involvement with eccentric disease and wall layer destruction. The classic malignant pathology showing gut wall thickening is adenocarcinoma of the stomach or colon. These are guidelines rather than rules, because chronically thickened gut in Crohn disease may show layer destruction related to fibrotic and subacute inflammatory change, and infiltrative adenocarcinoma may show some wall layer preservation. Lymphadenopathy and hyperemia of the thickened gut wall

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FIG. 8.2  Gut Signature in a Patient With Mild Gut Thickening Caused by Crohn Disease.  The muscle layers are hypoechoic. The submucosa and superficial mucosa layers are hyperechoic. There is a small amount of fluid and air in the gut lumen.

may be seen in association with both malignant and benign gut wall thickening. Gut wall masses, as distinguished from thickened gut wall, may be intraluminal, mural, or exophytic, all with or without ulceration. Intraluminal gut masses and mucosal masses have a variable appearance on sonography but are frequently hidden by gas or luminal content. In contrast, gut pathology creating an exophytic mass (without or with mucosal involvement or ulceration) may form masses that are more readily visualized. These may be difficult to assign to a GI tract origin if typical gut signatures, targets, or pseudokidneys are not seen on sonographic examination. Consequently, intraperitoneal masses of varying morphology, which do not clearly arise from the solid abdominal viscera or the lymph nodes, should be considered to have a potential gut origin.

Imaging Technique Routine sonograms are best performed when the patient has fasted. A real-time survey of the entire abdomen is performed

with a 3.5- to 5-MHz transducer, and any obvious masses or gut signatures are observed. The pelvis is scanned before and after the bladder is emptied because the full bladder facilitates visualization of pathologic conditions in some patients and displaces abdominal bowel loops in others. A routine gut evaluation should include assessment of all of the small bowel and the colon. In women, transvaginal sonography is invaluable for evaluation of the portions of the gut within the true pelvis, particularly the rectum, sigmoid colon, and, in some patients, the ileum. Further, oral fluid and a Fleet enema may improve localization and diagnosis of intraluminal or intramural gastric masses and rectal masses, respectively. Still images in long-axis and cross-sectional views as well as cine sweeps to show pathologic features allow for optimal review. Areas of interest then receive detailed analysis, including compression sonography6 (Fig. 8.5). Although this technique was initially described using high-frequency linear probes, 5- to 9-MHz convex probes and some sector probes work extremely well. The critical factor is a transducer with a short focal zone,

CHAPTER 8  The Gastrointestinal Tract

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FIG. 8.3  Gut Recognition.  (A) Sagittal and (B) cross-sectional views of the stomach show normal gastric rugae. The collapsed stomach shows variable wall thickness. (C) and (D) Valvulae conniventes (plicae circulares) of the small bowel. These are more easily seen when (C) there is fluid in the lumen of the bowel or (D) the valvulae are edematous. (E) and (F) Variations in the appearance of the colonic haustrations in two normal persons.

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FIG. 8.4  Gut Wall Pathology.  Schematic of sonographic appearances with sonographic equivalents. Top, Intraluminal mass. Inflammatory pseudopolyp on sonogram. Middle, Pseudokidney sign, with symmetrical wall thickening and wall layer destruction. Carcinoma of the colon on sonogram. Bottom, Exophytic mass. Serosal seed on visceral peritoneum of the gut on sonogram. (With permission from Wilson SR. The bowel wall looks thickened: what does that mean? In: Cooperberg PL, editor. RSNA categorical course syllabus. Chicago: RSNA; 2002. pp. 219-228.1)

allowing optimal resolution of structures close to the skin. Slow, graded pressure is applied. Normal gut will be compressed and gas pockets displaced away from the region of interest. In contrast, thickened abnormal loops of bowel and obstructed noncompressible loops will remain unchanged. Patients with peritoneal irritation or local tenderness will usually tolerate the slow, gentle increase in pressure of compression sonography, whereas they show a marked painful response if rapid, uneven scanning is performed.

Doppler Evaluation of Gut Wall Normal gut shows little signal on conventional color Doppler because interrogation is difficult in a normal and mobile bowel loop. Both neoplasia and inflammatory disease show increased vascularity compared with the normal gut wall (Fig. 8.6), whereas ischemic and edematous gut tends to be relatively hypovascular. The addition of color and spectral Doppler ultrasound evaluation to the study of the gut wall provides supportive evidence that gut wall thickening is caused by either ischemic or inflammatory

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FIG. 8.5  Schematic of Compression Sonography.  Left, Normal gut is compressed. Middle, Abnormally thickened gut, or right, an obstructed loop, such as that seen in acute appendicitis, will be noncompressible.

change in the patient with acute abdominal pain. Teefey et al.7 examined 35 patients and found absent or barely visible blood flow on color Doppler and absence of arterial signal to be suggestive of ischemia. In contrast, readily detected color Doppler flow was consistent with inflammation.

Contrast-Enhanced Ultrasound and Elastography of the Bowel Two exciting new applications of ultrasound of the bowel include contrast-enhanced ultrasound (CEUS) and elastography. The former provides objective repeatable measures of mural blood flow, which may change in response to inflammation and neoplasia, and the latter measures bowel wall stiffness.9 Although these investigations are still in their infancy, their additional benefit over routine gray-scale ultrasound with Doppler is evident. Their great contribution to the evaluation of those with inflammatory bowel disease will be discussed in that section. CEUS is also useful in the assessment of mass lesions to determine the presence of vascularity analogous to the role of contrast enhancement on CT or MRI scan.

GASTROINTESTINAL TRACT NEOPLASMS The role of sonography in the evaluation of GI tract neoplasms is similar to that of CT. Visualization is limited in cases of early mucosal lesions or with small intramural nodules, whereas tumors growing to produce an exophytic mass, a thickened segment of gut, or a sizable intraluminal mass are more easily detected (Fig. 8.7, Video 8.1). Sonograms are frequently performed early in

the diagnostic workup of patients with GI tract tumors, often before their initial identification. Vague abdominal symptomatology, abdominal pain, a palpable abdominal mass, and anemia are common indications for these scans. Appreciation of the typical morphologies associated with GI tract neoplasia may lead to accurate recognition, localization, and even staging of disease, with the opportunity for directing appropriate further investigation, including sonography-guided aspiration biopsy.

Adenocarcinoma Adenocarcinoma is the most common malignant tumor of the GI tract. Grossly, it has variable growth patterns (see Fig. 8.7), including infiltrative, polypoid, fungating, and ulcerated tumors. Most GI tract mucosal cancers are not visualized on sonography. However, large masses, either intraluminal or exophytic, and annular tumors create sonographic abnormalities.10,11 Tumors of variable length may thicken the gut wall in either a concentric symmetrical or an asymmetrical pattern. A target or pseudokidney morphology may be created (see Fig. 8.4). Air in mucosal ulcerations typically produces linear echogenic foci, often with ring-down artifact, within the bulk of the mass. Tumors are usually, but not invariably, hypoechoic. Annular lesions may produce gut obstruction with dilation, hyperperistalsis, and increased luminal fluid of the gut proximal to the tumor site.11 Evidence of direct invasion, regional lymph node enlargement, and liver metastases should be sought. Adenocarcinoma accounts for 80% of all malignant gastric neoplasms, where infiltration may be superficial or transmural, the latter creating a linitis plastica, or “leather bottle,” stomach. Adenocarcinoma occurs much less frequently in the small bowel than in the stomach or large bowel. It accounts for approximately

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FIG. 8.6  Contribution of Doppler to Gut Assessment in Three Patients.  (A) and (B) Cross-sectional images of the ileum proximal to an inflammatory stricture in Crohn disease. The lumen is distended with fluid. The wall is slightly thick. (B) Color Doppler image shows marked hyperemia of the gut wall as a reflection of its inflammation. (C) and (D) Transvaginal views in a young woman with right lower quadrant pain show the appendix as a round, tubular structure adjacent to the ovary. (D) Color Doppler image shows that appendix is hyperemic, consistent with inflammation. (E) and (F) Transverse images of the ascending colon show wall thickening with total layer destruction related to invasive colon carcinoma. Neoplastic tumors of the gut invariably show vascularity as here.

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FIG. 8.7  Adenocarcinoma of the Gut in Three Patients.  (A) and (B) Cancer at gastroesophageal junction. (A) Sagittal and (B) transverse sonograms of the upper abdomen show a pseudokidney (arrowheads) adjacent to the left lobe of the liver. (C) and (D) Carcinoma of descending colon. (C) Long-axis image of the colon shows an abrupt transition from normal to thickened bowel. (D) An axial image shows a hypoechoic, circumferential mass with an “apple core” appearance. There is echogenic infiltrated fat and an enlarged hypoechoic lymph node adjacent to the tumor. (E) and (F) Intraluminal villous adenocarcinoma of stomach. (E) Transverse sonogram after fluid ingestion shows a relatively well-defined, inhomogeneous, echogenic mass (arrows) within body of stomach. Fluid is in the stomach lumen (S). (F) Confirmatory barium swallow shows the villous tumor (arrows). See also Video 8.1.

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50% of the small bowel tumors found, 90% of them arising in either the proximal jejunum (Fig. 8.8A and B) or the duodenum. Crohn disease is associated with a significantly increased incidence of adenocarcinoma that usually develops in the ileum. Small bowel adenocarcinomas are generally annular in gross morphology, frequently with ulceration. Colon carcinoma is very common and accounts for virtually all malignant colorectal neoplasms. Colorectal adenocarcinoma grows with two major gross morphologic patterns: polypoid intraluminal tumors, which are most prevalent in the cecum and ascending colon, and annular constricting lesions (see Fig. 8.7C and D), which are most common in the descending and sigmoid colon. In rare cases, infiltrative tumors similar to those seen in the stomach may occur in the colon (Fig. 8.8C and D).

Gastrointestinal Stromal Tumors Of the mesenchymal tumors affecting the gut, those of smooth muscle origin are the most common and account for about 1% of all GI tract neoplasms. These gastrointestinal stromal tumors (GISTs) are found most often in the stomach and the small bowel.

Colonic tumors are the least common and occur most often in the rectum. Although GISTs may be found as an incidental observation at surgery, sonography, or autopsy, these vascular tumors frequently become very large and may undergo ulceration, degeneration, necrosis, and hemorrhage.12 On sonography, smooth muscle (stromal) tumors typically produce round mass lesions of varying size and echogenicity, often with central cystic areas13 related to hemorrhage or necrosis (Fig. 8.9). Their gut origin is not always easily determined, but if ulceration is present, pockets of gas in an ulcer crater may suggest their origin. Smooth muscle tumors of gut origin should be considered in the differential diagnosis of incidentally noted, indeterminate abdominal masses in asymptomatic patients, particularly if they show central cystic or necrotic change (Fig. 8.9E and F). These tumors are very amenable to sonographicguided aspiration biopsy.

Lymphoma The gut may be involved with lymphoma in two basic forms: as widespread dissemination in stage III or IV lymphoma of any

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FIG. 8.8  Adenocarcinoma of Bowel: Sonographic-CT Correlation.  (A) Sonogram and (B) CT scan show large, necrotic, left upper quadrant mass at the ligament of Treitz with enlargement of the perienteric lymph nodes (arrow) in a 60-year-old man who presented with abdominal discomfort and blood loss. (C) and (D) Infiltrative carcinoma of transverse colon in a 42-year-old man who presented to the emergency department with acute abdominal pain. (C) Transverse sonogram of the epigastrium shows a featureless segment of thick gut with total loss of wall layering in the location of the transverse colon. Deep to the gut is a diffuse echogenic mass effect (arrow) suggesting infiltrated or inflamed fat. (D) Confirmatory CT scan. The infiltrated fat is black and streaky on the CT image. Neoplasia was not suspected on the basis of either imaging test or at surgery.

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FIG. 8.9  Gastrointestinal Stromal Tumors (GISTs) in Four Patients.  (A) and (B) Exophytic gut mass, a gastric leiomyoma. (A) Transverse sonogram of epigastrium shows the normal gastric gut signature and the focal exophytic mass. (B) After water ingestion, the lumen contains fluid that appears hypoechoic. The solid mass is clearly seen. (C) and (D) Gastric leiomyosarcoma. (C) Transverse sonogram after fluid ingestion shows a complex, smooth intramural mass (arrows) projecting into the fluid-filled stomach lumen (S). (D) Confirmatory barium swallow shows the intramural tumor (arrows). (E) and (F) Two patients with a large, upper abdominal, complex, and necrotic-appearing mass on sonography. Although the gut origin of the masses is not evident on the images, the correct diagnosis of GIST was suggested based on the appearance. The jejunum is the origin of the tumor in (E) and the stomach in (F).

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cell type or, more often, as primary lymphoma of the GI tract, which is virtually always a non-Hodgkin lymphoma. Primary tumors constitute only 2% to 4% of all GI tract malignant tumors12 but account for 20% of those found in the small bowel. Three predominant growth patterns are observed: nodular or polypoid, carcinoma-like ulcerations, and infiltrating tumor masses that frequently invade the adjacent mesentery and lymph nodes. Small, submucosal nodules may be easily overlooked on sonography. However, many patients have large, easily visible, very hypoechoic, ulcerated masses in the stomach or small bowel14,15 (Fig. 8.10). Long, linear, high-amplitude echoes with ring-down artifacts, indicating gas in the residual lumen or ulcerations, and aneurysmal dilation of the bowel lumen are common observations. This particular pathologic state has been recognized as one of the more frequent presentations of patients with acquired immunodeficiency syndrome (AIDS)–related lymphoma. Regional lymph node enlargement may be visualized, although generalized lymph node abnormality is uncommon.

bowel, and colon are involved. On sonography, small submucosal nodules that tend to ulcerate are rarely seen, whereas large, diffusely infiltrative tumors with large ulcerations are common, particularly in the small bowel where they create hypoechoic, well-defined masses that often have bright, specular echoes with ring-down artifacts in areas of ulceration. Secondary neoplasm affecting the omentum and peritoneum may cause ascites (which may be particulate ascites), tiny or confluent superficial secondary nodules on the gut surface, or extensive omental cakes that virtually engulf the involved gut loops17 (Fig. 8.12). Metastases to the peritoneum most often arise from primary tumors in the ovary or the gut. A drop metastasis in the pelvic pouch of Douglas shows as a small, solid, peritoneal nodule without obvious origin from the pelvic viscera.

INFLAMMATORY BOWEL DISEASE: CROHN DISEASE

Metastases Malignant melanoma and primary tumors of the lung and breast are the tumors most likely to have secondary involvement of the GI tract16 (Fig. 8.11). In order of frequency, the stomach, small

Inflammatory bowel disease (IBD) comprises Crohn disease and ulcerative colitis. Ulcerative colitis is a mucosal inflammation of the colon and often shows little in the way of gross morphologic

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FIG. 8.10  Small Bowel Lymphoma in Two Patients.  (A) Transverse left sonogram shows a hypoechoic round mass lesion. Central echogenicity with ring-down gas artifact suggests its gut origin. (B) Correlative CT scan shows large, soft tissue mass with corresponding residual gut lumen. (C) Sonogram in AIDs patient shows a focal midabdominal, hypoechoic mass with no wall layer definition, which is classic for gut lymphoma. The luminal gas appears as central bright echogenicity with dirty shadowing. (D) Correlative CT scan.

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FIG. 8.11  Metastatic Malignant Melanoma to Small Bowel.  (A) Transverse paraumbilical sonogram shows well-defined, hypoechoic mass with central irregular echogenicity with gas artifact suggesting gut origin. (B) Confirmatory CT scan.

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FIG. 8.12  Peritoneal Metastases in Two Patients.  (A) Transvaginal image shows ascites and visceral peritoneal plaque on the surface of the small bowel loop (arrows) from metastatic ovarian cancer. (B) Transvaginal scan of peritoneal drop metastasis from stomach primary shows grossly particulate ascites. There is a small peritoneal implant in the vesicouterine angle.

change except with acute disease. Further, the involved colon is readily evaluated with colonoscopy and also with all crosssectional imaging, making its assessment relatively straightforward. Crohn disease, by comparison, is a chronic transmural. The peak age of onset is early in life, between the ages of 15 and 40 years, thus affecting patients during their most productive years. The natural course of the disease includes alternating periods of active inflammation and remission with a strong tendency to complicate over time, with the development of penetrating and/ or fibrostenotic lesions. As a result, surgical intervention rates have been high. Historically, Crohn disease was managed according to patient symptomatology. It is recognized, however, that neither inflammatory markers nor symptoms are an accurate reflection of the state of the disease. Today, therefore, there is a dramatic shift in approach with an effort to treat to the target

of mucosal healing on endoscopy, including the use of aggressive biologic therapy and the increasing popularity of early introduction of anti–tumor necrosis factor-α (anti-TNFα). These management changes necessitate frequent monitoring of all patients because repeated endoscopic performance is poorly tolerated, expensive, and not without risk. Therefore safe, objective, noninvasive, and accurate methods for measuring the severity of inflammatory activity are vital. Imaging plays a major role in the diagnosis of disease,18 in the detection of recurrence, and in the recognition of complications, which may be associated with a silent clinical course. Surveillance imaging and monitoring response to therapy (which may be both expensive and toxic) is of prime importance. In a meta-analysis comparing different modalities for diagnosis of IBD, mean sensitivity estimates for the diagnosis on a per-patient

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basis were high and not significantly different for ultrasound (89.7%), MRI (93.0%), and CT (84.3%).19 Therefore in this era of cost and radiation awareness, ultrasound is rising in importance for imaging of IBD.20 Sonography is our routine evaluation technique for initial disease diagnosis, the detection of recurrence,21 the determination of the extent, complications22 and activity of disease, and in the assessment of response to treatment. Although any portion of the gut may be involved, Crohn disease most commonly affects the terminal ileum and the colon. This transmural, granulomatous inflammatory process affects all layers of the gut wall and also the perienteric soft tissues. Grossly, the gut wall may become very thick and rigid with secondary luminal narrowing. Discrete or continuous ulcers and deep fissures are characteristic, frequently leading to fistula formation. Mesenteric lymph node enlargement and matting of involved loops are common. The mesentery may be markedly thickened and fatty, creeping over the edges of the gut to the antimesenteric border. The classic features of Crohn disease—wall thickening, inflammatory fat, lymphadenopathy, and hyperemia—reflect these gross morphologic changes. Complications of Crohn disease include stricture, incomplete bowel obstruction, perforation, fistulas, and inflammatory masses.21

The immediate objectives of a sonogram on a patient with known or suspected IBD, therefore, include documentation of the distribution and the extent of the disease, as well as the disease activity. A global assessment is made on ultrasound grading all of the classic features from 0, not present; through 1, mild; 2, moderate; and 3, showing severe change23 (Table 8.2). Utilization of such a scoring system allows for consistency of performance and reproducibility of results. It also facilitates comparisons for monitoring response to therapy.

Crohn Disease on Sonography CLASSIC FEATURES Gut wall thickening Inflammatory fat Mesenteric lymphadenopathy Hyperemia COMPLICATIONS Strictures Mechanical bowel obstruction Perforation Inflammatory masses Fistulas Appendicitis

TABLE 8.2  Ultrasound Global Assessment Showing Crohn Disease Activity Scores on GrayScale Ultrasound and Color Doppler Imaging Classification

Gray-Scale Ultrasound Features of Activity Wall thickness (mm) Inflammatory fat

INACTIVE 8.1

• Absent • Perienteric region resembles normal mesenteric fat

• Masslike • Slightly echogenic • Of less area than the bowel on axial view • Small regions of color without the vessel

• Masslike • More echogenic • Equal area to the bowel on axial view • Medium-length segments of color vessels in the bowel wall

• Masslike • Significantly echogenic • Of greater area than the bowel on axial view

• Mild wall thickness • Minimal inflammatory fat • Present but not minimal signal on CDI • Wall layer preservation

• Moderate wall thickness • Moderate inflammatory fat • Moderate signal on CDI • ± Wall layer preservationa

• Moderate to severely thickened bowel wall • Abundant inflammatory fat • Long continuous mural blood vessels on CDI • ± Wall layer preservationa • Spiculation of serosal bordera

Color Doppler imaging (CDI) Mural blood flow

• Absent

Ultrasound global assessment

• No signs of active disease

• Circumferential or continuous depiction of vessels in the bowel wall with or without mesenteric vessels

a Loss of wall layering and serosal spiculation both suggest increasing disease severity. Reproduced with permission from Medellin-Kowalewski A, Wilkens R, Wilson A, et al. Quantitative contrast-enhanced ultrasound parameters in Crohn disease: their role in disease activity determination with ultrasound. AJR Am J Roentgenol. 2016;206(1):64-73.23

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Classic Features Gut Wall Thickening Gut wall thickening is the most frequently observed abnormality in patients with Crohn disease and varies in proportion to disease severity. Its identification comprises the basis for initial disease detection, for detection of recurrence,24 and for determining the extent of disease. In a meta-analysis on the accuracy of sonography in detecting Crohn disease, Fraquelli et al.25 showed sensitivity and specificity of 88% and 93%, respectively, when a bowel wall thickness threshold greater than 3 mm was used, and 75% and 97% with a threshold greater than 4 mm. Gut wall thickening in Crohn disease is most frequently concentric and may be marked.26,27 Wall echogenicity varies depending on the degree of inflammatory infiltration and fibrosis. Stratification with retention of the gut layers is typical (Fig. 8.13A and B; also see Fig. 8.2, Videos 8.2 and 8.3). A target or pseudokidney appearance is possible in acute disease or long-standing fibrotic or subacute inflammatory disease as the gut wall layering is progressively lost (Fig. 8.13C and D). Long-standing and often burnt-out disease may also show wall thickening with fat deposition in the submucosa, which appears as increased echogenicity of this layer (Fig. 8.13E and F). Actively involved gut typically appears rigid and fixed, with decreased or absent peristalsis (Video 8.4). Involvement of the serosal border of the bowel may result in spiculation of the border of the bowel (Fig. 8.14). Skip areas are frequent. Involved segments vary in length from a few millimeters to many centimeters. Bowel wall thickening may be caused by acute inflammatory change or related to chronic fibrosis and smooth muscle hypertrophy. Inflammatory Fat Mesenteric edema and inflammation of the mesenteric fat are also characteristic of Crohn disease, producing a mass in the mesentery adjacent to the diseased gut that may creep over the border of the abnormal gut or completely engulf it, the so-called creeping fat. Fat creeping onto the margins of the involved gut creates a uniform echogenic halo around the mesenteric border of the gut, with a thyroidlike appearance in cross section (Fig. 8.15). It may become more heterogeneous and even hypoechoic in long-standing disease. Creeping fat is the most common cause of gut loop separation seen on GI contrast studies.21 It is also the most striking and detectable abnormality on sonography of patients with perienteric inflammatory processes. Therefore detection of creeping fat should lead to a detailed evaluation of the regional gut. Lymphadenopathy Tender and enlarged mesenteric and perienteric nodes are common features of the active phase of inflammation with Crohn disease (Fig. 8.16). Lymphadenopathy may persist in the inactive phase. The nodes appear as focal hypoechoic masses circumferentially surrounding the gut and in the expected location of the mesenteric attachment. Nodes are frequently quite round, are of moderate size, and typically lose the normal linear echogenic streak from the nodal hilum. Similar to the gut, the lymph nodes show hyperemia as a reflection of their inflammation.

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Hyperemia Mesenteric vascularization and neoangiogenesis are recognized components of the inflammatory process, and evaluation of blood flow is a useful tool for monitoring inflammatory activity and response to therapy. Disease activity correlates with hyperemia, as seen on color Doppler evaluation28 (Fig. 8.17, Video 8.5). Although subjective, this addition of color Doppler to gray-scale sonography can provide valuable supportive evidence of inflammatory change in the gut and adjacent inflamed fat21 (see Fig. 8.6B, D, and F). However, color Doppler shows blood flow in major blood vessels with relatively fast-moving blood and does not show blood flow at the perfusion level. To overcome this limitation of activity assessment, there has been increasing interest over recent years in the use of CEUS of the bowel, performed with the injection of microbubble contrast agents. Using ultrasound quantitative techniques, CEUS allows for objective measurement of blood flow at the perfusion level as a reflection of activity. On observation, we look for transmural enhancement of the bowel wall and also a “comb sign,” reflective of blood flow within the mesenteric vasculature (Fig. 8.18, Videos 8.6 and 8.7). Generation of time intensity curves allows for measurement of the peak enhancement and the area under the curve. Studies have shown a direct correlation between the level of bowel wall enhancement and active inflammatory disease, as assessed on colonoscopy.29,30 Further, Ripollés et al.29 show that CEUS measurements perform better than wall thickness in prediction of disease severity at colonoscopy. In our own laboratory, we have integrated the objective measurements of blood flow on CEUS with the baseline gray-scale assessments of wall thickness and inflammatory fat to improve the objectivity of activity assessments on ultrasound.23 Mucosal Abnormalities Although endoscopy remains the major tool for evaluating mucosal and luminal abnormality, ultrasound may on occasion show luminal polypoid masses, such as inflammatory polyps, and deep ulcerations with pockets of echogenic air projecting within the gut wall. Ultrasound may also show intramural sinus tracts with air dissecting within the layers of the bowel wall (Fig. 8.19), as a complication of both Crohn disease and diverticulitis. Conglomerate Masses Conglomerate masses may be related to clumps of matted bowel, inflamed edematous mesentery, increased fat deposition in the mesentery, or, infrequently, mesenteric lymphadenopathy. Involved loops may demonstrate angulation and fixation resulting from retraction of the thickened fibrotic mesentery.

COMPLICATIONS Strictures Strictures are the most common complication of Crohn disease requiring surgical intervention. These are due to rigid narrowing of the gut lumen, contributed to by mural inflammation, fibrosis, and smooth muscle hypertrophy. The luminal surfaces of involved

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FIG. 8.13  Gut Wall Thickening in Three Patients With Crohn Disease.  (A) Cross-sectional and (B) sagittal views showing the typical thickening in active disease with wall layer retention; arrow, lymph node. (C) Cross-sectional and (D) sagittal views show complete loss of wall layering, as seen with active disease. (E) Sonogram and (F) corresponding CT image of the terminal ileum in a patient with burnt-out disease and fatty deposition in the submucosa, which appears echogenic on the sonogram. See also Videos 8.2 and 8.3. (C and D with permission from Wilson SR. The bowel wall looks thickened: what does that mean? In: Cooperberg PL, editor. RSNA categorical course syllabus. Chicago: RSNA; 2002. pp. 219-228.1)

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FIG. 8.14  Concerning Features for Severe Disease and Complication on Bowel Ultrasound in Two Patients.  (A) A long-axis view of the terminal ileum shows bowel wall thickening and abundant surrounding echogenic inflammatory fat. The serosal margin of the bowel shows spiculation. (B) A long-axis view of the terminal ileum shows a hypoechoic bowel with loss of wall layering. There is a fixed acute angulation as well as spiculation of the serosal margin. Both the spiculation and fixed angulation have an association with stricture and perforation.

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FIG. 8.15  Creeping Fat in Two Patients With Crohn Disease.  (A) Cross-sectional view of terminal ileum shows a hyperechoic mass effect (arrows) along the medial border of the gut representing creeping fat. (B) Confirmatory CT scan shows both the thick wall of the terminal ileum and the streaky fat (arrows). In another patient, (C) long-axis and (D) cross-sectional images of the sigmoid colon show gut wall thickening and surrounding echogenic inflammatory fat (arrows).

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FIG. 8.16  Lymphadenopathy in Two Patients With Crohn Disease.  (A) Transverse image in the right lower quadrant shows a thick terminal ileum in cross section. There is inflamed fat in the location of the mesentery. A mesenteric node (arrow) shows as a small, solid, hypoechoic mass within the fat. (B) Multiple mesenteric nodes of varying size show as hypoechoic soft tissue masses within the mesentery, optimally shown in an oblique plane between the region of the ileocecal valve and the aortic bifurcation.

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FIG. 8.17  Classic Features of Active Crohn Disease.  Gray-scale (A, C) and color Doppler (B, D) images of the terminal ileum show moderate wall thickening (7 mm), moderate inflammatory fat, and moderate hyperemia on color Doppler imaging. See also Videos 8.4 and 8.5.

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B FIG. 8.18  Contrast-Enhanced Ultrasound of the Bowel in Crohn Disease, Subjective and Objective.  (A) Two images of contrast-enhanced bowel, axial view, show the comblike vessels from vascularization of the mesentery and the transmural enhancement of the bowel wall. The adjacent images on the right are low mean intensity poor detail gray-scale, used for reference. (B) Images are in long axis. A region of interest in the bowel wall and a subsequent objective time intensity curve allow measurement of the peak enhancement and area under the curve. At the bottom is the time intensity curve that allows for quantification of the enhancement parameters. See also Videos 8.6 and 8.7. (A with permission from Wilson S. Evaluation of the small intestine by ultrasonography. In: Gourtsoyiannis N, editor. Radiologic imaging of the small intestine. Heidelberg: Springer-Verlag; 2002. pp. 73-86.18)

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FIG. 8.19  Intramural Sinus Tract in Active Crohn Disease of the Neoterminal Ileum.  (A) and (B) Long-axis views of the terminal ileum show wall thickening and surrounding abundant inflammatory fat. The luminal surfaces are in apposition and are central within the thickened loop. (B) Bright echogenic line running parallel to the serosa, an intramural sinus tract filled with air. (C) and (D) Axial images show two bright echogenic linear streaks suggesting air dissected within the layers of the bowel, deep to the echogenic submucosal layer.

segments of gut most often appear to be in fixed constant apposition, with the lumen appearing as a linear echogenic central area within a thickened gut loop (Fig. 8.20). This is in contrast to thickened sections, where the luminal diameter may be maintained (Fig. 8.21). Fixed acute angulations are frequent associations with advanced strictures (Video 8.8). Incomplete mechanical obstruction may be inferred if dilated, hyperperistaltic segments are seen proximal to a stricture (Fig. 8.21C and D, Videos 8.9 and 8.10). Peristaltic waves from the obstructed gut, proximal to a narrowed segment, may produce visible movement through the strictured segment. Less often, involved segments of gut show luminal dilation with sacculation, as well as narrowing, and the retained lumen is of variable caliber. Concretions and bezoars may develop in gut between strictured segments. Parente et al.31 showed that bowel ultrasound is an accurate technique for detecting small bowel strictures, especially in patients with severe disease who are candidates for surgery. Management of strictures in Crohn disease is challenging. Differentiating between patients who have a predominantly inflammatory versus a mainly fibrotic component of their stricture is imperative to improve selection between medical therapy and surgery. Investigations using only gray-scale ultrasound features are frequently inconclusive. However, bowel ultrasound has been shown to detect fibrosis using a variety of elastographic techniques. Shear wave

elastography uses acoustic radiation force impulse technology to assess elastic properties of tissue through an acoustic ultrasound force that propagates a shear wave through tissue. Measurements of the velocity in meters per second (m/sec) of this shear wave traversing through the tissue are made. Shear wave elastography provides an objective and reproducible quantitative measurement of tissue stiffness.32 Early investigations assessing fibrosis in animal models with elastography show some promising results.33 Our recent experience combines both CEUS and point shear wave elastography. Our results suggest CEUS parameters reflect inflammation and elastography values reflect the chronic features of fibrosis and smooth muscle hypertrophy, improving greatly our contributions to patient management.34

Incomplete Mechanical Bowel Obstruction Obstructive symptoms of bloating abdominal pain and abdominal distention are frequently associated with stricture in IBD. On sonography, distended prestenotic loops of bowel are fluid distended and show dysfunctional and excess peristalsis (see Fig. 8.21C and D, Videos 8.9 and 8.10).

Localized Perforation Although free perforation of the bowel is rare in Crohn disease, localized perforation with phlegmonous masses contained within the surrounding perienteric inflammatory fat is common

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FIG. 8.20  Strictures in Three Patients With Crohn Disease.  (A) An axial view of the terminal ileum shows wall thickening and surrounding inflammatory fat. (B) The long-axis image shows long segment thickening with luminal apposition. (C) Confirmatory fluoroscopic image from a small bowel enema shows the long, tight stricture in the ileum. (D) and (E) Sonograms of the terminal ileum show an abrupt transition in the caliber of the gut (arrow). The gut proximal to the arrow is dilated and fluid filled. The distal gut has a stricture, confirmed on (F), the small bowel enema. (G) Short-axis image through the stricture shows the thickened wall and surrounding inflamed fat. (H) Long-axis image of the neoterminal ileum shows a thickened, featureless wall with a caliber alteration (arrows). (I) Confirmatory CT scan.

(Fig. 8.22, Video 8.11). Spiking of the border of acutely inflamed gut is characteristic (see Fig. 8.14). On occasion, an air-containing tract may be identified, traversing the bowel wall into the perienteric fat. Phlegmonous masses should alert the sonographer to possible underlying localized perforation.

Inflammatory Masses Inflammatory masses involving the fibrofatty mesentery are the most common complication of Crohn disease, although the development of abscesses with drainable pus occurs infrequently. Before the stage of liquefaction, phlegmonous change may be noted as poorly defined, hypoechoic areas without fluid content

interdigitating into the surrounding inflamed fat (Figs. 8.23A and B and 8.24A). Abscess formation results in a complex or fluid-filled mass (Figs. 8.23G-I and 8.24B). Gas content within an abscess is helpful in suggesting an abscess, but this gas content is also a potential source of sonographic error, particularly if large quantities are present. Abscesses may be intraperitoneal or extraperitoneal or may be in remote locations such as the liver, abdominal wall (Fig. 8.23H and I), and psoas muscles. An excellent application of CEUS is in the characterization of inflammatory masses related to the bowel in a variety of clinical situations. The differentiation of phlegmonous inflammatory masses, without drainable pus, from those with liquid content

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FIG. 8.21  Bowel Proximal to a Stricture in Three Patients.  (A) and (B) Images of the small bowel slightly proximal to a stricture show a fluid-distended lumen and moderate mural wall thickening. (C) and (D) Two patients with prestenotic fluid-distended bowel and a stricture distal with an obvious transition point. See also Videos 4.9 and and 4.10.

is frequently a challenge.35 The addition of CEUS will quickly and effectively differentiate these masses as phlegmons are invariably hypervascular, whereas all fluid-containing abscesses are completely avascular on CEUS (Fig. 8.25)

Fistula Formation This characteristic penetrating complication of Crohn disease occurs most often at the proximal end of a thickened, strictured segment of bowel. Although mucosal ulcerations are not well assessed on sonography, deep fissures in the gut wall or intramural sinus tracts appear as echogenic linear areas penetrating deeply into the wall beyond the margin of the gut lumen (see Fig. 8.22, Video 8.11). With fistula formation, linear bands of varying echogenicity can be seen extending from segments of abnormal gut to the skin (Fig. 8.26C), bladder (Figs. 8.26B and 8.27D), vagina, or other abnormal loops (Video 8.12). If there is gas or movement in the fistula during the sonographic study, the fistula will usually appear bright or echogenic, with or without ring-down artifact related to air in the tract. Conversely, if the tract is empty or partially closed, the fistula may appear as a hypoechoic or hypoechoic tract. Palpation of the abdomen during the examination may produce

movement of fluid or air through the fistula, assisting in its identification.

Perianal Inflammatory Disease Perianal inflammation is a frequent and debilitating complication of Crohn disease and its presence at initial diagnosis is a poor prognostic indicator. Highly complex, transsphincteric tracts may extend to involve the deep tissues of the buttocks (Fig. 8.28), perineum, scrotum (men), and labia and vagina (women). Unlike commonly encountered perianal fistulas based on the cryptoglandular theory, fistulas in Crohn disease have no predilection for the location of the internal openings and are highly complex. In patients of either gender, we have found transperineal scanning to be the most comfortable and often most informative technique, performed alone or in combination with transrectal ultrasound.36 Further, in women, transvaginal scan contributes greatly to our assessment of rectal and perirectal disease. It is also ideal for showing enterovesical, enterovaginal, and rectovaginal fistulas.37 Rectal involvement in Crohn disease is characterized by (1) thickening of the rectal wall with wall layer preservation, (2) inflammation of the perirectal fat, and (3) enlargement of the perirectal lymph nodes.

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FIG. 8.22  Localized Perforation With Phlegmon.  Two young women with acute flare of Crohn disease symptoms. (A) and (B) First patient. (A) Cross-sectional and (B) long-axis images of the bowel show wall thickening and a deep hypoechoic mass with fingerlike projections into the surrounding perienteric fat, suggesting phlegmon. Also, on (A), air appears as a bright focus extending beyond the lumen of the bowel into the bowel wall, suggesting localized perforation. (C) and (D) Second patient. (C) Cross-sectional image of the ileum shows a large area of disruption of the bowel wall, an adjacent hypoechoic phlegmon, and an air tract from localized perforation. (D) Long-axis image of loop of ileum shows that the wall is uniformly thickened with layer preservation. The phlegmon is on the margin of the bowel and not shown in the longitudinal view. See also Video 8.11.

ACUTE ABDOMEN Sonography is a valuable imaging tool in patients with specific suspected acute GI abnormalities such as acute appendicitis or acute diverticulitis.38 However, its contribution to the assessment of patients with possible GI tract disease is less certain. Seibert et al.39 emphasized the value of ultrasound in assessing the patient with a distended and gasless abdomen and detecting ascites, unsuspected masses, and abnormally dilated, fluid-filled loops of small bowel. In my experience, sonography has been helpful not only in the gasless abdomen but also in a variety of other situations. The real-time aspect of sonographic study allows for direct patient–sonographer/physician interaction, with confirmation of palpable masses and focal points of tenderness. The doctrine “scan where it hurts” is invaluable and has led sonographers to describe the value of the sonographic equivalent

to clinical examination with such descriptors as a sonographic Murphy sign or sonographic McBurney sign. Similar to the radiographic approach to plain film interpretation, a systematic approach is essential in the sonographic assessment of the abdomen in a patient with an acute abdomen of uncertain origin. The abdominal ultrasound evaluation should include visible gas and fluid (to determine their luminal or extraluminal location), the perienteric soft tissues, and the GI tract itself. Identification of gas in a location where it is not usually found is a clue to many important diagnoses. The gas itself may appear as a bright, echogenic focus, but the identification of the artifacts associated with the gas pockets usually leads to their detection. These include both ring-down artifact and “dirty” shadowing. Extraluminal gas may be intraperitoneal (Free intraperitoneal

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FIG. 8.23  Inflammatory Masses in Crohn Disease.  Top row, Phlegmons (P). (A) Loop of thick sigmoid colon is seen in cross section. Adjacent to the margin is a poorly defined, hypoechoic zone within extensive inflamed fat. (B) Transverse sonogram in the right lower quadrant shows a thick terminal ileum superficially. Within the extensive inflamed fat is a poorly defined, hypoechoic zone representing the phlegmon. (C) Confirmatory CT scan. Middle row, Inflammatory masses, with air but no drainable pus. (D) Transverse image of the right lower quadrant shows abundant inflamed fat. Centrally, there is a small fluid collection or abscess (A) with small, echogenic shadowing foci (arrows) caused by air bubbles. (E) Cross-sectional sonogram through the terminal ileum shows gut thickening, echogenic inflamed fat, and a poorly defined, focal hypoechoic area deep to the gut. Bubbles of gas outside the gut are seen as bright, echogenic foci (arrow) on sonography. (F) Confirmatory CT scan. Bottom row, Drainable abscesses. (G) Large, interloop fluid collection. (H) Sonogram and (I) confirmatory CT scan show a superficial fluid collection with small gas bubbles in the anterior abdominal wall. (B, E, F, H, and I with permission from Sarrazin J, Wilson SR. Manifestations of Crohn disease at US. Radiographics. 1996;16[3]:499-520.21)

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FIG. 8.24  Inflammatory Masses on Sonography.  (A) Classic phlegmon with no drainable pus. The mass is hypoechoic and interdigtitates with the surrounding inflammatory fat. There are bright foci of extraluminal air within. (B) Classic abscess—a well-defined mass with uniform low-level echoes within related to the presence of pus.

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FIG. 8.25  Use of Contrast-Enhanced Ultrasound (CEUS) to Distinguish Between Abscess and Phlegmon; Exams in Two Patients.  Both examinations include a contrast-enhanced image (left) and low-resolution gray-scale image (right). (A) Hypoechoic mass on baseline is completely avascular on CEUS diagnostic for a fluid-containing abscess (A). (B) Hypoechoic mass is uniformly vascular on CEUS, diagnostic for a hypervascular inflammatory mass, a phlegmon. (With permission from Wilson S. Evaluation of the small intestine by ultrasonography. In: Gourtsoyiannis N, editor. Radiologic imaging of the small intestine. Heidelberg: Springer-Verlag; 2002. pp. 73-86.18)

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FIG. 8.26  Fistulas in Patients With Crohn Disease.  (A) and (B) Enterovesical fistulas. (A) Tract between the abnormal gut (G) and the bladder (B). An air bubble within shows as a bright, echogenic focus (arrow). (B) Hypoechoic tract connects an inflammatory mass (M) to the bladder (B). (C) Enterocutaneous fistula. Hypoechoic tract runs from a loop of abnormal gut (G) to the skin surface (arrow). (D) Rectovaginal fistula on transvaginal sonogram appears as a bright, air-containing tract (arrow) coursing from the rectum (R) to the vagina (V). See also Video 8.12 for enteroenteric fistula.

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FIG. 8.27  Enterovesical Fistula in Crohn Disease.  (A) and (B) Cross-sectional images of the terminal ileum show wall thickening and hyperemia. (C) Air in the bladder appears as nondependent bright echoes with dirty shadowing. (D) and (E) Long-axis views of the ileum show the hyperemia and the constant luminal apposition, consistent with stricture. (F) Bladder with the luminal air and an air-containing tract from the bladder to the adjacent bowel. (G) Dilated, fluid-filled bowel proximal to the thickening, suggesting incomplete mechanical bowel obstruction. (H) and (I) Coronal CT images confirm the bladder air and an inflammatory mass related to the bladder dome.

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FIG. 8.28  Perianal Inflammatory Crohn Disease.  (A) Axial image of the anal canal shows an internal opening (arrow) posteriorly at 6 o’clock. A transsphincteric fistula runs to a large, horseshoe-shaped posterior abscess more optimally shown in (B), which also shows deeper collections in the left buttock.

air) or retroperitoneal, and its presence should suggest either hollow viscus perforation or infection with gas-forming organisms40 (Fig. 8.29). Nonluminal gas may be easily overlooked, particularly if the collection is large. Gas in the wall of the GI tract, pneumatosis intestinalis, with or without gas in the portal veins, raises the possibility of ischemic gut. The likelihood of gas artifacts between the abdominal wall and the underlying liver to be related to free intraperitoneal gas was well described by Lee et al.40 In my group’s work, we have found that the peritoneal stripe appears as a bright, continuous, echogenic line, and that air adjacent to the peritoneal stripe produces enhancement of this layer, because the gas has a higher acoustic impedance to sound waves than does the peritoneum itself. Careful peritoneal assessment is best done with a 5-MHz probe or even a 7.5-MHz probe, with the focal zone set at the expected level of the peritoneum. In a clinical situation, enhancement of the peritoneal stripe is a highly specific but insensitive sign to detect pneumoperitoneum.41 Loculated fluid collections can mimic portions of the GI tract. Left upper quadrant and pelvic collections suggestive of the stomach and rectum may be clarified by adding fluid orally and rectally. Assessing peristaltic activity and wall morphology also helps in distinguishing luminal from extraluminal collections. Interloop and flank collections are aperistaltic and tend to correspond in contour to the adjacent abdominal wall or intestinal loops, frequently forming acute angles, which are rarely seen with intraluminal fluid. The appearance of the perienteric soft tissues is frequently the first and most obvious clue to abdominal pathology on abdominal sonograms. Inflammation of the perienteric fat shows as a hyperechoic mass effect (see Fig. 8.15), often without the usual appearance of normal gut and its contained small pockets of gas. Neoplastic infiltration of the perienteric fat is often

Acute Abdomen: Sonographic Approach GAS Intraluminal Extraluminal Intraperitoneal Retroperitoneal Gut wall Gallbladder/biliary ducts Portal veins FLUID Intraluminal Normal caliber gut Dilated gut Extraluminal Free Loculated MASSES Neoplastic Inflammatory Perienteric Soft Tissues Inflamed fat Lymph nodes Gut Wall Caliber Peristalsis Clinical Interaction Palpable mass Maximal tenderness Sonographic Murphy sign Sonographic McBurney sign

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FIG. 8.29  Value of Gas for Sonographic Diagnosis in Two Patients.  (A) Pneumoperitoneum. Sonogram shows a bright, echogenic focus representing free air between the abdominal wall and liver. Also shown is enhancement of the peritoneal stripe. (B) Confirmatory plain film. (C) Transvaginal image shows a large, gas-containing abscess (arrows) posterior to the uterus (U), secondary to acute diverticulitis in a renal transplant recipient. (D) Confirmatory CT scan shows the air containing deep abscess (arrows).

indistinguishable from inflammatory infiltration on ultrasound (see Fig. 8.8C and D). Mesenteric adenopathy is another manifestation of both inflammatory and neoplastic processes of the gut that should be specifically sought when performing abdominal sonography. As elsewhere, lymph nodes tend to change in size and shape when replaced by abnormal tissue. A normal, oval or flattened lymph node with a normal linear hilar echo becomes increasingly round and hypoechoic with either inflammatory or neoplastic replacement. In contrast to the sonographic appearance of loops of gut, mesenteric lymph nodes typically appear as focal, discrete hypoechoic masses of varying size (see Fig. 8.16). Their identification on sonography suggests enlargement because they are not usually seen on routine examinations. In the presence of mesenteric adenopathy, abnormal masses related to or causing a GI tract abnormality should also be sought; these most often are neoplastic or inflammatory in origin.

Right Lower Quadrant Pain Acute Appendicitis Acute appendicitis is the most common explanation for the “acute abdomen presentation” to an emergency department. Patients typically have right lower quadrant (RLQ) pain, tenderness, and leukocytosis. A mass may also be palpable. The patient with a classic presentation may have an appendectomy without preoperative imaging. This approach often becomes complicated when a normal appendix is removed in a patient with symptoms caused by other factors. On the other hand, surgery may be delayed in some patients with acute appendicitis if the presentation is atypical. This approach may lead to perforation before the surgery, making it a complicated and difficult procedure, often followed by abscess formation. In older clinical literature before routine cross-sectional imaging was available, laparotomy resulted in removal of normal, noninflamed appendices in 16% to 47% of cases (mean, 26%).42,43 Also, perforation occurred in up to 35%

CHAPTER 8  The Gastrointestinal Tract of patients.44 It is a balance between this negative laparotomy rate and the perforation rate at surgery that motivates crosssectional imaging before initiating treatment for the patient with acute RLQ pain. For a patient with suspected appendicitis, the sonographic objectives are to identify the patient with acute appendicitis, to identify the patient without acute appendicitis, and, in this latter population, to identify an alternate explanation for the RLQ pain. Symptoms of appendicitis, RLQ pain, and elevated white blood cell count overlap with a variety of other GI conditions, including typhlitis, mesenteric adenitis, Crohn disease, right-sided diverticulitis, segmental infarction of the omentum, and, in women, acute gynecologic conditions such as ruptured or torsion of an adnexal cyst or pelvic inflammatory disease.45 Urologic disease, especially stone-related and right-sided segmental omental infarction, may also mimic acute appendicitis. Addressing the value of sonography in establishing an alternative diagnosis in patients with suspected acute appendicitis, Gaensler et al.46 found that 70% of patients with another diagnosis had abnormalities visualized on the sonogram. From a retrospective review of 462 patients with suspected appendicitis who underwent appendectomy, Bendeck et al.47 found that women in particular benefit most from preoperative imaging, with a statistically significant, lower negative appendectomy rate than women with no preoperative imaging. Both CT and ultrasound provide sensitive and accurate diagnosis of appendicitis. The choice of imaging modality is determined somewhat by local expertise.48 Some institutions also screen patients on the basis of their weight, sending thin patients for ultrasound and reserving CT for larger patients. These considerations aside, we recommend sonographic evaluation of all women (and children)—with the addition of transvaginal scan for all patients whose pain is still not explained after completion of a traditional suprapubic pelvic sonogram. The pathophysiology of acute appendicitis likely involves obstruction of the appendiceal lumen, with 35% of cases demonstrating a fecalith.49 Mucosal secretions continue, increasing the intraluminal pressure and compromising venous return. The mucosa becomes hypoxic and ulcerates. Bacterial infection ensues,

Acute Appendicitis: Sonographic Diagnosis IDENTIFY APPENDIX Blind ended Noncompressible Aperistaltic tube Gut signature Arising from base of cecum (typically appendix is caudal to the base of the cecum but it may also be retrocecal and retroileal) Diameter greater than 6 mm (some use 7 mm for greater specificity) SUPPORTIVE FEATURES Inflamed perienteric fat Pericecal collections Appendicolith

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eventually with gangrene and perforation. A walled-off abscess is more common than free peritoneal contamination. Acute appendicitis begins with transient, visceral, or referred crampy pain in the periumbilical area associated with nausea and vomiting. Coincident with inflammation of the serosa of the appendix, the pain shifts to the RLQ and may be associated with physical signs of peritoneal irritation. Both clinical and experimental data support the belief that some patients have repeated attacks of appendicitis.50,51 In 1986 Puylaert6 described the value of graded compression sonography in the evaluation of 60 consecutive patients suspected of having acute appendicitis. Puylaert’s initial reports of success in diagnosing acute appendicitis depended solely on visualization of the abnormal appendix, a blind-ended, noncompressible, aperistaltic tube arising from the tip of the cecum with a gut signature (Fig. 8.30). However, other investigators reported seeing normal appendices on a sonogram.52,53 The normal appendix is compressible, with a wall thickness of 3 mm or less54 (Fig. 8.31, Video 8.13). Jeffrey et al.55 concluded that size can differentiate the normal from the acutely inflamed appendix. Threshold levels for the diameter of the appendix, above which acute appendicitis is highly likely, have been set at either 6 mm or 7 mm, with a resultant change in sensitivity and specificity. Sonographic visualization of an appendix with an appendicolith, regardless of appendiceal diameter, should also be regarded as a positive test. Rettenbacher et al.56 added assessment of appendiceal morphology in confirming suspicion of appendicitis. A round or partly round appendix had a high correlation with acute appendicitis, whereas an ovoid appendix did not. Color Doppler is also contributory, showing hyperemia in the appendiceal wall in the acutely inflamed appendix. Lee et al.57 described visualization of the appendix in 485 of 570 patients (85%) using graded compression sonography alone. Use of a posterior manual compression technique allowed for identification of the appendix in an additional 57 of the remaining 85 patients, increasing the percentage of identified appendices to 95%. The appendix positioned in the true pelvis may show subtle evidence of inflammation on a suprapubic scan because the pathology may be deep in the pelvic cavity. In our experience, this occurs most often in women, possibly related to a more capacious pelvis, and the clinical presentation is frequently that of pelvic inflammatory disease. This particular disease is optimally studied with transvaginal placement of the ultrasound probe because the appendix is often intimately related to either the uterus or the ovaries. The origin of such an appendix from the base of the cecum may be impossible to determine on transvaginal sonography, and compression with the ultrasound probe is often not feasible. Nonetheless, the identification of the blind-ended tip of the appendix with an increased diameter, luminal distention, and inflammation of the surrounding fat is obvious (Fig. 8.32). If rupture of a pelvic appendix has occurred before the sonogram, the identification of a pelvic abscess without identification of the appendix itself may produce an equivocal result as to the source of the pelvic inflammatory problem. Although the sensitivity of sonography for the diagnosis of appendicitis decreases with perforation, features associated with

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FIG. 8.30  Acute Appendicitis in Three Patients.  (A), (C), and (E) Long-axis views show the blind-ended tip of the appendix. (C) Tip is directed to the left of the image as the appendix ascends cephalad from its origin from the cecum. (B), (D), and (F) Corresponding cross-sectional views. The appendix looks round in short axis on all cases, and the lumen is distended with fluid. The appendix is surrounded with inflamed fat. The gut signature is preserved in the top two cases (A-D). The bottom case (E and F) shows loss of definition of the wall layers, suggesting gangrenous change.

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FIG. 8.31  Normal Appendix.  (A) Long-axis image and (B) cross-sectional image show the normal appendix (A) arising from the base of the cecum (C). The appendix shows a gut signature, a blind end, and measures 6 mm or less in diameter. See also Video 8.13.

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FIG. 8.32  Value of Transvaginal Sonography for Diagnosis of Acute Appendicitis.  (A) Long-axis view of the appendix on transvaginal sonography was the only view to show the blind-ended tip of the fluid-distended appendix. (B) Appendix is a large, fluid-filled, thick-walled structure and shows a shadowing appendicolith.

Sonography of Appendiceal Perforation Loculated pericecal fluid Phlegmon Abscess Prominent pericecal fat Circumferential loss of submucosal layer of the appendix

its occurrence include loculated pericecal fluid, phlegmon or abscess, prominent pericecal or periappendiceal fat, and circumferential loss of the submucosal layer of the appendix58 (Fig. 8.33, Video 8.14). False-positive diagnosis for acute appendicitis may occur if a normal appendix or a thickened terminal ileum is mistaken for an inflamed appendix.

Crohn Appendicitis Patients with Crohn disease may have acute appendicitis caused by IBD involvement of the appendix, in contrast to acute suppurative appendicitis. The wall of the appendix typically is extremely thickened and hyperemic with wall layer preservation, and the luminal surfaces are often in apposition59 (Fig. 8.34). This appearance contrasts with that in suppurative appendicitis,

where luminal distention is the expectation and wall thickening is moderate at best. Crohn appendicitis is a self-limited process,60,61 and treatment may be conservative if the appropriate diagnosis can be established with noninvasive techniques. In a small number of the patients for whom we have suggested this diagnosis, follow-up sonograms have shown resolution of the sonographic findings with no disease progression. Patients with Crohn disease who present with Crohn appendicitis account for about 10% of total presentations. This patient population typically has a more benign course. If the appendix is removed surgically in the mistaken belief that the patient has acute suppurative appendicitis, recurrence or progression of Crohn disease is rare.

Right-Sided Diverticulitis Acute inflammation of a right-sided diverticulum is distinct from the more common diverticulitis that is encountered in the left hemicolon. These diverticula occur more often in women than in men and have a predilection for Asian populations. Most patients are young adults. Right-sided diverticula are usually solitary and are congenital in origin. They are true diverticula and therefore have all layers of the gut wall. Their inflammation is associated with RLQ pain, tenderness, and leukocytosis, with a mistaken diagnosis of appendicitis in virtually all cases.

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FIG. 8.33  Perforation of Appendix in Three Patients.  (A) Long-axis image and (B) cross-sectional image show the blind-ended appendix. There is loss of definition of the wall layers, and the appendix is surrounded by an echogenic mass effect representing inflamed fat in the mesoappendix. (A) Arrow points to a bubble of extraluminal gas at the tip of the appendix; tip perforation was confirmed at surgery. (C) Sonogram and (D) CT scan show a periappendiceal abscess. The decompressed appendix is seen centrally on the sonogram. (E) Long-axis and (F) transverse images in the right lower quadrant show an abscess with an escaped appendicolith with acoustic shadowing. The appendix is no longer visible. See also Video 8.14. (C with permission from Birnbaum B, Wilson S. Appendicitis at the millennium. Radiology. 2000;215[2]:337-348.48)

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FIG. 8.34  Crohn Appendicitis.  (A) Transverse sonogram in the right lower quadrant shows a thick-walled loop of gut surrounded by inflamed fat. (B) Cross-sectional and (C) long-axis high-frequency linear images of this loop of gut show that it is blind ended. There is massive mural thickening and hyperemia. The luminal surfaces are in apposition. All changes resolved completely with conservative management. (With permission from Wilson SR. The bowel wall looks thickened: what does that mean? In: Cooperberg PL, editor. RSNA categorical course syllabus. Chicago: RSNA; 2002. pp. 219-228.1)

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On sonography, acute diverticulitis is associated with inflammation of the pericolonic fat. The diverticula may be located in the cecum or the adjacent ascending colon. When inflamed, they may have one of two appearances.62 Most often, the diverticulum may show as a pouch or saclike structure arising from the colonic wall63 (Fig. 8.35). Wall layers are continued into the wall of the congenital diverticulum. Hyperemia of the diverticulum and the inflamed fat is typical. If a fecalith is present within the diverticulum, it may show as a bright, echogenic focus located within or beyond a segment of thickened colonic wall. Occasionally, the culprit diverticulum is not evident and the only observations are those of inflamed fat and focal thickening of the colonic

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wall. In the appropriate clinical milieu, this is highly suspicious for acute diverticulitis. Treatment of acute diverticulitis is conservative and not surgical, emphasizing the importance of preoperative imaging in patients with RLQ pain attributed to this condition.

Acute Typhlitis Immunocompromised patients are most often affected with acute typhlitis. Although infrequent today in North America, AIDS patients previously accounted for the overwhelming majority of cases of acute typhlitis seen since 1990. Cytomegalovirus (CMV) and Cryptosporidium are the pathogens isolated most often in

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FIG. 8.35  Right-Sided Diverticulitis in Two Patients.  Transverse sonograms through the ascending colon (AC) show a hypoechoic pouchlike projection, representing the inflamed diverticulum, which arises from (A) the lateral wall of the gut and (B) the medial border of the gut. Both are surrounded by inflamed fat (arrows).

patients with typhlitis and colitis, although other organisms have been implicated. Sonographic study most often shows striking concentric, uniform thickening of the colon wall, usually localized to the cecum and the adjacent ascending colon64 (Fig. 8.36). The colon wall may be several times the normal thickness, reflecting inflammatory infiltration throughout the gut wall.65,66 Acute abdominal catastrophe in patients with AIDS is usually a complication of CMV colitis with deep ulceration and may result in hemorrhage, perforation, and peritonitis.67 Tuberculous colitis may similarly affect the right colon and is frequently associated with lymphadenopathy (particularly involving the mesenteric and omental nodes), splenomegaly, intrasplenic masses, ascites, and peritoneal masses, all of which may be assessed using sonography.

Mesenteric Adenitis With Terminal Ileitis Mesenteric adenitis, in association with acute terminal ileitis, is the most frequent GI cause of misdiagnosis of acute appendicitis. Patients typically have RLQ pain and tenderness. On the sonographic examination, enlarged mesenteric lymph nodes and mural thickening of the terminal ileum are noted. Yersinia enterocolitica and Campylobacter jejuni are the most common causative agents.68,69 Right-Sided Segmental Omental Infarction Right-sided segmental infarction of the omentum is a rare condition invariably mistaken clinically for acute appendicitis.70 Of unknown origin, it is postulated to occur with an anomalous and fragile blood supply to the right lower omentum, making it susceptible to painful infarction. Patients experience RLQ pain

and tenderness and are diagnosed clinically with acute appendicitis. On sonography, a plaque or cakelike area of increased echogenicity, suggesting inflamed or infiltrated fat, is seen superficially in the right flank with adherence to the peritoneum70 (Fig. 8.37). No underlying gut abnormality is shown. Because segmental infarction is a self-limited process, its correct diagnosis will prevent unnecessary surgery. CT scan is confirmatory, showing streaky fat in a masslike configuration in the right side of the omentum.

Left Lower Quadrant Pain The sonographic evaluation of the patient with left lower quadrant (LLQ) pain is less problematic than that of the patient with pain on the right side as acute diverticulitis is the explanation for the overwhelming majority of cases for which a valid explanation for the pain is found. The diagnostic features of acute diverticulitis are also less variable than those for acute appendicitis, making a suspicion of diverticulitis a good indication for the use of sonographic examination.

Acute Diverticulitis Diverticula of the colon are usually acquired deformities and are found most frequently in Western urban populations.71 The incidence of diverticula increases with age,72 affecting approximately half the population by the ninth decade. Muscular dysfunction and hypertrophy are constant associated features. Diverticula are usually multiple, and their most common location is the sigmoid and left colon. Both acute diverticulitis and spastic diverticulosis may be associated with a classic triad of presentation: LLQ pain, fever, and leukocytosis. Diverticula may also be

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FIG. 8.36  Acute Typhlitis in AIDS Patient With Cytomegalovirus Colitis.  (A) Long-axis view of the ascending colon shows marked mural thickening of the cecum and the wall of the ascending colon. Wall layer preservation is noted. (B) Crosssectional view of the thickened colon (at level of left arrow in A), with luminal surfaces in apposition. (C) Cross-sectional view of the cecum (at level of right arrow in A), which is thick walled and shows a fluid-filled lumen. (With permission from Wilson SR. The bowel wall looks thickened: what does that mean? In: Cooperberg PL, editor. RSNA categorical course syllabus. Chicago: RSNA; 2002. pp. 219-228.1)

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FIG. 8.37  Acute Omental Infarction.  (A) Sonogram shows a large, tender mass in the right lower quadrant (RLQ; arrows) in older man with acute RLQ pain. The mass is uniformly echogenic and attenuating, with an ultrasound appearance suggesting inflamed fat. (B) Confirmatory CT scan shows the heterogeneous superficial fatty mass.

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found singly and in the right colon, where no association with muscular hypertrophy or dysfunction has been established. Inspissated fecal material is believed to incite the initial inflammation in the apex of the diverticulum leading to acute diverticulitis.73 Spread to the peridiverticular tissues and microperforation or macroperforation may follow. Localized abscess formation occurs more often than peritonitis. Fistula formation, with communication to the bladder, vagina, skin, or other bowel loops, is present in a minority of cases. Surgical specimens demonstrate shortening and thickening of the involved segment of colon, associated with muscular hypertrophy. The peridiverticular inflammatory response may be minimal or extensive. Sonography appears to be of value in early assessment of patients thought to have acute diverticulitis.74,75 Classic features include segmental thickened gut and inflamed diverticula and inflamed perienteric fat. A negative scan combined with a low clinical suspicion is usually a good indication to stop investigation. However, a negative scan in a patient with a highly suggestive clinical picture justifies a CT scan. Similarly, demonstration of extensive pericolonic inflammatory changes on the sonogram may be appropriately followed by CT scan to define better the nature and extent of the pericolonic disease before surgery or other intervention. Because diverticula and smooth muscle hypertrophy of the colon are so prevalent, it seems likely that they would be frequently seen on routine sonography, but this is not the usual experience. However, with the development of acute diverticulitis, both the inflamed diverticulum and the thickened colon become evident. Presumably, the impacted fecalith, with or without microabscess formation, accentuates the diverticulum, whereas smooth muscle spasm, inflammation, and edema accentuate the gut wall thickening. Identification of diverticula on the sonogram strongly indicates diverticulitis.76 Diverticula are arranged in parallel rows along the margins of the teniae coli, so careful technique is required to make their identification. After demonstration of a thickened loop of gut, the long axis of the loop should be determined (Fig. 8.38). Slight tilting of the transducer to the margins of the loop will increase visualization of the diverticula, because they may be on the lateral and medial edges of the loop rather than directly anterior or posterior (Fig. 8.39). Cross-sectional views are then obtained along the entire length of the thickened gut. Abnormalities must be confirmed on both views. Errors related to overlapping gut loops, in particular, can be virtually eliminated with this careful technique. Identification of diverticula on sonography is correlated highly with inflammation, because it is unusual to show the diverticula in the absence of inflammation (Fig. 8.40). Failure to identify gas-containing abscesses or interloop abscesses is the major source of error when using sonography to evaluate patients with suspected diverticulitis. The meticulous technique of following involved thickened segments of colon in long-axis and transverse section will help detect even small amounts of extraluminal gas. Sonographic features of diverticulitis include segmental concentric thickening of the gut wall that is frequently strikingly hypoechoic, reflecting the predominant thickening in the muscle

layer; inflamed diverticula, seen as bright, echogenic foci with acoustic shadowing or ring-down artifact within or beyond the thickened gut wall; acute inflammatory changes in the pericolonic fat, seen as poorly defined hyperechoic zones without obvious gas or fluid content (Fig. 8.41, Video 8.15); and abscess formation, seen as loculated fluid collections in an intramural, pericolonic, or remote location. With the development of extraluminal inflammatory masses, the diverticulum may no longer be identified on sonography, presumably being incorporated into the inflammatory process. Therefore demonstration of a thickened segment of colon with an adjacent inflammatory mass may be consistent with diverticulitis, but also with neoplastic or other inflammatory disease. Intramural sinus tracts appear as highamplitude, linear echoes, often with ring-down artifact, within the gut wall. Typically, the tracts are deep, between the muscularis propria and the serosa. Fistulas appear as linear tracts that extend from the involved segment of gut to the bladder, vagina, or adjacent loops. Their echogenicity depends on their content, usually gas or fluid. Thickening of the mesentery and inflamed mesenteric fat may also be seen (Fig. 8.41). The sonographic and clinical features of diverticulitis are more specific than those of acute appendicitis, and errors of diagnosis occur less often. However, torsion of appendices epiploicae (omentales) may produce a sonographic appearance so closely resembling acute diverticulitis that differentiation may be difficult.76 The inflamed or infarcted fat of the appendix shows as shadowing of increased echogenicity related to the margin of the colon, mimicking an inflamed diverticulum. However, regional perienteric inflammatory change is usually minimal, with fewer systemic symptoms. The noninflamed colonic appendices epiploicae are not visible, except with ascites, where they are seen as uniformly spaced, echogenic foci along the margins of the colon.

Sonography of Diverticulitis GUT Segmental concentric thickening of wall Hypoechoic reflecting muscular hypertrophy INFLAMED DIVERTICULA Echogenic foci within or beyond gut wall Intramural sinus tracts High-amplitude linear echoes within gut wall Acoustic shadowing or ring-down artifact PERIENTERIC SOFT TISSUE Inflammation of pericolonic fat Hyperechoic mass effect Thickening of the mesentery Abscess formation Loculated fluid collection Often with gas component Fistulas Linear tracts from gut to bladder, vagina, or adjacent loops Hypoechoic or hyperechoic

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FIG. 8.38  Muscular Hypertrophy From Diverticular Colon Disease.  (A) Long-axis sonogram of the sigmoid colon shows prominence of the outer muscular layer, the muscularis propria, which appears hypoechoic. The outer longitudinal muscle fibers are slightly more echogenic than the inner circular muscle fibers. (B) Cross-sectional view. (C) Characteristic CT scan shows the effects of the smooth muscle hypertrophy.

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FIG. 8.39  Diverticulum of Colon.  (A) Long-axis sonogram and (B) correlative CT scan show a small pouch (arrows) arising from the wall of the descending colon. There is mild inflammatory change in the perienteric fat.

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FIG. 8.40  Acute Diverticulitis of Sigmoid Colon in Three Patients.  Cross-sectional views of part of the left colon. (A) Mild prominence of the muscular layer. The diverticulum (arrow) shows as a bright, echogenic shadowing focus, possibly related to a fecalith within. The wall of the diverticulum is not evident. There is minimal inflamed fat. (B) Diverticulum (arrow) has a thick, hypoechoic wall. There is a small, bright focus centrally but no shadowing. (C) Larger focus of echogenicity and shadowing related to an abscess that formed at the base of the inflamed diverticulum. Diverticula frequently show optimally on the cross-sectional images.

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FIG. 8.41  Pericolonic Changes With Diverticulitis in Two Patients.  (A) Long-axis view of descending colon shows a long segment of thickened gut with prominent muscularis propria. Edema of the perienteric fat is striking and shows as a homogeneous echogenic mass effect deep to the gut. (B) Similarly inflamed fat; phlegmonous change (P) shows as a hypoechoic zone centrally within the fat. G, Gut. See also Video 8.15.

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OTHER ABNORMALITIES Occlusion of the GI tract lumen producing obstruction may be either mechanical, where an actual physical impediment to the progression of the luminal content exists, or functional, where paralysis of the intestinal musculature impedes progression (paralytic ileus).

Mechanical Bowel Obstruction Mechanical bowel obstruction (MBO) is characterized by (1) dilation of the GI tract proximal to the site of luminal occlusion, (2) accumulation of large quantities of fluid and gas, and (3) hyperperistalsis as the gut attempts to pass the luminal content beyond the obstruction. If the process is prolonged, exhaustion and overdistention of the bowel loops may occur, with a secondary decrease in peristaltic activity. There are three broad categories of mechanical obstruction: obturation obstruction, related to blockage of the lumen by material in the lumen; intrinsic abnormalities of the gut wall, associated with luminal narrowing; and extrinsic bowel lesions, including adhesions. Strangulation obstruction develops when the circulation of the obstructed intestinal loop becomes impaired. Sonography in patients with suspected MBO is frequently unhelpful as adhesions, the most common cause of intestinal obstruction, are not visible on the sonogram. Also, the presence of abundant gas in the intestinal tract, characteristic of most patients with obstruction, frequently produces sonograms of nondiagnostic quality. However, in the minority of patients with MBO who do not have significant gaseous distention, sonography may be helpful. In a prospective study of 48 patients, Meiser and Meissner77 found that ultrasound was positive in 25% of patients with a “normal” plain film. Ultrasound alone allowed complete diagnosis of the cause of obstruction in 6 patients in a retrospective study of sonography on 26 patients with known colonic obstruction; it also correctly predicted the location of colonic obstruction in 22 cases (85%) and the cause of the obstruction in 21 cases (81%).11 Of 13 patients ultimately confirmed to have adenocarcinoma, 5 had a mass on sonography, 5 had segmental thickening, and 11 others showed a target sign of intussusception. Sonographic study of potential MBO should include assessment of the following: • GI tract caliber from the stomach to the rectum, noting any point at which the caliber alters (Fig. 8.42). • Content of any dilated loops, with special attention to their fluid and gaseous nature (Fig. 8.43; see also Videos 8.9, 8.10, and 8.16). • Peristaltic activity within the dilated loops, which is typically greatly exaggerated and abnormal, frequently producing a to-and-fro motion of the luminal content. With strangulation, peristalsis may decrease or cease. • Site of obstruction for luminal (large gallstones, bezoars,78 foreign bodies, intussusception, occasional polypoid tumors), intrinsic (segmental gut wall thickening and stricture formation from Crohn disease, annular carcinomas), and extrinsic (abscesses, endometriomas) abnormality as a cause of the obstruction (Video 8.16).

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• Location of gut loops, noting any abnormal position. Obstruction associated with external hernias is ideal for sonographic detection in that dilated loops of gut may be traced to a portion of the gut with normal caliber but abnormal location (Fig. 8.44). Spigelian and inguinal hernias are the types most frequently seen on sonograms. Unique sonographic features are seen in the following: Closed-loop obstruction occurs if the bowel lumen is occluded at two points along its length, a serious condition that facilitates strangulation and necrosis. As the obstructed loop is closed off from the more proximal portion of the GI tract, little or no gas is present within the obstructed segments, which may become dilated and fluid filled. Consequently, the abdominal radiograph may be unremarkable (Fig. 8.45A), and sonography may be most helpful by showing the dilated involved segments (Fig. 8.45B) and often the normal-caliber bowel distal to the point of obstruction. The features of closed-loop obstruction are well described on ultrasound and include dilated small bowel, a C- or U-shaped bowel loop (Fig. 8.45C), a whirl sign, and two adjacent collapsed loops.79,80 This last important observation is difficult to observe on ultrasound, in contrast to CT scan. However, we have correctly suspected closed-loop obstruction in many patients on the basis of virtually normal plain films, small bowel dilation, and a U- or C-shaped bowel loop, especially if there is gut wall thickening or pneumatosis intestinalis suggesting gut infarction. Afferent loop obstruction is an uncommon complication of subtotal gastrectomy, with Billroth II gastrojejunostomy, that may occur by twisting at the anastomosis, internal hernias, or anastomotic stricture. Again, a gasless, dilated loop may be readily recognized on sonography in a location consistent with the enteroenteric anastomosis coursing from the right upper quadrant across the midline. Its detection, location, and shape should allow for correct sonographic diagnosis of afferent loop obstruction.81 Intussusception, invagination of a bowel segment (the intussusceptum) into the next distal segment (the intussuscipiens), is seen on sonography of the abdomen most often as a transient and infrequent occurrence. However, it is a relatively infrequent cause of MBO in the adult, usually associated with a tumor as a lead point. In our experience, this is often a lipoma that appears as a highly echogenic, intraluminal mass related to its fat content. A sonographic appearance of multiple concentric rings, related to the invaginating layers of the telescoped bowel and seen in cross section, is virtually pathognomonic82 (Fig. 8.46A). Occasionally, only a target appearance may be seen.83,84 The longitudinal appearance suggesting a “hay fork”84 is not as reliably detected. In both projections, the mesenteric fat invaginating with the intussusceptum will show as an eccentric area of increased echogenicity. A lipoma, as a lead point, similarly shows as a focus of increased echogenicity (Fig. 8.46B and C). Midgut malrotation predisposes to MBO and infarction. It is infrequently encountered in adults. A sonographic abnormality related to the superior mesenteric vessels suggests malrotation.85 On transverse sonograms, the superior mesenteric vein is seen on the left ventral aspect of the superior mesenteric artery, a reversal of the normal relationship.

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FIG. 8.42  Mechanical Small Bowel Obstruction.  (A) Sagittal image of right flank shows multiple, adjacent, long loops of dilated, fluid-filled small bowel with the classic morphology for a distal mechanical small bowel obstruction. (B) Transverse image in the left lower quadrant confirms the multiplicity of dilated loops involved in the process. A small amount of ascites is seen between the dilated loops.

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FIG. 8.43  Dilated Hypoperistaltic Segments.  (A) Sagittal sonogram in the right flank of a patient with a Crohn stricture shows gross dilation of the ascending colon. A long, fluid-sediment level is seen as a reflection of the hypoperistalsis of this segment of obstructed gut. (B) Sagittal sonogram in a patient with paralytic ileus shows extensive small bowel dilation. Loops are fluid filled and quiet with fluid-fluid level (arrowheads). See also Video 8.16. K, Kidney. (A with permission from Sarrazin J, Wilson SR. Manifestations of Crohn disease at US. Radiographics. 1996;16[3]:499-520.21)

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FIG. 8.44  Mechanical Small Bowel Obstruction: Ventral Hernia.  (A) Sonogram shows dilated fluid-filled loops of small bowel with edematous valvulae conniventes. (B) Transverse paraumbilical sonogram shows normal-caliber gut lying in abnormal superficial location between two dilated loops of small bowel (SB).

CHAPTER 8  The Gastrointestinal Tract

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Paralytic Ileus Paralytic ileus is a type of bowel obstruction related to adynamic function of the bowel wall. Paralysis of the intestinal musculature, in response to general or local insult, may impede the progression of luminal contents. Although the lumen remains patent, no progression occurs. Sonography is usually of little value because these patients characteristically have poor-quality sonograms resulting from large quantities of gas in the intestinal tract. However, on rare occasions, the sonogram may demonstrate dilated, fluid-filled, very quiet, or aperistaltic loops of intestine. A fluid-fluid level in a dilated loop is characteristic of paralytic ileus, reflecting lack of movement of the intestinal contents (see Fig. 8.43).

Gut Edema Patients with acute vasculitis of various causes may present with acute abdominal pain and ascites, with massive edema of the small bowel wall seen as the major abnormality on imaging.

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FIG. 8.45  Closed-Loop Obstruction.  (A) Plain film is unremarkable. (B) Sonogram shows grossly dilated, gasless, fluid-filled, small bowel loops. (C) Single loop shows a suggestive C or U shape.

Hypoalbuminemia, congestive heart failure, and spontaneous venous thrombosis may also show diffuse edema of the gut wall. Prominent, thickened, hypoechoic valvulae conniventes (Fig. 8.47) and gastric rugae are relatively easy to recognize on the sonographic study, which should also include Doppler evaluation of the mesenteric and portal veins.

Gastrointestinal Tract Infections Although fluid-filled, actively peristaltic gut may be seen with infectious viral or bacterial gastroenteritis, most affected patients do not demonstrate a sonographic abnormality. However, some pathogens, notably Yersinia enterocolitica, Mycobacterium tuberculosis, and Campylobacter jejuni, produce highly suggestive sonographic abnormalities in the ileocecal area, as described earlier. Certain high-risk populations, such as those with AIDS and neutropenia,64 appear to be susceptible to acute typhlitis and colitis, which also have a highly suggestive sonographic appearance.

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Abdominal and Pelvic Sonography FIG. 8.46  Intussusception in Two Patients  (A) Sonogram shows multiple concentric rings representative of the invaginating intussuscipiens and the intussusceptum. Submucosal metastatic nodule as lead point. (B) Sonogram of the right lower quadrant shows a highly echogenic lead point related to a lipoma (arrow). The invaginating fat in the mesentery is also echogenic. (C) Confirmatory CT scan for image B. (B and C with permission from Wilson SR. The bowel wall looks thickened: what does that mean? In: Cooperberg PL, editor. RSNA categorical course syllabus. Chicago: RSNA; 2002. pp. 219-228.1)

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AIDS Patients Today, effective antiviral medications for HIV infection have drastically changed the outlook for those living with AIDS in the Western world. Nonetheless, patients with AIDS are at increased risk for development of both GI tract neoplasia, especially lymphoma (see Fig. 8.10C and D), and unusual opportunistic infections, most often Candida esophagitis and CMV colitis65,66 (see Fig. 8.36). Pseudomembranous Colitis Pseudomembranous colitis is a necrotizing inflammatory bowel condition that may occur as a response to a heterogeneous group of insults. At present, antibiotic therapy with effects from the toxin of Clostridium difficile, a normal inhabitant of the GI tract, is most often implicated. Watery diarrhea is the most common symptom and usually occurs during antibiotic therapy but may

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be quite remotely associated, occurring up to 6 weeks later. Endoscopic demonstration of pseudomembranous exudative plaques on the mucosal surface of the gut and culture of the enterotoxin of C. difficile are diagnostic. Superficial ulceration of the mucosa is associated with inflammatory infiltration of the lamina propria and the submucosa, which may be thickened to many times the normal size.86 Sonography is frequently performed before pseudomembranous colitis is diagnosed, often based on a history of fever, abdominal pain, and watery diarrhea. Sonographic features have only rarely been described87,88 but are suggestive of pseudomembranous colitis. Usually the entire colon is involved in a process that may produce striking thickening of the colon wall. Exaggerated haustral markings and a nonhomogeneous thickened submucosa, with virtual apposition of the mucosal surfaces of the thickened walls, are characteristic63 (Fig. 8.48).

CHAPTER 8  The Gastrointestinal Tract

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FIG. 8.47  Small Bowel Edema Secondary to Vasculitis.  (A) and (B) Sonograms show marked edema of the valvulae conniventes of the entire small bowel. (C) is a confirmatory CT scan with identical observations. (With permission from Wilson S. Evaluation of the small intestine by ultrasonography. In: Gourtsoyiannis N, editor. Radiologic imaging of the small intestine. Heidelberg: Springer-Verlag; 2002. pp. 73-86.18)

Pseudomembranous colitis should be suspected in any patient with diffuse colonic wall thickening but without a previous history of IBD. Because the history of concurrent or prior antibiotic therapy is not always given, direct questioning of the patient is frequently helpful.

Congenital Cysts Duplication cysts, characterized by the presence of the normal layers of the gut wall, can occur in any portion of the GI tract. These cysts may be visualized on sonogram, either routine or endoscopic, and should be considered as diagnostic possibilities whenever unexplained abdominal cysts are seen. Tailgut cysts are variants of abdominal cysts that are seen in the presacral region and are related to the rectum (Fig. 8.49). Ischemic Bowel Disease Ischemic bowel disease most often affects the colon and is most prevalent in older persons with arteriosclerosis. In younger patients, it may complicate cardiac arrhythmia, vasculitis, coagulopathy, embolism, shock, or sepsis.12 Sonographic features

of ischemic bowel disease have been poorly described, although gut wall thickening may be encountered. Pneumatosis intestinalis may complicate gut ischemia with a characteristic sonographic appearance.

Pneumatosis Intestinalis Pneumatosis intestinalis is a relatively rare condition in which intramural pockets of gas are found throughout the GI tract. It has been associated with a wide variety of underlying conditions, including chronic obstructive pulmonary disease, collagen vascular disease, IBD, traumatic endoscopy, and post–jejunoileal bypass. In many situations, affected patients are asymptomatic and the observation is incidental. However, its demonstration is of great clinical significance when necrotizing enterocolitis or ischemic bowel disease is present. Both conditions are associated with mucosal necrosis in which gas from the lumen passes to the gut wall. Sonographic description of pneumatosis intestinalis is limited to isolated case reports. High-amplitude echoes may be demonstrated in the gut wall, with typical air artifact or shadowing89,90

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FIG. 8.48  Pseudomembranous Colitis.  (A) Long-axis view and (B) cross-sectional view of the ascending colon show striking mural thickening of the gut wall. (With permission from O’Malley M, Wilson S. US of gastrointestinal tract abnormalities with CT correlation. Radiographics. 2003;23[1]:59-72.63)

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FIG. 8.49  Congenital Cysts.  (A) Sagittal and (B) transverse sonograms in the epigastrium show an incidental gastric duplication cyst adjacent to the lesser curve of the stomach (S). (C) Suprapubic and (D) transvaginal pelvic scans show a complex, presacral pelvic mass, an incidental tailgut cyst.

CHAPTER 8  The Gastrointestinal Tract (Fig. 8.50). Gut wall thickening may be noted if the pneumatosis is associated with underlying IBD. If gut ischemia is suspected, careful evaluation of the liver is recommended to look for evidence of portal venous air.

Mucocele of Appendix Mucocele of the appendix is relatively uncommon, occurring in 0.25% of 43,000 appendectomy specimens in one series. Many patients with this condition are asymptomatic. A mass may be

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palpated in approximately 50% of cases. Benign and malignant varieties occur in a ratio of approximately 10 : 1.91 In the benign form the appendiceal lumen is obstructed by either inflammatory scarring or fecaliths. The glandular mucosa in the isolated segment continues to secrete sterile mucus. The neoplastic variety of mucocele is associated with primary mucous cystadenoma or cystadenocarcinoma of the appendix. Although the gross morphology of the appendix may be similar in the benign and malignant varieties, the malignant form is often associated with pseudomyxoma peritonei if rupture occurs.92 On sonography, mucoceles typically produce large, hypoechoic, well-defined RLQ cystic masses with variable internal echogenicity, wall thickness, and wall calcification (Fig. 8.51). The internal contents often show a laminated or whorled appearance. These masses are frequently retrocecal and may be mobile.

Gastrointestinal Tract Hematoma Blunt abdominal trauma, complicated by duodenal hematoma and rectal trauma, either sexual or iatrogenic after rectal biopsy, are the major causes of local hematomas seen on sonography. Hematoma is usually localized to the submucosa. Larger or more diffuse hematomas may complicate anticoagulation therapy or bleeding disorders associated with leukemia. If hematomas are large, diffuse gut wall thickening may be seen on sonograms.

FIG. 8.50  Pneumatosis Intestinalis.  Sonogram shows three loops of gut with bright, high-amplitude echoes (arrows) originating within the gut wall.

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Peptic Ulcer Peptic ulcer, a defect in the epithelium to the depth of the submucosa, may be seen in either gastric or duodenal locations. Although rarely visualized, peptic ulcer has a fairly characteristic sonographic appearance. A gas-filled ulcer crater is seen as a bright, echogenic focus with ring-down artifact, either in a focal area of wall thickening or beyond the wall, depending on the depth of penetration (Fig. 8.52). Edema in the acute phase and fibrosis in the chronic phase may produce localized wall thickening and deformity.

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FIG. 8.51  Mucocele of the Appendix.  (A) Sonogram and (B) CT scan show a large, mucus-filled appendix as an incidental observation. The whorled appearance on the sonogram is characteristic. There is a fleck of calcification in the wall on the CT scan.

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FIG. 8.52  Peptic Ulcer.  (A) Cross-sectional sonogram of the stomach shows a hypoechoic eccentric mass with a bright, central echogenic focus representing air in the ulcer crater. (B) Confirmatory scan with barium swallow.

Bezoars Bezoars are masses of foreign material or food, typically found in the stomach after surgery for peptic ulcer disease (phytobezoars) or after ingestion of indigestible organic substances such as hair (trichobezoars). These masses may produce shadowing intraluminal densities on the sonogram and have been documented as a rare cause of small bowel obstruction.78 They may also form in the small bowel in association with chronic stasis. Intraluminal Foreign Bodies Large foreign bodies, including bottles, candles, sexual vibrators, contraband, tools, and food, may be identified in the GI tract, particularly in the rectum and sigmoid colon, where they produce fairly sharp, distinct specular echoes with sharp, acoustic shadows. Their recognition is enhanced by suspicion of their presence. Celiac Disease Undiagnosed adult patients with celiac disease are encountered infrequently in general ultrasound departments. Nonetheless, I have occasionally seen patients in whom sonography is the first test to suggest the correct diagnosis. Sonographic observations include abnormal fluid-filled small intestine with moderate dilation of the involved loops. Abnormal morphology is observed, which Dietrich et al.93 describe as a reduction in Kerckring plicae circulares (valvulae conniventes) with loss of density and uniformity. Peristalsis is increased above normal. An increase in the caliber of the superior mesenteric artery and portal vein may also be seen.94 Cystic Fibrosis Aggressive treatment of the pulmonary problems of cystic fibrosis (CF) increases the likelihood of encountering adult patients in a general ultrasound department that performs abdominal

sonography. Thickening of the gut wall, particularly of the right hemicolon and to a lesser extent the left colon and small bowel, may be seen in association with infiltration of both the pericolonic and the mesenteric fat.95 These may often be incidental observations without significant associated symptomatology. In advanced CF, a fibrosing colonopathy with stricture may be seen.96,97 The culture of C. difficile is also documented in some patients with CF and colon wall thickening, without the accompanying symptoms of abdominal pain and diarrhea.98 However, positive stool culture is not the rule in CF patients with detectable colon wall thickening.

ENDOSONOGRAPHY Endoscopic sonography, performed with high-frequency transducers in the lumen of the gut, allows for detection of mucosal abnormality, delineation of the layers of the gut wall, and definition of the surrounding soft tissues to a depth of 8 to 10 cm from the transducer crystal. Thus tumors hidden below normal mucosa, tumor penetration into the layers of the gut wall, and tumor involvement of surrounding vital structures or lymph nodes may be well evaluated. Staging of previously identified mucosal tumors is one of the major applications of endosonographic technique.

Upper Gastrointestinal Tract Rotating, high-frequency transducers, using 7.5-MHz crystals fitted into a fiberoptic endoscope, are most suitable for endosonography of the esophagus, stomach, and duodenum. Light sedation of the patient is usually required. The patient is placed in the left lateral decubitus position and the endoscope inserted to the desired location. Intraluminal gas is aspirated, and a balloon covering the transducer crystal is inflated with deaerated water. Localization is determined from the distance of insertion from

CHAPTER 8  The Gastrointestinal Tract the teeth and identification of anatomic landmarks, such as the spleen, liver, pancreas, and gallbladder. Rotation and deflection of the transducer tip allow scanning of visualized lesions in different planes.99 Identification, localization, and characterization of benign masses are possible with endosonography. Varices are seen as compressible hypoechoic or cystic masses deep to the submucosa or in the outer layers of the esophagus, gastroesophageal junction, or gastric fundus.100 Benign tumors such as fibromas or leiomyomas are well-defined, solid masses without mucosal involvement that can be localized to the layer of the wall from which they arise, usually the submucosa and the muscularis propria, respectively. Peptic ulcer typically produces marked thickening of all layers of the gastric wall, with a demonstrated ulcer crater. Ménétrier disease produces thickening of the mucosal folds. Staging of esophageal carcinoma involves assessment of depth of tumor invasion and evaluation of involvement of the local lymph nodes and adjacent vital structures.101 Constricting lesions that do not allow passage of the endoscope may produce technically unsatisfactory or incomplete examinations. Gastric lymphoma is typically very hypoechoic; its invasion is along the gastric wall or horizontal, and involvement of extramural structures and lymph nodes is less than with gastric carcinoma. Thus, localized mucosal ulceration with extensive infiltration of the deeper layers suggests lymphoma, which may also grow with a polypoid pattern or as a diffuse infiltration without ulceration.102 Gastric carcinoma, in contrast, arises from the gastric mucosa, is usually more echogenic, tends to invade vertically or through the gastric wall, and frequently involves the perigastric lymph nodes at diagnosis.

Rectum: Tumor Staging of Rectal Carcinoma Transrectal (endorectal) sonography is an established modality for the staging of rectal carcinoma.103-105 Its resolution of the layers of the rectum surpasses the performance of both CT and MRI. Although a variety of pathologic conditions may be assessed with endorectal sonography, the staging of previously detected rectal carcinoma is its major role. Patients are scanned in the left lateral decubitus position following a cleansing enema. Both axial and sagittal images are obtained. A variety of rigid intrarectal probes are commercially available, using a range of transducer technologies with phased array, mechanical sector, and rotating crystals. Further, we have also been routinely evaluating women with rectal carcinoma using a transvaginal probe placed in the vagina after a Fleet enema. This technique is excellent, especially for larger tumors, because the rectovaginal septum, the tumor, and the lymph nodes in the mesorectum are more optimally seen.106 Tumors are staged according to the Astler-Coller modification107 of the Dukes Classification, or more simply with the primary tumor component of the Union Internationale Contre le Cancer (UICC) TNM classification,108 where T represents the primary tumor, N the nodal involvement, and M the distant metastases (Fig. 8.53).

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FIG. 8.53  Schematic of Tumor (T) Component of TNM Staging of Rectal Cancer on Sonography.  Tumors (red) exhibit progressively deeper invasion beginning at 10 o’clock, where T superficial noninvasive lesion involves only superficial layers of intestinal wall. At 7 o’clock, T1 lesion invades submucosa (yellow). At 5 o’clock, T2 lesion invades muscularis propria (blue). At 2 o’clock, T3 lesion exhibits full-thickness invasion through layers of rectal wall, with invasion of surrounding perirectal fat. In directly anterior aspect (12 o’clock), T4 lesion exhibits invasion of prostate gland.

Rectal carcinoma arises from the mucosal surface of the gut. Tumors appear as relatively hypoechoic masses that may distort the rectal lumen. Invasion of the deeper layers, the submucosa, the muscularis propria, and the perirectal fat produces discontinuity of these layers on the sonogram (Fig. 8.54). Superficial ulceration or crevices that allow small bubbles of gas to be trapped deep to the crystal surface may demonstrate ring-down artifact and shadowing, with loss of layer definition deep to the ulceration. Lymph nodes appear as round or oval, hypoechoic masses in the perirectal fat (Fig. 8.54C). Color Doppler is an excellent addition to transrectal probes, showing the extent of tumors on the basis of their hypervascularity (Fig. 8.55) Infrequently, actual deposits may be shown within enlarged nodes. Therefore definitive staging requires pathologic assessment of both the tumor and the regional nodes. Limitations of rectal sonography include the following: inability to identify microscopic tumor invasion, to image stenotic tumors, and to image tumors greater than 15 cm from the anal verge. It is also limited for distinguishing nodes involved with tumor from those with reactive change and to identify normalsized nodes with microscopic tumor invasion.

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FIG. 8.54  Rectal Tumors Seen at Transrectal Sonography.  (A) Rectal carcinoma: T1. Hypoechoic mass between 6 o’clock and 8 o’clock is noted. The submucosa (the echogenic line) and the muscularis propria (the external hypoechoic line) are intact. (B) Rectal carcinoma: T2. Tumor is seen anteriorly. The muscularis propria (arrows) is the hypoechoic line that is thickened and nodular, consistent with tumor involvement. (C) Rectal carcinoma: T3. A large tumor involves the entire right lateral wall of the rectum. Invasion of the perirectal fat (arrows) is noted in several locations. A large node is seen at the 6 o’clock position; smaller nodes are seen at 5 o’clock and 8 o’clock. (D) Metastatic prostate carcinoma to rectal wall. Hypoechoic mass is seen between 10 o’clock and 1 o’clock. It involves the deep layers of the rectal wall and not the rectal mucosa. There is a small lymph node (arrow). (With permission from Berton F, Gola G, Wilson S. Perspective on the role of transrectal and transvaginal sonography of tumors of the rectum and anal canal. AJR Am J Roentgenol. 2008;190[6]:1495-1504.106)

Recurrent rectal cancer after local resection is usually extraluminal, involving the resection margin secondarily. Serial transrectal sonography may be used in conjunction with serum carcinoembryonic antigen levels to detect these recurrences. A pericolic hypoechoic mass or local thickening of the rectal wall, in either deep or superficial layers, is taken as evidence of recurrence. Previous radiation treatment may produce a diffuse thickening of the entire rectal wall, usually of moderate or high echogenicity, with an appearance that is usually easily differentiated from the focal hypoechoic appearance of recurrent cancer. Sonographic-guided biopsy of a detected abnormality facilitates histologic differentiation of recurrence from postoperative, inflammatory, or postradiation change. Prostatic carcinoma may invade the rectum directly, or more remote tumors may involve the rectum, usually as a result of

seeding to the posterior peritoneal pouch. Because these tumors initially involve the deeper layers of the rectal wall, with mucosal involvement occurring as the disease progresses, their sonographic appearance is distinct from that of primary rectal carcinoma (see Fig. 8.54D). Benign mesenchymal tumors, especially of smooth muscle origin, are uncommon in the rectum. When seen, their sonographic features are the same as elsewhere (Fig. 8.56). Mucous retention cysts, resulting from obstruction of mucous glands, produce cystic masses of varying size that are located deep in the rectal wall.

Anal Canal Cancer of the anal canal is a very rare tumor that is well shown on anal sonography (Fig. 8.57).

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FIG. 8.55  Contribution of Color Doppler at Transrectal Sonography to Staging and Diagnosis of Rectal Cancer.  (A) and (B) T2 rectal cancer in 58-year-old man. (A) Axial image shows hypoechoic tumor. Destruction of submucosa is evident with involvement of muscularis propria on right side of image. (B) Color Doppler shows typical hypervascularity. Color demarcates tumor from normal rectal wall on left side of image. (C) and (D) Small rectal adenocarcinoma originating in adenomatous polyp in 55-year-old man. (C) Axial image shows an isoechoic polypoid mass with a broad base surrounded by fluid within the rectal lumen. Mass involves the submucosal layer only. (D) Color Doppler image shows profuse vascularity and vascular stalk of the polypoid mass. (E) and (F) tubulovillous adenoma in 58-year-old woman. (E) Axial transvaginal image shows a mixed-echogenic mass that seems to fill the lumen of the rectum. (F) Color Doppler frequently shows this type of stellate, branching vascularity in tubulovillous tumors. (With permission from Berton F, Gola G, Wilson S. Perspective on the role of transrectal and transvaginal sonography of tumors of the rectum and anal canal. AJR Am J Roentgenol. 2008;190[6]:1495-1504.106)

FIG. 8.56  Gastrointestinal Stromal Tumor (GIST) of Rectum.  Transrectal sonographic image shows solid, well-defined, round mass arising from muscularis propria layer in 59-year-old woman with asymptomatic palpable mass found at routine physical examination. Tumor is growing with submucosal pattern, and mucosal surface bulges into fluid-filled lumen.

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FIG. 8.57  Cancer of Anal Canal.  (A) Long-axis image and (B) cross-sectional image show a hypoechoic tumor disrupting the normal planes of the anal canal. (C) Sonogram shows the vascularity of the tumor. (With permission from Berton F, Gola G, Wilson S. Perspective on the role of transrectal and transvaginal sonography of tumors of the rectum and anal canal. AJR Am J Roentgenol. 2008;190[6]:1495-1504.106)

CHAPTER 8  The Gastrointestinal Tract Fecal Incontinence Anal endosonography, performed with the addition of a hard cone attachment to a radial 7.5-MHz probe, allows accurate assessment of the anal canal, including the internal and external sphincters.109 Performed primarily for assessment of fecal incontinence, this test shows the integrity of the sphincters with documentation of the degree and size of muscle defects. We do not use this technique any longer, preferring instead assessment of the sphincter and perianal soft tissues with a combination of transvaginal and transperineal scan.37,110-113 Young women, following traumatic obstetric delivery, are most often afflicted with fecal incontinence. The internal anal sphincter, in continuity with the muscularis propria of the rectum above, is seen as a thick circular hypoechoic or hypoechoic ring just deep to the convoluted mucosal echoes (Fig. 8.58). The external

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anal sphincter, in contrast, is less well defined and more echogenic, appearing gray on the ultrasound examination, and in continuity with fibers from the puborectalis sling. Traumatic disruption of the muscle layers will show as defects in the continuity of the normal muscle texture, most often anterior (Fig. 8.59). Posttraumatic scarring may be associated with a change of shape of the anal canal from round to oval.

Perianal Inflammatory Disease Perianal inflammatory disease is seen in two distinct patient populations: (1) those with Crohn disease who develop perianal inflammation as part of their disease and (2) those who develop a perianal abscess or perianal fistula as a spontaneous event. The first group is described earlier in the section on Crohn disease. In other patients, perianal infection arises in small,

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FIG. 8.58  Normal Rectum and Anal Canal.  (A) Transvaginal approach. Cross-sectional image of rectum taken with vaginal probe showing the normal, convoluted rectal mucosa; prominent submucosa (white); and the muscularis propria as a thin, hypoechoic rim (arrows). The rectum is usually oval, as shown here. (B) Transperineal approach. Anal canal shows the thick, well-defined internal anal sphincter (arrows) as a continuous hypoechoic ring continuous with the muscularis propria of the rectal wall above. The external anal sphincter is less well defined and echogenic. (C) Transperineal approach. Rotation of the probe by 90 degrees from image B shows the anal canal in long axis (arrows, internal anal sphincter).

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FIG. 8.59  Traumatic Disruption of Anal Sphincter in Two Patients.  (A) Cross-sectional and (B) long-axis views of the anal canal from a transvaginal approach show disruption of the sphincter anteriorly from 9 to 3 o’clock. The arrow on the sagittal image shows the cephalad extent of the internal anal sphincter. (C) Cross-sectional and (D) long-axis views of the anal canal show full-thickness disruption of the anterior anal canal between 11 and 1 o’clock. The arrow in each image shows air bubbles within an anovaginal fistula.

intersphincteric anal glands predominantly located at the dentate line. This occurs most frequently in young adult men. Documentation of fluid collections and the relationship of inflammatory tracts to the sphincter mechanism are important for surgical treatment. We prefer transvaginal sonography (Video 8.17) in conjunction with transperineal sonography in women and transperineal sonography in men for evaluation of this problem. Scans are performed with curved and high-frequency linear probes placed firmly on the skin of the perineum between the introitus and the anal canal in women and between the scrotum and the anal canal in men.111 Firm pressure on the transducer is required to afford good visualization of the anal canal. We begin the procedure with the transducer in the transverse plane relative to the body. The transducer should be directed cephalad and anterior to the plane of the anal canal, then angled slowly through the plane of the anal canal, which will show it in cross section from the anorectal junction to the external anal

Sonography of Perianal Inflammatory Disease Internal opening in the anal canal or rectum Tracts and their relationship to anal sphincter External openings Fluid collections

opening. Rotation of the transducer by 90 degrees will allow for imaging in the longitudinal plane. Tracts and collections in the perineum, buttocks, scrotum, and labia can also be assessed and followed in a retrograde direction to their connection with the anal canal. Perianal inflammatory tracts and masses are classified according to Parks et al.114 Their classification provides an anatomic description of fistulous tracts, which acts as a guide to operative

CHAPTER 8  The Gastrointestinal Tract treatment. The four main subtypes are intersphincteric (between internal and external sphincter), transsphincteric (crossing both internal and external anal sphincter into ischiorectal or ischioanal fossa), suprasphincteric, and extrasphincteric. In each patient, we also document the internal opening and the external openings, as possible. Tracts show on the ultrasound scan as hypoechoic linear areas or fluid-containing tubular areas, depending on their size and activity (Fig. 8.60). As with fistulas elsewhere, air bubbles within the tract show as bright, echogenic foci that

307

may move during the scan, helping with their identification. In our initial experience with 54 patients with perianal inflammatory masses, sonographic findings were confirmed in 22 of 26 patients (85%) who underwent surgical treatment for their disease.

Acknowledgment The author would like to acknowledge Gordana Popovich for her artwork.

A

B

C

D

E

F

G

H

I

FIG. 8.60  Perianal Inflammatory Disease in Nine Patients.  Top row, Simple inflammatory openings and tracts (arrows). Cross-sectional images of the anal canal show internal opening at 1 o’clock with (A) transsphincteric tract running to a small collection; (B) intersphincteric tract; (C) larger extrasphincteric tract. Middle row, More complex tracts (arrows). (D) Anterior extrasphincteric tract shows fluid within. (E) Bilateral, complex, intersphincteric tracts and collections show bright, echogenic foci representing extraluminal air. (F) Boomerang, or horseshoe, tract surrounds the anal canal posteriorly and laterally. There are internal openings at 2, 4, and 9 o’clock. Bottom row, Perianal abscesses (A). (G) Abscess on left posterolateral aspect of the anal canal is particle filled. (H) Large, posterior abscess is complex, with a dependent debris level. (I) Large, posterior abscess shows a large internal opening posteriorly at 6 o’clock.

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PART II

Abdominal and Pelvic Sonography

REFERENCES 1. Wilson SR. The bowel wall looks thickened: what does that mean? In: Cooperberg PL, editor. RSNA categorical course syllabus. Chicago: RSNA; 2002. pp. 219-228. 2. Heyder N, Kaarmann H, Giedl J. Experimental investigations into the possibility of differentiating early from invasive carcinoma of the stomach by means of ultrasound. Endoscopy. 1987;19(6):228-232. 3. Kimmey MB, Martin RW, Haggitt RC, et al. Histologic correlates of gastrointestinal ultrasound images. Gastroenterology. 1989;96(2 Pt 1): 433-441. 4. Lutz HT, Petzoldt R. Ultrasonic patterns of space occupying lesions of the stomach and the intestine. Ultrasound Med Biol. 1976;2(2):129-132. 5. Bluth E, Merritt C, Sullivan M. Ultrasonic evaluation of the stomach, small bowel, and colon. Radiology. 1979;133(3 Pt 1):677-680. 6. Puylaert JB. Acute appendicitis: US evaluation using graded compression. Radiology. 1986;158(2):355-360. 7. Teefey SA, Roarke MC, Brink JA, et al. Bowel wall thickening: differentiation of inflammation from ischemia with color Doppler and duplex US. Radiology. 1996;198(2):547-551. 8. Romanini L, Passamonti M, Navarria M, et al. Quantitative analysis of contrast-enhanced ultrasonography of the bowel wall can predict disease activity in inflammatory bowel disease. Eur J Radiol. 2014;83(8):1317-1323. 9. Dillman JR, Stidham RW, Higgins PDR, et al. Ultrasound shear wave elastography helps discriminate low-grade from high-grade bowel wall fibrosis in ex vivo human intestinal specimens. J Ultrasound Med. 2014;33(12):2115-2123. 10. Lim JH. Colorectal cancer: sonographic findings. AJR Am J Roentgenol. 1996;167(1):45-47. 11. Lim JH, Ko YT, Lee DH, et al. Determining the site and causes of colonic obstruction with sonography. AJR Am J Roentgenol. 1994;163(5):1113-1117. 12. Shorter RG. Gastrointestinal pathology: an atlas and text. Mayo Clin Proc. 1989;64(12):1567-1568. 13. Kaftori J, Aharon M, Kleinhaus U. Sonographic features of gastrointestinal leiomyosarcoma. J Clin Ultrasound. 1981;9(1):11-15. 14. Derchi LE, Banderali A, Bossi C, et al. The sonographic appearances of gastric lymphoma. J Ultrasound Med. 1984;3(6):251-256. 15. Salem S, Hiltz C. Ultrasonographic appearance of gastric lymphosarcoma. J Clin Ultrasound. 1978;6(6):429-430. 16. Telerman A, Gerard B, Van den Heule B, Bleiberg H. Gastrointestinal metastases from extra-abdominal tumors. Endoscopy. 1985;17(3):99-101. 17. Yeh H. Ultrasonography of peritoneal tumors. Radiology. 1979;133(2):419-424. 18. Wilson S. Evaluation of the small intestine by ultrasonography. In: Gourtsoyiannis N, editor. Radiologic imaging of the small intestine. Heidelberg: Springer-Verlag; 2002. pp. 73-86. 19. Horsthuis K, Bipat S, Bennink R, Stoker J. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology. 2008;247(1):64-79. 20. Panés J, Bouzas R, Chaparro M, et al. Systematic review: the use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn’s disease. Aliment Pharmacol Ther. 2011;34(2):125-145. 21. Sarrazin J, Wilson SR. Manifestations of Crohn disease at US. Radiographics. 1996;16(3):499-520. 22. Gasche C, Moser G, Turetschek K, et al. Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut. 1999;44(1):112-117. 23. Medellin-Kowalewski A, Wilkens R, Wilson A, et al. Quantitative contrastenhanced ultrasound parameters in Crohn disease: their role in disease activity determination with ultrasound. AJR Am J Roentgenol. 2016;206(1):64-73. 24. DiCandio G, Mosca F, Campatelli A, et al. Sonographic detection of postsurgical recurrence of Crohn disease. AJR Am J Roentgenol. 1986;146(3):523-526. 25. Fraquelli M, Colli A, Casazza G, et al. Role of US in detection of Crohn disease: meta-analysis 1. Radiology. 2005;236(1):95-101. 26. Dubbins PA. Ultrasound demonstration of bowel wall thickness in inflammatory bowel disease. Clin Radiol. 1984;35(3):227-231. 27. Worlicek H, Lutz H, Heyder N, Matek W. Ultrasound findings in Crohn’s disease and ulcerative colitis: a prospective study. J Clin Ultrasound. 1987;15(3):153-163.

28. Spalinger J, Patriquin H, Miron M, et al. Doppler US in patients with Crohn disease: vessel density in the diseased bowel reflects disease activity. Radiology. 2000;217(3):787-791. 29. Ripollés T, Martínez M, Paredes J, et al. Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology. 2009;253(1):241-248. 30. Ripollés T, Rausell N, Paredes J, et al. Effectiveness of contrast-enhanced ultrasound for characterisation of intestinal inflammation in Crohn’s disease: a comparison with surgical histopathology analysis. J Crohns Colitis. 2013;7(2):120-128. 31. Parente F, Maconi G, Bollani S, et al. Bowel ultrasound in assessment of Crohn’s disease and detection of related small bowel strictures: a prospective comparative study versus x ray and intraoperative findings. Gut. 2002;50(4):490-495. 32. Ferraioli G, Tinelli C, Lissandrin R, et al. Point shear wave elastography method for assessing liver stiffness. World J Gastroenterol. 2014;20(16):4787-4796. 33. Dillman J, Stidham R, Higgins P, et al. US elastography–derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn Disease animal model. Radiology. 2013;267(3):757-766. 34. Lu C, Gui X, Chen W, et al. Ultrasound shear wave elastography identifies muscle wall hypertrophy and is a novel surrogate for inflammation in Crohn’s disease. United European Gastroenterol J. 2015;3:P0333. 35. Ripollés T, Martínez-Pérez M, Blanc E, et al. Contrast-enhanced ultrasound (CEUS) in Crohn’s disease: technique, image interpretation and clinical applications. Insights Imaging. 2011;2(6):639-652. 36. Stewart LK, McGee J, Wilson SR. Transperineal and transvaginal sonography of perianal inflammatory disease. AJR Am J Roentgenol. 2001;177(3):627-632. 37. Damani N, Wilson S. Nongynecologic applications of transvaginal US. Radiographics. 1999;19(Spec No):S179-S200. 38. Puylaert J. Ultrasound of acute GI tract conditions. Eur Radiol. 2001;11(10):1867-1877. 39. Seibert JJ, Williamson SL, Golladay ES, et al. The distended gasless abdomen: a fertile field for ultrasound. J Ultrasound Med. 1986;5(6):301-308. 40. Lee DH, Lim JH, Ko YT, Yoon Y. Sonographic detection of pneumoperitoneum in patients with acute abdomen. AJR Am J Roentgenol. 1990;154(1):107-109. 41. Muradali D, Wilson S, Burns PN, et al. A specific sign of pneumoperitoneum on sonography: enhancement of the peritoneal stripe. AJR Am J Roentgenol. 1999;173(5):1257-1262. 42. Pieper R, Forsell P, Kager L. Perforating appendicitis. A nine-year survey of treatment and results. Acta Chir Scand Suppl. 1986;530:51-57. 43. Kazarian K, Roeder W, Mersheimer W. Decreasing mortality and increasing morbidity from acute appendicitis. Am J Surg. 1970;119(6):681-685. 44. Van Way 3rd CW, Murphy JR, Dunn EL, Elerding SC. A feasibility study of computer aided diagnosis in appendicitis. Surg Gynecol Obstet. 1982;155(5):685-688. 45. Berry J, Malt R. Appendicitis near Its centenary. Ann Surg. 1984;200(5): 567-575. 46. Gaensler EH, Jeffrey RB, Laing FC, Townsend RR. Sonography in patients with suspected acute appendicitis: value in establishing alternative diagnoses. AJR Am J Roentgenol. 1989;152(1):49-51. 47. Bendeck S, Nino-Murcia M, Berry G, Jeffrey R. Imaging for suspected appendicitis: negative appendectomy and perforation rates. Radiology. 2002;225(1):131-136. 48. Birnbaum B, Wilson S. Appendicitis at the millennium. Radiology. 2000;215(2):337-348. 49. Shaw R. Appendix calculi and acute appendicitis. Br J Surg. 1965;52(6):451-459. 50. Savrin R, Clausen K, Martin E, Cooperman M. Chronic and recurrent appendicitis. Am J Surg. 1979;137(3):355-357. 51. Dachman AH, Nichols JB, Patrick DH, Lichtenstein JE. Natural history of the obstructed rabbit appendix: observations with radiography, sonography, and CT. AJR Am J Roentgenol. 1987;148(2):281-284. 52. Jeffrey RB, Laing FC, Townsend RR. Acute appendicitis: sonographic criteria based on 250 cases. Radiology. 1988;167(2):327-329. 53. Abu-Yousef MM, Bleicher JJ, Maher JW, et al. High-resolution sonography of acute appendicitis. AJR Am J Roentgenol. 1987;149(1):53-58. 54. Rioux M. Sonographic detection of the normal and abnormal appendix. AJR Am J Roentgenol. 1992;158(4):773-778. 55. Jeffrey RB, Laing FC, Lewis FR. Acute appendicitis: high-resolution real-time US findings. Radiology. 1987;163(1):11-14.

CHAPTER 8  The Gastrointestinal Tract 56. Rettenbacher T, Hollerweger A, Macheiner P, et al. Ovoid shape of the vermiform appendix: a criterion to exclude acute appendicitis—evaluation with US. Radiology. 2003;226(1):95-100. 57. Lee J, Jeong Y, Hwang J, et al. Graded compression sonography with adjuvant use of a posterior manual compression technique in the sonographic diagnosis of acute appendicitis. AJR Am J Roentgenol. 2002;178(4):863-868. 58. Borushok KF, Jeffrey Jr RB, Laing FC, Townsend RR. Sonographic diagnosis of perforation in patients with acute appendicitis. AJR Am J Roentgenol. 1990;154(2):275-278. 59. Agha FP, Ghahremani GG, Panella JS, Kaufman MW. Appendicitis as the initial manifestation of Crohn’s disease: radiologic features and prognosis. AJR Am J Roentgenol. 1987;149(3):515-518. 60. Roth T, Zimmer G, Tschantz P. Maladie de Crohn appendiculaire. Ann Chir. 2000;125(7):665-667. 61. Higgins MJ, Walsh M, Kennedy SM, et al. Granulomatous appendicitis revisited: report of a case. Dig Surg. 2001;18(3):245-248. 62. Chou Y, Chiou H, Tiu C, et al. Sonography of acute right side colonic diverticulitis. Am J Surg. 2001;181(2):122-127. 63. O’Malley M, Wilson S. US of gastrointestinal tract abnormalities with CT correlation. Radiographics. 2003;23(1):59-72. 64. Teefey SA, Montana MA, Goldfogel GA, Shuman WP. Sonographic diagnosis of neutropenic typhlitis. AJR Am J Roentgenol. 1987;149(4):731-733. 65. Frager DH, Frager JD, Brandt LJ, et al. Gastrointestinal complications of AIDS: radiologic features. Radiology. 1986;158(3):597-603. 66. Balthazar EJ, Megibow AJ, Fazzini E, et al. Cytomegalovirus colitis in AIDS: radiographic findings in 11 patients. Radiology. 1985;155(3):585-589. 67. Teixidor HS, Honig CL, Norsoph E, et al. Cytomegalovirus infection of the alimentary canal: radiologic findings with pathologic correlation. Radiology. 1987;163(2):317-323. 68. Puylaert JB. Mesenteric adenitis and acute terminal ileitis: US evaluation using graded compression. Radiology. 1986;161(3):691-695. 69. Puylaert JB, Lalisang RI, van der Werf SD, Doornbos L. Campylobacter ileocolitis mimicking acute appendicitis: differentiation with gradedcompression US. Radiology. 1988;166(3):737-740. 70. Puylaert JB. Right-sided segmental infarction of the omentum: clinical, US, and CT findings. Radiology. 1992;185(1):169-172. 71. Painter NS, Burkitt DP. Diverticular disease of the colon, a 20th century problem. Clin Gastroenterol. 1975;4(1):3-21. 72. Parks TG. Natural history of diverticular disease of the colon. A review of 521 cases. Br Med J. 1969;4(5684):639-642. 73. Fleischner F, Ming S. Revised concepts on diverticular disease of the colon. Radiology. 1965;84(4):599-609. 74. Wilson SR, Toi A. The value of sonography in the diagnosis of acute diverticulitis of the colon. AJR Am J Roentgenol. 1990;154(6): 1199-1202. 75. Parulekar SG. Sonography of colonic diverticulitis. J Ultrasound Med. 1985;4(12):659-666. 76. Derchi LE, Reggiani L, Rebaudi F, Bruschetta M. Appendices epiploicae of the large bowel. Sonographic appearance and differentiation from peritoneal seeding. J Ultrasound Med. 1988;7(1):11-14. 77. Meiser G, Meissner K. [Sonographic differential diagnosis of intestinal obstruction—results of a prospective study of 48 patients]. Ultraschall Med. 1985;6(1):39-45. 78. Tennenhouse JE, Wilson SR. Sonographic detection of a small-bowel bezoar. J Ultrasound Med. 1990;9(10):603-605. 79. Siewert B, Raptopoulos V. CT of the acute abdomen: findings and impact on diagnosis and treatment. AJR Am J Roentgenol. 1994;163(6):1317-1324. 80. Balthazar EJ. George W. Holmes Lecture. CT of small-bowel obstruction. AJR Am J Roentgenol. 1994;162(2):255-261. 81. Lee DH, Lim JH, Ko YT. Afferent loop syndrome: sonographic findings in seven cases. AJR Am J Roentgenol. 1991;157(1):41-43. 82. Parienty RA, Lepreux JF, Gruson B. Sonographic and CT features of ileocolic intussusception. AJR Am J Roentgenol. 1981;136(3):608-610. 83. Weissberg D, Scheible W, Leopold G. Ultrasonographic appearance of adult intussusception. Radiology. 1977;124(3):791-792. 84. Alessi V, Salerno G. The “Hay-fork” sign in the ultrasonographic diagnosis of intussusception. Gastrointest Radiol. 1985;10(1):177-179. 85. Gaines PA, Saunders AJS, Drake D. Midgut malrotation diagnosed by ultrasound. Clin Radiol. 1987;38(1):51-53.

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86. Totten MA, Gregg JA, Fremont-Smith P, Legg M. Clinical and pathological spectrum of antibiotic-associated colitis. Am J Gastroenterol. 1978;69(3 Pt 1):311-319. 87. Downey DB, Wilson SR. Pseudomembranous colitis: sonographic features. Radiology. 1991;180(1):61-64. 88. Bolondi L, Ferrentino M, Trevisani F, et al. Sonographic appearance of pseudomembranous colitis. J Ultrasound Med. 1985;4(9):489-492. 89. Vernacchia FS, Jeffrey RB, Laing FC, Wing VW. Sonographic recognition of pneumatosis intestinalis. AJR Am J Roentgenol. 1985;145(1):51-52. 90. Sigel B, Machi J, Ramos JR, et al. Ultrasonic features of pneumatosis intestinalis. J Clin Ultrasound. 1985;13(9):675-678. 91. Cotrin RS, Kumar V, Collins T, editors. Robbins pathologic basis of disease. 6th ed. Philadelphia: Saunders; 1999. pp. 1583-1584. 92. Young R, Gilks C, Scully R. Mucinous tumors of the appendix associated with mucinous tumors of the ovary and pseudomyxoma peritonei. Am J Surg Pathol. 1991;15(5):415-429. 93. Dietrich CF, Brunner V, Seifert H, et al. [Intestinal B-mode sonography in patients with endemic sprue. Intestinal sonography in endemic sprue]. Ultraschall Med. 1999;20(6):242-247. 94. Rettenbacher T, Hollerweger A, Macheiner P, et al. Adult celiac disease: US signs. Radiology. 1999;211(2):389-394. 95. Pickhardt PJ, Yagan N, Siegel MJ, et al. Cystic fibrosis: CT findings of colonic disease. Radiology. 1998;206(3):725-730. 96. Haber HP, Benda N, Fitzke G, et al. Colonic wall thickness measured by ultrasound: striking differences in patients with cystic fibrosis versus healthy controls. Gut. 1997;40(3):406-411. 97. Connett G, Lucas J, Atchley J, et al. Colonic wall thickening is related to age and not dose of high strength pancreatin microspheres in children with cystic fibrosis. Eur J Gastroenterol Hepatol. 1999;11(2):181-184. 98. Welkon CJ, Long SS, Thompson Jr CM, Gilligan PH. Clostridium difficile in patients with cystic fibrosis. Am J Dis Child. 1985;139(8):805-808. 99. Shorvon PJ, Lees WR, Frost RA, Cotton PB. Upper gastrointestinal endoscopic ultrasonography in gastroenterology. Br J Radiol. 1987;60(713):429-438. 100. Strohm WD, Classen M. Benign lesions of the upper GI tract by means of endoscopic ultrasonography. Scand J Gastroenterol Suppl. 1986;21(123): 41-46. 101. Takemoto T, Ito T, Aibe T, Okita K. Endoscopic ultrasonography in the diagnosis of esophageal carcinoma, with particular regard to staging it for operability. Endoscopy. 1986;18(Suppl. 3):22-25. 102. Bolondi L, Casanova P, Caletti GC, et al. Primary gastric lymphoma versus gastric carcinoma: endoscopic US evaluation. Radiology. 1987;165(3):821-826. 103. Hildebrandt U, Feifel G. Preoperative staging of rectal cancer by intrarectal ultrasound. Dis Colon Rectum. 1985;28(1):42-46. 104. Wang KY, Kimmey MB, Nyberg DA, et al. Colorectal neoplasms: accuracy of US in demonstrating the depth of invasion. Radiology. 1987;165(3): 827-829. 105. Yamashita Y, Machi J, Shirouzu K, et al. Evaluation of endorectal ultrasound for the assessment of wall invasion of rectal cancer. Dis Colon Rectum. 1988;31(8):617-623. 106. Berton F, Gola G, Wilson S. Perspective on the role of transrectal and transvaginal sonography of tumors of the rectum and anal canal. AJR Am J Roentgenol. 2008;190(6):1495-1504. 107. Astler V, Coller F. The prognostic significance of direct extension of carcinoma of the colon and rectum. Ann Surg. 1954;139(6):846-852. 108. Spiessl B, Beahrs OH, Hermanek P, et al., editors. TNM atlas: illustrated guide to the TNM/pTNM-classification of malignant tumours. 3rd ed. Berlin: Springer Verlag; 2003. 109. Law P, Bartram C. Anal endosonography: technique and normal anatomy. Gastrointest Radiol. 1989;14(1):349-353. 110. Rifkin MD, Ehrlich SM, Marks G. Staging of rectal carcinoma: prospective comparison of endorectal US and CT. Radiology. 1989;170(2):319-322. 111. Berton F, Gola G, Wilson S. Sonography of benign conditions of the anal canal: an update. AJR Am J Roentgenol. 2007;189(4):765-773. 112. Stewart LK, Wilson SR. Transvaginal sonography of the anal sphincter: reliable, or not? AJR Am J Roentgenol. 1999;173(1):179-185. 113. Sudakoff G, Quiroz F, Foley W. Sonography of anorectal, rectal, and perirectal abnormalities. AJR Am J Roentgenol. 2002;179(1):131-136. 114. Parks AG, Gordon PH, Hardcastle JD. A classification of fistula-in-ano. Br J Surg. 1976;63(1):1-12.

CHAPTER

9

 

The Kidney and Urinary Tract Mitchell Tublin, Deborah Levine, Wendy Thurston, and Stephanie R. Wilson

SUMMARY OF KEY POINTS • Renal ultrasound is the screening modality of choice for the initial evaluation of renal insufficiency. Relevant imaging markers include parenchymal echogenicity, renal length, and collecting system dilatation. • The primary role for ultrasound in the evaluation of renal masses is to differentiate between cystic and solid lesions, although an appropriate differential diagnosis may be given based on clinical history and cyst complexity. • Echogenic renal masses are problematic, and although several discriminatory features have been proposed, renal computed tomography or magnetic resonance imaging is typically employed for larger lesions to

differentiate between renal cell carcinoma and angiomyolipoma. • The role of ultrasound in the evaluation of hematuria continues to evolve. Ultrasound is an effective screening modality for typical “urologic” causes of hematuria (namely, renal calculi) in younger patients. • Focal and diffuse bladder wall thickening at ultrasound is nonspecific and may be caused by a variety of infectious, inflammatory reactions or neoplastic processes. Urine analysis, clinical history, and potentially cystoscopy are typically performed after thickening is identified at sonography.

CHAPTER OUTLINE EMBRYOLOGY Development of the Kidneys and Ureter Development of the Bladder Development of the Urethra ANATOMY Kidney Ureter Bladder SONOGRAPHIC TECHNIQUE Kidney Ureter Bladder and Urethra HYDRONEPHROSIS PITFALLS IN ASSESSMENT OF OBSTRUCTION CONGENITAL ANOMALIES Anomalies Related to Renal Growth Hypoplasia Fetal Lobation Compensatory Hypertrophy Anomalies Related to Ascent of Kidney Ectopia Crossed Renal Ectopia Horseshoe Kidney Anomalies Related to Ureteral Bud Renal Agenesis Supernumerary Kidney Duplex Collecting System and Ureterocele Ureteropelvic Junction Obstruction

310

Congenital Megacalices Congenital Megaureter Anomalies Related to Vascular Development Aberrant Vessels Retrocaval Ureter Anomalies Related to Bladder Development Bladder Agenesis Bladder Duplication Bladder Exstrophy Urachal Anomalies Anomalies Related to Urethral Development: Diverticula GENITOURINARY INFECTIONS Pyelonephritis Acute Pyelonephritis Renal and Perinephric Abscess Pyonephrosis Emphysematous Pyelonephritis Emphysematous Pyelitis Chronic Pyelonephritis Xanthogranulomatous Pyelonephritis Papillary Necrosis Tuberculosis Fungal Infections Candida Albicans Parasitic Infections Schistosomiasis Echinococcal (Hydatid) Disease

Acquired Immunodeficiency Syndrome Cystitis Infectious Cystitis Malacoplakia Emphysematous Cystitis Chronic Cystitis FISTULAS, STONES (CALCULI), AND CALCIFICATION Bladder Fistulas Renal Calculi Ureteral Calculi Bladder Calculi Nephrocalcinosis GENITOURINARY TUMORS Renal Cell Carcinoma Imaging and Treatment Approaches Sonographic Appearance Biopsy and Prognosis Pitfalls in Interpretation Transitional Cell Carcinoma Renal Tumors Ureteral Tumors Bladder Tumors Squamous Cell Carcinoma Adenocarcinoma Oncocytoma Angiomyolipoma Lymphoma Kidney Ureter

CHAPTER 9  The Kidney and Urinary Tract Bladder Leukemia Metastases Kidney Ureter Bladder Urachal Adenocarcinoma Rare Neoplasms Kidney Bladder RENAL CYSTIC DISEASE Cortical Cysts Parapelvic Cysts Medullary Cysts Medullary Sponge Kidney Medullary Cystic Disease Polycystic Kidney Disease Multicystic Dysplastic Kidney Lithium Nephropathy

Multilocular Cystic Nephroma Localized Cystic Disease Neoplasm-Associated Renal Cystic Disease Acquired Cystic Kidney Disease Von Hippel–Lindau Disease Tuberous Sclerosis TRAUMA Renal Injuries Ureteral Injuries Bladder Injuries VASCULAR ABNORMALITIES Renal Vascular Doppler Sonography Renal Artery Occlusion and Infarction Arteriovenous Fistula and Malformation Renal Artery Stenosis Renal Artery Aneurysm Renal Vein Thrombosis Ovarian Vein Thrombosis

T

he prime function of the kidney is excretion of metabolic waste products. The kidneys do this by converting more than 1700 liters of blood per day into 1 liter of highly concentrated urine.1 The kidney is an endocrine organ that secretes many hormones, including erythropoietin, renin, and prostaglandins. The kidneys also function to maintain homeostasis by regulating water-salt and acid-base balance. The renal collecting system, ureters, and urethra function as conduits, and the bladder serves as a reservoir for urinary excretion.

311

MEDICAL GENITOURINARY DISEASES Acute Tubular Necrosis Acute Cortical Necrosis Glomerulonephritis Acute Interstitial Nephritis Diabetes Mellitus Amyloidosis Endometriosis Interstitial Cystitis NEUROGENIC BLADDER BLADDER DIVERTICULA POSTSURGICAL EVALUATION Nephrectomy Urinary Diversion CONCLUSION Acknowledgment

and a dorsal rectum. The bladder develops from the urogenital sinus. Initially, the bladder is continuous with the allantois, which eventually becomes a fibrous cord called the urachus, the adult median umbilical ligament. As the bladder enlarges, the distal portion of the mesonephric ducts is incorporated as connective tissue into the bladder trigone. At the same time, the ureters come to open separately into the bladder.2 In infants and children the bladder is an abdominal organ; it is not until after puberty that it becomes a true pelvic structure2 (Fig. 9.2).

Development of the Urethra

EMBRYOLOGY Development of the Kidneys and Ureter Three sets of kidneys develop in human embryos: the pronephros, mesonephros, and metanephros (definitive or permanent kidney).2 The pronephroi appear early in the fourth embryologic week and are rudimentary and nonfunctioning. The mesonephroi form late in the fourth week and function as interim kidneys until the developing metanephroi begin to function (ninth week). The metanephroi (permanent kidneys) develop from two sources: the ureteric bud and metanephrogenic blastema.2 The ureteric bud forms the ureter, renal pelvis, calices, and collecting ducts, interacting with and penetrating the metanephrogenic blastema. This interaction is necessary to initiate ureteric bud branching and differentiation of nephrons within the blastema (Fig. 9.1). Initially, the permanent kidneys are found in the pelvis. With fetal growth, the kidneys come to lie in the upper retroperitoneum. With ascent, the kidneys rotate medially 90 degrees so that the renal pelvis is directed anteromedially. The kidneys are in their adult location and position by the ninth gestational week. As the kidneys ascend, they derive their blood supply from nearby vessels; adult blood supply is from the abdominal aorta.

Development of the Bladder In the seventh gestational week the urorectal septum fuses with the cloacal membrane, dividing it into a ventral urogenital sinus

The epithelium of most of the male urethra and the entire female urethra is derived from the endoderm of the urogenital sinus. The urethral connective tissue and smooth muscle form from adjacent splanchnic mesenchyme.2

ANATOMY Kidney In the adult, each kidney measures approximately 11 cm long, 2.5 cm thick, and 5 cm wide and weighs 120 to 170 grams.3 Emamian et al.4 demonstrated that the parenchymal volume of the right kidney is smaller than that of the left kidney, possibly because of a relatively larger potential space for left renal growth (growth of right kidney inhibited by liver) or relatively increased left renal blood flow (left renal artery typically shorter than right renal artery). Renal length correlates best with body height, and renal size decreases with advancing age because of parenchymal reduction. The left kidney usually lies 1 to 2 cm higher than the right kidney.3 The kidneys are mobile and will move depending on body position. In the supine position, the superior pole of the left kidney is at the level of the 12th thoracic vertebra, and the inferior pole is at the level of the third lumbar vertebra. The normal adult kidney is bean shaped with a smooth, convex contour anteriorly, posteriorly, and laterally. Medially,

Mesonephric duct Remnant of pronephros

Metanephric mass of mesoderm

B

Ureteric bud Mesonephros Developing liver

Pelvis

C

Nephrogenic cord

Major calix Ureter

Minor calix

Cloaca Pelvis

Mesonephric duct

D Metanephric diverticulum or ureteric bud

A

Mesenchymal cell cluster

Metanephric mass of intermedate mesoderm

Straight collecting tubule

Primordium of metanephros

Metanephric mass of mesoderm

E

Groove between lobes Lobe

Arched collecting tubule

FIG. 9.1  Embryology of the Kidney and Ureter.  (A) Lateral view of a 5-week embryo shows the three embryologic kidneys. (B)-(E) Successive stages of development of the ureteric bud (fifth to eighth week) into the ureter, pelvis, calices, and collecting tubules. (With permission from The urogenital system. In: Moore KL, Persaud TVN, editors. The developing human: clinically oriented embryology. 5th ed. Philadelphia: Saunders; 1993. pp. 265-303.2) Allantois

Primitive urigenital sinus Mesonephros

Mesonephros

Ureteric bud Urorectal septum

Mesonephric duct

Hindgut

B

Cloacal membrane Vesical part Pelvic part

C

Genital tubercle

Urogenital membrane

Phallic part

Mesonephros

Urogenital sinus

A

Metanephros

D

Mesonephros

E

Urachus

Rectum

Ureter

Urinary bladder

Mesonephric duct

Ureter

Pelvic portion of urogenital sinus

Uterine tube

F Urinary bladder

Kidney

Kidney

Testis

Ovary

Ureter

Uterus Clitoris

G

Mesonephros Metanephros

Metanephros

FIG. 9.2  Embryology of the Bladder and Urethra.  Diagrams show division of the cloaca into the urogenital sinus and rectum; absorption of the mesonephric ducts; development of the urinary bladder, urethra, and urachus; and change in location of the ureters. (A) and (B) Five-week embryo. (C)-(H) Seven- to 12-week embryo. (A, C, E, and G, female; B, D, F, and H, male.) (With permission from The urogenital system. In: Moore KL, Persaud TVN, editors. The developing human: clinically oriented embryology. 5th ed. Philadelphia: Saunders; 1993. pp. 265-303.2)

Gonad

Ductus deferens

Vagina Penis Spongy urethra

H

CHAPTER 9  The Kidney and Urinary Tract the surface is concave; the medial surface is known as the renal hilum. The renal hilum is continuous with a central cavity called the renal sinus. Within the renal sinus are the major branches of the renal artery, major tributaries of the renal vein, and the collecting system.3 The remainder of the renal sinus is packed with fat. The collecting system (renal pelvis) lies posterior to the renal vessels in the renal hilum (Fig. 9.3). Renal parenchyma is composed of cortex and medullary pyramids. The renal medullary pyramids are hypoechoic relative to the renal cortex and can be identified in most normal adults (Fig. 9.4). Normal renal cortex is typically less echogenic than adjacent liver and spleen. Platt et al.5 found that 72% of 153 patients with renal cortical echogenicity equal to that of the liver had normal renal function. Greater renal echogenicity than liver echogenicity showed a specificity and a positive predictive value for abnormal renal function of 96% and 67%, respectively. However, the sensitivity of this ultrasound criterion was poor (20%). During normal development, two parenchymal masses called ranunculi partially fuse. Parenchymal junctional defects occur at the site of fusion and must not be confused with pathologic processes (e.g., renal scar, angiomyolipoma). The junctional parenchymal defect is most often located anteriorly and superiorly, typically at the junction of the upper and middle thirds of the kidney, and can be traced medially and inferiorly into the renal sinus. Usually, it is oriented more horizontally than vertically and therefore it is best appreciated on sagittal scans6 (Fig. 9.5). Junctional cortical defects are more often shown within the right kidney, although left junctional cortical defects may be detected with favorable acoustic windows. A hypertrophied column of Bertin (HCB) is a normal variant; it represents unresorbed polar parenchyma from one or both of the two subkidneys that fuse to form the normal kidney.7 Sonographic features that may aid in the demarcation of HCB include indentation of the renal sinus laterally and a border formed by the junctional parenchymal defect. Hypertrophied columns are usually located at the junction of the upper and middle thirds of the kidney and contain renal cortex that is continuous with the adjacent renal cortex of the same subkidney.

A

313

FIG. 9.3  Anatomy of the Kidney, Ureter, and Bladder.

B

FIG. 9.4  Normal Kidney.  (A) Sagittal and (B) transverse sonograms of normal anatomy with corticomedullary differentiation show relatively hypoechoic medullary pyramids, with cortex slightly less echogenic than the liver and spleen.

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Bladder

FIG. 9.5  Anterior Junction Line.  Sagittal sonogram demonstrates an echogenic line that extends from the renal sinus to perinephric fat. The defect is typically located at the junction of the upper and middle thirds of the kidney, as in this example.

Sonographic Criteria for Hypertrophied Column of Bertin Indentation of renal sinus laterally Bordered by junctional parenchymal defect Location at junction of upper and middle thirds Continuous with adjacent renal cortex Similar color flow to surrounding parenchyma Contains renal pyramids Less than 3 cm in size

Columns contain renal pyramids and usually measure less than 3 cm7,8 (Fig. 9.6). The echogenicity of HCB and adjacent renal cortex depend on the scan plane. Alterations in tissue orientation produce different acoustic reflectivity.7 The echoes of the HCB are brighter than those of adjacent renal cortex when seen en face7 (Fig. 9.6). It may be difficult to differentiate a small, hypovascular tumor from an HCB; however, demonstration of arcuate arteries by color Doppler ultrasound indicates an HCB rather than a tumor. Occasionally, contrast-enhanced computed tomography (CT) may be necessary to differentiate between an HCB and a non–border-deforming renal lesion. The kidney has a thin, fibrous capsule. The capsule is surrounded by perirenal fat. Perirenal fat is encased anteriorly by Gerota fascia and posteriorly by Zuckerkandl fascia.9 The right perirenal space opens superiorly at the bare area of the liver, and both perirenal spaces communicate with the pelvic peritoneal space.10 Right and left perirenal spaces communicate with each other across the midline at the level of the third to fifth lumbar vertebrae.10

The bladder is positioned in the pelvis, inferior and anterior to the peritoneal cavity and posterior to the pubic bones.3 Superiorly, the peritoneum is reflected over the anterior aspect of the bladder. Within the bladder, the ureteric and urethral orifices demarcate an area known as the trigone; the urethral orifice also marks the bladder neck. The bladder neck and trigone remain constant in shape and position; however, the remainder of the bladder will change shape and position depending on the volume of urine within it. Deep to the peritoneum covering the bladder is a loose, connective tissue layer of subserosa that forms the adventitial layer of the bladder wall. Adjacent to the adventitia are three muscle layers: the outer (longitudinal), middle (circular), and internal longitudinal layers. Adjacent to the muscle, the innermost layer of the bladder is composed of mucosa. The bladder wall should be smooth and of uniform thickness. The wall thickness depends on the degree of bladder distention.

SONOGRAPHIC TECHNIQUE The ability to visualize organs of the genitourinary tract by ultrasound depends on the patient’s body habitus, operator experience, and scanner platform. High-frequency probes should be used for patients with a favorable body habitus. Harmonic imaging is often useful for difficult-to-scan patients (e.g., obese patients). Compound imaging and speckle reduction may increase lesion conspicuity and decrease artifacts.

Kidney The kidneys should be assessed in the transverse and coronal plane. Optimal patient positioning varies; supine and lateral decubitus positions often suffice, although oblique and occasionally prone positioning may be necessary (e.g., obese patients). Usually, a combination of subcostal and intercostal approaches is required to evaluate the kidneys fully; the upper pole of the left kidney may be particularly difficult to image without a combination of approaches. When the collecting system is dilated, additional images should be taken to assess for the level of obstruction, any obstructing lesion, and appearance of the kidneys after voiding (see “Hydronephrosis”).

Ureter The proximal ureter is best visualized using a coronal oblique view with the kidney as an acoustic window. The ureter is followed to the bladder, maintaining the same approach. A nondilated ureter may be impossible to visualize because of overlying bowel gas. Transverse scanning of the retroperitoneum often demonstrates a dilated ureter, which can then be followed caudally with both transverse and sagittal imaging. In women, a dilated distal ureter is well seen with transvaginal scanning.

Ureter

Bladder and Urethra

The ureter is a long (30-34 cm), mucosal-lined conduit that delivers urine from the renal pelvis to the bladder. Each ureter varies in diameter from 2 to 8 mm.3 As it enters the pelvis, the ureter passes anterior to the common/external iliac artery. The ureter has an oblique course through the bladder wall (see Fig. 9.3).

The bladder is best evaluated when it is moderately filled; an overfilled bladder causes patient discomfort. The bladder should be scanned in the transverse and sagittal planes. To better visualize the bladder wall in women, transvaginal scanning may be helpful. If the nature of a large, fluid-filled mass in the pelvis is uncertain,

CHAPTER 9  The Kidney and Urinary Tract

A

B

C

E

315

D

F

FIG. 9.6  Hypertrophied Column of Bertin. (A) Sagittal and (B) transverse sonograms show classic appearance of the column of Bertin. (C) Medullary pyramids can be seen within the hypertrophied column of Bertin. (D) Echogenicity of the column may vary based on orientation. (E) Transverse sonogram and (F) corresponding power Doppler image confirm a hypertrophied column.

voiding or insertion of a Foley catheter will clarify the location and appearance of the bladder relative to the fluid-filled mass. Incomplete bladder emptying can be due to prostate enlargement, neurogenic bladder, or pelvic floor weakness. Bladder stones and infection are important complications. Initial assessment includes assessment of the kidneys and ureter for dilatation, as well as calculation of both a prevoid and postvoid residual. We typically calculate bladder volume by taking the three

orthogonal measurements and multiplying by .6 (this is different from most organs, which multiply by .52). This slightly larger value is because the shape of the bladder is more of a cuboidal shape than a prolate ellipse. The urethra in a woman can be scanned with transvaginal, transperineal, or translabial sonography11 (Fig. 9.7). The posterior or the prostatic urethra in men is best visualized with transrectal probes (Fig. 9.8).

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HYDRONEPHROSIS The term hydronephrosis refers to dilatation of the collecting system. Obstruction is often present, but this is not always the case. There are many causes of a dilated renal collecting system, and ultrasound is the initial imaging modality of choice for the majority of these assessments (except as discussed in the previous section where noncontrast-enhanced CT may be used in the initial assessment of acute renal colic). Initial sonographic evaluation should include an assessment of the degree of dilatation, appearance of surrounding renal parenchyma, assessment for level of obstruction and any obstructing lesion. Numerous grading systems for the assessment of the degree of hydronephrosis have been proposed following Ellenbogen and colleagues’ original article on the topic.12 None has been readily adopted, however, and most radiologists continue to use descriptive terminology such as mild, moderate, and severe.13

FIG. 9.7  Translabial Ultrasound of Female Urethra.  Sagittal sonogram shows the tubular hypoechoic urethra extending from the bladder to the skin surface.

A

A practical pearl for the ultrasound evaluation of hydronephrosis is to assess the degree of dilatation before and after bladder voiding. Hydronephrosis that persists after voiding suggests an anatomic obstruction. If collecting system dilatation diminishes postvoiding, then one might consider nonobstructive pelvicaliectasis (i.e., vesicoureteral reflux). Most obstructing lesions are located within the pelvis (fibroids, prostatic hypertrophy, ovarian tumor, bladder tumor) and thus are obvious on sonographic evaluation. When the pelvis is normal, the length of the ureter should be assessed for dilatation and/or obstructing lesion. In pregnancy, it is helpful to have the patient lie in the decubitus position with the symptomatic side up to allow for the weight of the uterus to move off of the ureter. Over time the obstructed kidney will initially become enlarged. Later, renal damage may occur with parenchymal atrophy and blunting of calices. In pregnancy, the urinary tract frequently is dilated. Smooth muscle relaxation occurs as a result of elevated hormone levels. Mass effect on the ureter may be caused by the enlarged uterus. Because of the location of the ureters, the right ureter is frequently more dilated than the left ureter. Physiologic dilatation of the urinary tract in pregnancy is suggested when the distal ureters taper at the sacral promontory. Pregnant patients are also at increased risk for urinary tract infections (UTIs), which can complicate the assessment. In addition, stone disease can occur and this needs to be distinguished from the physiologic dilatation associated with pregnancy. In acute hydronephrosis of pregnancy, patients may present with severe flank or lower abdominal pain radiating to the groin due to ureteric obstruction. The obstruction usually occurs at the level of the pelvic brim. Symptoms may improve with change in posture with the patient in the lateral decubitus position, symptomatic side up. In extreme cases, ureteral stunting may be required. When severe overdistention syndrome occurs, rupture of the urinary tract may occur, which can be identified as fluid collection around the periphery of the kidney by ultrasound.

B

FIG. 9.8  Transrectal Ultrasound of Male Urethra.  (A) Sagittal and (B) transverse sonograms show the urethra with calcifications in the urethral glands (arrows) surrounded by the echo-poor muscle of the internal urethral sphincter. B, Bladder; arrowhead, ejaculatory duct; S, seminal vesicles. (Courtesy of Ants Toi, MD, Toronto Hospital.)

CHAPTER 9  The Kidney and Urinary Tract

317

Causes of Hydronephrosis Genitourinary Obstruction

Comments

Genitourinary Obstruction

Comments

Renal/ureteral stone

Look for stone in common sites of obstruction: ureterovesical junction and ureteropelvic junction Hematuria

Aneurysm

Should be obvious on Doppler assessment of vessels Mass typically seen in pelvis Ureter dilated to pelvic brim

Transitional cell carcinoma Sloughed papilla Blood clot Posterior urethral valves Ureterocele

Ureteropelvic junction obstruction Ureteral stricture (prior infection, surgery, radiation) Neurogenic bladder Extrinsic Obstruction Retrocaval ureter Prostatic hypertrophy Tumor (fibroid, ovarian carcinoma, lymphoma) Lymphadenopathy Retroperitoneal fibrosis

Hematuria Bilateral, pediatric diagnosis May be orthotopic or heterotopic If heterotopic, look for renal duplication abnormality Extrarenal pelvis may be dilated out of proportion to calices History aids in diagnosis

Endometriosis Pregnancy Nonobstructive Vesicoureteral reflux Congenital megacalices

Check for postvoid residual

Prior obstruction

May need CT for diagnosis Enlarged prostate impinges on bladder Abnormal mass seen in pelvis Abnormal mass seen in pelvis Mass encasing the aorta CT may be needed for diagnosis

Infection

PITFALLS IN ASSESSMENT OF OBSTRUCTION Although obstruction typically causes dilatation, early in the process the renal collecting system may not dilate. In cases of renal failure, a poorly functioning kidney may not make sufficient urine to demonstrate dilatation. In addition, in cases of severe obstruction, pelvocaliceal rupture may lead to decompression of the collecting system with a perinephric hematoma/urinoma. Hydronephrosis (a condition in which dilated calices communicate with central collecting system) should be distinguished from multiple parapelvic cysts (which do not communicate).

CONGENITAL ANOMALIES Anomalies Related to Renal Growth Hypoplasia Renal hypoplasia is a renal parenchymal anomaly in which there are too few nephrons. Renal function depends on the mass of the kidney. True hypoplasia is a rare anomaly. Many patients

High flow states (diabetes insipidus, psychogenic polydipsia) Distended bladder

Cortical scarring, typically in upper poles May be unilateral or bilateral If associated with congenital megaureter, both dilated ureter and calices will be present May need contrastenhanced CT for diagnosis Prior severe dilatation may not return to normal Signs and symptoms of infection Typically mild dilatation

Returns to normal after bladder emptying

with unilateral hypoplasia are asymptomatic; the condition is typically an incidental finding. Patients with bilateral hypoplasia often have renal insufficiency. Hypoplasia is believed to result from the ureteral bud making contact with the most caudal portion of the metanephrogenic blastema. This can occur with delayed development of the ureteric bud or from delayed contact of the bud with the cranially migrating blastema. Hypoplasia is established when fewer but otherwise histologically normal renal lobules are identified.14 At ultrasound, the kidney is small but otherwise appears normal.

Fetal Lobation Fetal lobation is usually present until 4 or 5 years of age; however, persistent lobation is seen in 51% of adult kidneys.15 There is infolding of the cortex without loss of cortical parenchyma. At ultrasound, sharp clefts are shown overlying the columns of Bertin.16 Compensatory Hypertrophy Compensatory hypertrophy may be diffuse or focal. It occurs when existing healthy nephrons enlarge to allow healthy renal parenchyma to perform more work. The diffuse form is seen

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with contralateral nephrectomy, renal agenesis, renal hypoplasia, renal atrophy, and renal dysplasia. Diffuse compensatory hypertrophy is suggested at ultrasound when an enlarged but otherwise normal-appearing kidney is identified. The focal form is seen when residual islands of normal tissue enlarge in an otherwise diseased kidney; focal compensatory hypertrophy may be particularly prominent in the setting of reflux nephropathy. Large areas of nodular but normal renal tissue identified between scars may mimic a solid renal mass.5

Anomalies Related to Ascent of Kidney Ectopia Failure of the kidney to ascend during embryologic development results in a pelvic kidney; prevalence is 1 in 724 pediatric autopsies.16 These kidneys are often small and abnormally rotated. Fifty percent of pelvic kidneys have decreased function.16 The ureters are often short; poor drainage and collecting system dilatation predispose pelvic kidneys to infection and stone formation. The blood supply is often complex; multiple arteries may be derived from regional arteries (typically, internal iliac or common iliac). If the kidney ascends too high, it may pass through the foramen of Bochdalek and become a true thoracic kidney; this is usually of no clinical significance. A search for a pelvic kidney should be performed if the kidney is not identified within renal fossae (Fig. 9.9). If the kidney has ascended too high, ultrasound is helpful to determine if the diaphragm is intact. Crossed Renal Ectopia In crossed renal ectopia, both kidneys are found on the same side. In 85% to 90% of cases, the ectopic kidney will be fused to the other kidney (crossed-fused ectopia). The upper pole of the ectopic kidney is usually fused to the lower pole of the other kidney, although fusion may occur anywhere. The incidence is 1 in 1000 to 1 in 1500 at autopsy.15 Fusion of metanephrogenic blastema does not allow proper rotation or ascent; thus both kidneys are more caudally located, although the ureterovesical

junctions (UVJs) are located normally. At sonography, both kidneys are on the same side and are typically fused (Fig. 9.10). In patients with renal colic, knowing that the UVJs are in the normal location is particularly important, since bilateral ureters need to be assessed.

Horseshoe Kidney The incidence of horseshoe kidneys in the general population is 0.01% to 0.25%. Horseshoe kidneys occur when metanephrogenic blastema fuse prior to ascent; fusion is usually at the lower poles (95%). Typically, the isthmus is composed of functioning renal tissue, although rarely it is made up of fibrous tissue. The horseshoe kidney sits anterior to the abdominal great vessels and derives its blood supply from the aorta and other regional vessels, such as inferior mesenteric, common iliac, internal iliac, and external iliac arteries. Abnormal rotation of renal pelves often results in ureteropelvic junction (UPJ) obstruction; the horseshoe kidney is thus predisposed to infection and stone formation. Additional associated anomalies include vesicoureteral reflux, collecting system duplication, renal dysplasia, retrocaval ureter, supernumerary kidney, anorectal malformation, esophageal atresia, rectovaginal fistula, omphalocele, and cardiovascular and skeletal abnormalities. At sonography, horseshoe kidneys are usually lower than normal and the lower poles project medially. Transverse imaging of the retroperitoneum will demonstrate the renal isthmus crossing the midline anterior to abdominal great vessels (Fig. 9.11). Hydronephrosis (pyelocaliectasis) and collecting system calculi may be evident.

Anomalies Related to Ureteral Bud Renal Agenesis Renal agenesis may be unilateral or bilateral. Bilateral renal agenesis is a rare anomaly that is incompatible with life. The prevalence rate of bilateral agenesis at autopsies is 0.04%. The condition has a 3 : 1 male predominance.15 Unilateral renal

*

FIG. 9.9  Pelvic Kidney.  Transverse sonogram demonstrates a left pelvic kidney posterior to the uterus (*).

FIG. 9.10  Cross-Fused Ectopia.  Sagittal sonogram demonstrates two kidneys fused to each other.

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319

Horseshoe kidney

RK

LK

A

B

FIG. 9.11  Horseshoe Kidney.  (A) Transverse sonogram shows the isthmus crossing anterior to the retroperitoneal great vessels, with the renal parenchyma of each limb of the horseshoe draping over the spine. (B) Confirmatory contrast-enhanced CT examination. LK, Left kidney; RK, right kidney.

agenesis is usually an incidental finding; the contralateral kidney of these patients may be quite large secondary to compensatory hypertrophy. Renal agenesis occurs when there is (1) absence of the metanephrogenic blastema, (2) absence of ureteral bud development, or (3) absence of interaction and penetration of the ureteral bud with the metanephrogenic blastema. Renal agenesis is associated with genital tract anomalies, which are often cystic pelvic masses in both men and women. Other associated anomalies include skeletal abnormalities, anorectal malformations, and cryptorchidism. At ultrasound, although the kidney is absent, a normal adrenal gland is usually found. The adrenal gland will be absent in 8% to 17% of patients with renal agenesis.16 It may be difficult to differentiate between renal agenesis and a small, hypoplastic or dysplastic kidney. With all these conditions, the contralateral kidney will be enlarged as a result of compensatory hypertrophy. Usually, the colon falls into the empty renal bed. Care should be taken not to confuse a loop of gut with a normal kidney.

Supernumerary Kidney Supernumerary kidney is an exceedingly rare anomaly. The supernumerary kidney is usually smaller than normal and can be found above, below, in front of, or behind the normal kidney. The supernumerary kidney often has only a few calices and a single infundibulum. The formation of a supernumerary kidney is likely caused by the same mechanism that gives rise to a duplex collecting system.15 Two ureteric buds reach the metanephrogenic blastema, which then divides, or alternatively, there are initially two blastema. On sonography, an extra kidney will be found. Duplex Collecting System and Ureterocele Duplex collecting system is the most common congenital anomaly of the urinary tract, with an incidence of 0.5% to 10% of live births.15 The degree of duplication is variable. Duplication is complete when there are two separate collecting systems and two separate ureters, each with their own ureteral orifice. Duplication is incomplete when the ureters join and enter the bladder through a single ureteral orifice. Ureteropelvic duplication arises

when two ureteral buds form and join with the metanephrogenic blastema or when there is division of a single ureteral bud early in embryogenesis. Normally during embryologic development, the ureteral orifice migrates superiorly and laterally to become part of the bladder trigone. With complete duplication, the ureter from the lower pole of the kidney migrates to assume its normal location, whereas the ureter draining the superior pole of the kidney migrates abnormally to a more medial and inferior ureteral orifice. Patients have an increased incidence of UPJ obstruction and uterus didelphys.16 In complete duplication, the ureter draining the lower pole has a more perpendicular course through the bladder wall, making it more prone to reflux. The ectopic ureter from the upper pole is prone to obstruction, reflux, or both (Fig. 9.12). Obstruction can result in cystic dilatation of the intramural portion of the ureter, giving rise to a ureterocele. Ureteroceles may be unilateral or bilateral and may occur in normal, duplicated, or ectopic ureters. Ureteroceles may result in ureteral obstruction and give rise to recurrent or persistent UTIs. If large, they may block the contralateral ureteral orifice and the urethral orifice at the bladder neck. Treatment of these symptomatic ureteroceles is surgical. However, most ureteroceles are transient, incidental, and clinically insignificant. At ultrasound, a duplex collecting system is seen as two central echogenic renal sinuses with intervening, bridging renal parenchyma. Unfortunately, this sign is insensitive and is only seen in 17% of duplex kidneys.17 Hydronephrosis of the upper-pole moiety and visualization of two distinct collecting systems and ureters are diagnostic. The bladder should always be carefully evaluated for the presence of a ureterocele. A ureterocele will appear as a round, cystlike structure within the bladder (Fig. 9.13). Occasionally, it may be large enough to occupy the entire bladder and will cause obstruction of the bladder neck. In female patients, transvaginal sonography can be helpful to identify small ureteroceles18 (Fig. 9.14). These ureteroceles may be transient. Madeb et al.19 demonstrated that transvaginal sonography with color Doppler and spectral analysis can provide additional information about flow dynamics, eliminating the need for invasive procedures.

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A

B

FIG. 9.12  Duplex Collecting System.  (A) Sagittal sonogram shows an upper-pole cystic mass. Note collecting system dilatation and cortical thinning. (B) Delayed intravenous urogram shows duplicated left collecting system and dilated upper-pole moiety.

A

C

B

FIG. 9.13  Duplex Collecting System.  (A) Sagittal sonogram shows dilatation of the lower-pole moiety, likely related to reflux. (B) Sagittal sonogram shows central parenchyma separating the upper-pole and lower-pole moieties. There is moderate dilatation of both moieties. (C) Sagittal sonogram of the bladder and distal ureter of the patient in B. Note dilatation of the ureter from the upper-pole moiety and a large ureterocele.

CHAPTER 9  The Kidney and Urinary Tract Ureteropelvic Junction Obstruction UPJ obstruction is a common anomaly with a 2 : 1 male predominance. The left kidney is affected twice as frequently as the right kidney. UPJ obstruction is bilateral in 10% to 30% of cases.20 Most adult patients present with chronic, vague, back or flank pain. Symptomatic patients and those with complications, including superimposed infection, stones, or impaired renal function, should be treated. Patients have an increased incidence of contralateral multicystic dysplastic kidney and renal agenesis. Most idiopathic UPJ obstructions are thought to be functional rather than anatomic.20 Histologic evaluation of affected specimens has demonstrated excessive collagen between muscle bundles, deficient or absent muscle, and excessive longitudinal muscle.20 Occasionally, intrinsic valves, true luminal stenosis, and aberrant arteries are the cause of obstruction. At ultrasound, hydronephrosis is present

321

to the level of the UPJ (Fig. 9.15). Marked ballooning of the renal pelvis is often shown, and if long-standing, there will be associated renal parenchymal atrophy. The caliber of the ureter, on the other hand, is normal. Careful evaluation of the contralateral kidney should be performed to exclude associated anomalies.

Congenital Megacalices Congenital megacalices refer to typically unilateral, nonobstructive enlargement of the calices. It is nonprogressive; overlying parenchyma and renal function are maintained. Infection and stone formation are increased because of caliceal enlargement. The exact pathogenesis is speculative; the most common association is with primary megaureter.21 At ultrasound, numerous enlarged clubbed calices are shown. Papillary impressions are absent, and cortical thickness is maintained. Congenital Megaureter Megaureter (congenital megaureter, megaloureter) results in functional ureteric obstruction. The most distal segment of ureter is aperistaltic: focal ureteral lack of peristalsis results in a wide spectrum of findings, from insignificant distal ureterectasis to progressive hydronephrosis/hydroureter. As with UPJ obstructions, men are affected more often, and the left ureter is typically involved.20 Bilateral involvement has been demonstrated in 8% to 50% of patients. The classic finding at ultrasound is fusiform dilatation of the distal third of the ureter (Fig. 9.16). Depending on the severity, associated pyelocaliectasis may or may not be present. Calculi may form just proximal to the adynamic segment.

Anomalies Related to Vascular Development FIG. 9.14  Small Bilateral Ureteroceles.  Transverse transvaginal sonogram demonstrates two small cystic structures related to the bladder wall. With the probe in the vagina, the bladder trigone and the ureteric orifices are shown in the near field of the transducer.

A

Aberrant Vessels As it ascends during embryologic development, the kidney derives its blood supply from successively higher levels of the aorta.

B

FIG. 9.15  Ureteropelvic Junction Obstruction.  (A) Sagittal and (B) transverse sonograms demonstrate marked ballooning of the renal pelvis with associated proximal caliectasis.

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A

B

FIG. 9.16  Congenital Megaureter.  (A) Sagittal sonogram shows marked dilatation of the distal ureter up to the ureterovesical junction. (B) Sagittal sonogram shows moderate midregion ureterectasis.

Aberrant renal arteries will be present if the vascular supply from the lower levels of the aorta persists. Aberrant vessels can compress the ureter anywhere along its course. Color Doppler ultrasound may be useful to identify obstructing vessels crossing at the UPJ.

Retrocaval Ureter Retrocaval ureter is a rare but well-recognized congenital anomaly with a 3 : 1 male predominance. Most patients present with pain in the second to fourth decade of life. Normally, the infrarenal inferior vena cava (IVC) develops from the supracardinal vein; if it develops from the subcardinal vein, the ureter will pass posterior to the IVC. The ureter then passes medially and anteriorly between the aorta and IVC to cross the right iliac vessels. It then enters the pelvis and bladder in a normal manner. Sonography shows collecting system and proximal ureteral dilatation. In easy-to-scan patients the compressed retrocaval ureter may be identified.

Anomalies Related to Bladder Development Bladder Agenesis Bladder agenesis is a rare anomaly. Most infants with bladder agenesis are stillborn; virtually all surviving infants are female.22 Many associated anomalies are often present. At ultrasound, the bladder is absent. Bladder Duplication Bladder duplication is divided into three types, as follows16: Type 1: A complete or incomplete peritoneal fold separates the two bladders. Type 2: An internal septum divides the bladder. The septum may be complete or incomplete and may be oriented in a sagittal or coronal plane. There may be multiple septa.

Type 3: A transverse band of muscle divides the bladder into two unequal cavities.

Bladder Exstrophy Bladder exstrophy occurs in 1 in 30,000 live births, with a 2 : 1 male predominance.16 Failure in development of the mesoderm below the umbilicus leads to absence of the lower abdominal and anterior bladder wall. There is a high incidence of associated musculoskeletal, gastrointestinal, and genital tract anomalies. These patients have an increased (200-fold) incidence of bladder carcinoma (adenocarcinoma in 90%).16 Urachal Anomalies Normally, the urachus closes in the last half of fetal life.16 The four types of congenital urachal anomalies, in order of frequency, are as follows16,23,24 (Fig. 9.17): 1. Patent urachus (50%) 2. Urachal cyst (30%) 3. Urachal sinus (15%) 4. Urachal diverticulum (5%) Urachal anomalies have a 2 : 1 predominance in males. A patent urachus is usually associated with urethral obstruction and serves as a protective mechanism to allow normal fetal development. A urachal cyst forms if the urachus closes at the umbilical and bladder ends but remains patent in between. The cyst is usually situated in the lower third of the urachus. There is an increased incidence of adenocarcinoma. At ultrasound, a midline cyst with or without internal echoes is seen superior to the bladder. A urachal sinus forms when the urachus closes at the bladder end but remains patent at the umbilicus. A urachal diverticulum forms if the urachus closes at the umbilical end but remains patent at the bladder. Urachal diverticula are usually incidentally found. There is an increased incidence of carcinoma and stone formation.

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Anomalies Related to Urethral Development: Diverticula The majority of urethral diverticula are acquired secondary to injury or infection, although congenital diverticula occur rarely. Most urethral diverticula in women form as a result of infection of the periurethral glands; some may be related to childbirth. Most diverticula are found in the midurethra and are bilateral. Often, a fluctuant anterior vaginal mass is felt. Stones may develop because of urinary stasis. Transvaginal or translabial scanning may demonstrate a simple or complex cystic structure communicating with the urethra through a thin neck (Fig. 9.18).

A

B

GENITOURINARY INFECTIONS Pyelonephritis

C

D

FIG. 9.17  Congenital Urachal Anomalies.  (A) Patent urachus extends from the bladder to the umbilicus. (B) Urachal sinus. (C) Urachal diverticulum. (D) Urachal cyst.

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Acute Pyelonephritis Acute pyelonephritis is a tubulointerstitial inflammation of the kidney. Two routes may lead to inflammation: ascending infection (85%; e.g., Escherichia coli) and hematogenous seeding (15%; e.g., Staphylococcus aureus). Women age 15 to 35 years are most often affected25; 2% of pregnant women will develop acute pyelonephritis.26 Most adults present with flank pain and fever and can be diagnosed clinically with the aid of laboratory studies (bacteriuria, pyuria, and leukocytosis). With appropriate antibiotics, both clinical and laboratory findings show rapid improvement. Imaging is necessary only when symptoms and laboratory abnormalities persist: imaging is useful to identify potential causes of insufficiently treated infection, including renal and perirenal abscesses, calculi, and urinary obstruction. The Society of Uroradiology proposed using acute pyelonephritis to describe acutely infected kidneys, eliminating the need for terms such as bacterial nephritis, lobar nephronia, renal cellulitis, lobar nephritis, renal phlegmon, and renal carbuncle.27

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FIG. 9.18  Urethral Diverticulum in Young Woman With Palpable Vaginal Mass.  (A) Sagittal and (B) transverse translabial sonograms show a complex cystic mass adjacent to the anterior urethra.

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At ultrasound, the majority of kidneys with acute pyelonephritis appear normal. However, ultrasound findings of pyelonephritis include (Fig. 9.19) renal enlargement, compression of the renal sinus, decreased echogenicity (secondary to edema) or increased echogenicity (potentially from hemorrhage), loss of corticomedullary differentiation, poorly marginated mass(es), gas within the renal parenchyma,26,27 and focal or diffuse absence of color Doppler perfusion corresponding to the swollen inflamed areas. If the pyelonephritis is focal, the poorly marginated masses may be echogenic, hypoechoic, or of mixed echogenicity. Echogenic masses may be the most common appearance of focal pyelonephritis.28 Sonography, including power Doppler, is less sensitive than CT, magnetic resonance imaging (MRI), or technetium-99m single-photon emission computed tomography (99mTc-DMSA SPECT) renal cortical scintigraphy for demonstrating changes of acute pyelonephritis. However, ultrasound is more accessible

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and less expensive and thus an excellent screening modality for monitoring and follow-up of complications,29 as well as in the assessment of pregnant patients with acute pyelonephritis because of its lack of ionizing radiation.26,27 A unique renal infection known as alkaline-encrusted pyelitis has been described in renal transplants and native kidneys of

Acute Pyelonephritis on Sonography Renal enlargement Compression of renal sinus Abnormal echotexture (either increased or decreased) Loss of corticomedullary differentiation Poorly marginated mass(es) Gas within renal parenchyma Focal or diffuse absence of color Doppler perfusion corresponding to the swollen inflamed areas

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FIG. 9.19  Acute Pyelonephritis in Three Patients.  (A) Subtle focal increased echogenic areas are seen in the anterior cortex of the right kidney. (B) Power Doppler perfusion defect in lower pole of kidney of patient with documented E. coli pyelonephritis. Note normal corresponding gray-scale image. (C) Sagittal and (D) transverse sonograms in a third patient show a swollen and edematous kidney with focal altered echogenicity and loss of corticomedullary differentiation. The renal sinus fat is attenuated by swollen parenchyma.

CHAPTER 9  The Kidney and Urinary Tract debilitated and immunocompromised patients.30 This entity is most frequently caused by Corynebacterium urealyticum, a ureasplitting microorganism. Urothelial stone encrustation develops in the kidney and bladder. If the kidney is affected, the patient may present with hematuria, stone passage, or an ammonium odor to the urine. Dysuria and suprapubic pain are the most common clinical signs if the bladder is involved. Treatment is with antibiotics and local acidification of the urine. On sonography, alkaline-encrusted pyelitis is suggested if thickened, calcified urothelium is identified.30 The calcification can be thin and smooth or thick and irregular. Care should be taken to distinguish urothelial calcification from layering of collecting system calculi.30

Renal and Perinephric Abscess Untreated or inadequately treated acute pyelonephritis may lead to parenchymal necrosis and abscess formation. Patients at increased risk for renal abscesses include those with diabetes, compromised immunity, chronic debilitating diseases, urinary tract obstruction, infected renal calculi, and intravenous drug abuse.26,31 Renal abscesses tend to be solitary and may spontaneously decompress into the collecting system or perinephric space. Perinephric abscesses, also a complication of pyonephrosis, may result from direct extension of peritoneal or retroperitoneal infection or interventions.24 Small abscesses are treated conservatively with antibiotics, whereas larger abscesses often require percutaneous drainage and, if drainage is unsuccessful, surgery. At ultrasound, renal abscesses appear as round, thick-walled, hypoechoic complex masses with through transmission (Fig. 9.20). Internal mobile debris and septations may be seen. Occasionally, “dirty shadowing” may be noted posterior to gas within the abscess. The differential diagnosis includes (1) hemorrhagic or infected cysts, (2) parasitic cysts, (3) multiloculated cysts, and (4) cystic neoplasms. Although not as accurate as CT in determining the presence and extent of perinephric abscess extension,26

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sonography is an excellent modality for following conservatively treated patients with abscesses to document resolution.

Pyonephrosis Pyonephrosis implies purulent material in an obstructed collecting system. Depending on the level of obstruction, any portion of the collecting system, including the ureter, can be affected. Early diagnosis and treatment are crucial to prevent development of bacteremia and life-threatening septic shock. The mortality rates of bacteremia and septic shock are 25% and 50%, respectively32; 15% of patients are asymptomatic at presentation.33 In the young adult, UPJ obstruction and calculi are the most frequent cause of pyonephrosis, whereas malignant ureteral obstruction is typically the predisposing factor in older patients.26 Pyonephrosis is suggested when ultrasound shows mobile collecting system debris (with or without a fluid-debris level), collecting system gas, and stones (Fig. 9.21). Emphysematous Pyelonephritis Emphysematous pyelonephritis (EPN) is an uncommon, lifethreatening infection of the renal parenchyma characterized by gas formation.34 Most patients are women (2 : 1) and diabetic (90%), with a mean age of 55 years. In diabetic patients, EPN tends to occur in nonobstructed collecting systems; the reverse is true in nondiabetic patients. Bilateral disease occurs in 5% to 10% of EPN patients. Escherichia coli is the offending organism in 62% to 70% of cases; Klebsiella (9%), Pseudomonas (2%) Proteus, Aerobacter, and Candida are additional causative organisms.26,31 At presentation, most patients are extremely ill with fever, flank pain, hyperglycemia, acidosis, dehydration, and electrolyte imbalance35; 18% present only with fever of unknown origin.36 Wan et al.37 retrospectively studied 38 patients with EPN and identified two types of disease: EPN1, characterized by parenchymal destruction and streaky or mottled gas, and EPN2,

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FIG. 9.20  Renal Abscess.  (A) Sagittal ultrasound shows a complex cystic upper-pole lesion containing layering low level echoes. (B) Corresponding contrast-enhanced CT exam shows a large right upper-pole cystic lesion with a thick rind. The patient was successfully treated with ultrasound guided drain placement and antibiotics.

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FIG. 9.21  Pyonephrosis.  (A) Sagittal ultrasound of an older male with Proteus mirabilis sepsis shows a deformed, chronically hydronephrotic kidney, with layering collecting system echoes. (B) Corresponding noncontrast-enhanced CT shows a large right hydronephrotic sac and perinephric infiltration. Clinical history and imaging findings prompted successful, emergent drainage.

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FIG. 9.22  Emphysematous Pyelonephritis Type 1 (EPN1).  (A) Sagittal sonogram of right renal fossa shows extensive shadowing gas occupying most of the right kidney. (B) Corresponding noncontrast-enhanced CT demonstrates diffuse parenchymal destruction of the right kidney with extensive mottled gas. Nephrectomy was eventually performed in this septic, diabetic patient. Caution must be exercised to avoid missing EPN1 altogether on ultrasound. Failure to see a kidney in a septic patient should prompt alternative cross-sectional imaging.

characterized as renal or perirenal fluid collections, with bubbly or loculated gas or with gas in the collecting system. Mortality rates for EPN1 and EPN2 were 69% and 18%, respectively. The authors postulated that the different clinical outcomes of EPN1 and EPN2 result from the patient’s immune status and the vascular supply of the affected kidney. Emergency nephrectomy is the treatment of choice for EPN1, whereas percutaneous drainage is recommended for EPN2. CT is the preferred method to image patients with EPN, to determine the location and extent of renal and perirenal gas. Sonographic evaluation of EPN1 or EPN2 may be difficult because dirty shadowing from parenchymal gas

will obscure deeper structures; shadowing might also prompt an erroneous interpretation of renal calculi or bowel gas38 (Fig. 9.22).

Emphysematous Pyelitis Emphysematous pyelitis refers to gas localized within the urinary collecting system.34 This disease entity is seen most often in women with diabetes or obstructing stone disease; a mortality rate of 20% has been reported. It is important to exclude iatrogenic causes of gas within the collecting system. At ultrasound, nondependent linear echogenic lines with dirty distal posterior

CHAPTER 9  The Kidney and Urinary Tract acoustic shadowing, indicative of gas are seen within the collecting system (Fig. 9.23). As with EPN, CT is often required to identify emphysematous pyelitis because dirty acoustic shadowing from gas at ultrasound may obscure the exact extent of renal and perirenal disease.

Chronic Pyelonephritis Chronic pyelonephritis is an interstitial nephritis often associated with vesicoureteric reflux. Reflux nephropathy is believed to cause 10% to 30% of all cases of end-stage renal disease (ESRD)39 (Fig. 9.24). Chronic pyelonephritis usually begins in childhood and is more common in women. The renal changes may be unilateral or bilateral but usually are asymmetric.

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Reflux into the collecting tubules occurs when the papillary duct orifices are incompetent. This reflux occurs more often in compound papillae, which are typically found at the poles of the kidneys. Cortical scarring therefore tends to occur over polar calices. There is associated papillary retraction with caliceal clubbing. At ultrasound, a dilated blunt calix is seen, associated with overlying cortical scar or cortical atrophy40 (Fig. 9.25). These changes may be multicentric and bilateral. If the disease is unilateral, there may be compensatory hypertrophy of the contralateral kidney. If the disease is multicentric, compensatory hypertrophy of normal intervening parenchyma may create an island of normal tissue simulating a tumor.

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FIG. 9.23  Emphysematous Pyelitis.  (A) Transverse sonogram of left kidney shows “clean” shadowing posterior to a renal calculus (C) and “dirty” shadowing posterior to nondependent collecting system gas (G). (B) Confirmatory unenhanced CT image shows both a calculus and gas within the left collecting system.

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FIG. 9.24  Reflux Nephropathy: Renal Transplantation Evaluation.  (A) Sagittal sonogram shows marked right hydronephrosis and absence of overlying cortex. (B) Cystogram confirms massive bilateral ureteral reflux.

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FIG. 9.25  Chronic Pyelonephritis.  (A) Sagittal sonogram of a patient with a history of vesicoureteral reflux shows upper-pole atrophy and severe cortical loss overlying a deformed, dilated calyx. (B) Sagittal sonogram shows an atrophic kidney with scarring and dilatation of the collecting system caused by reflux. (C) Sagittal sonogram shows an echogenic wedge-shaped scar in the midpole of the kidney. (D) Confirmatory CT scan.

Xanthogranulomatous Pyelonephritis Xanthogranulomatous pyelonephritis (XGP) is a chronic, suppurative renal infection in which destroyed renal parenchyma is replaced with lipid-laden macrophages. XGP is typically unilateral and may be diffuse, segmental, or focal. XGP is typically associated with nephrolithiasis (70%) and obstructive nephropathy.41-43 The disease most commonly occurs in middleaged women and diabetic patients.43 Presenting signs are nonspecific: pain, mass, weight loss, and UTI (Proteus or E. coli).41 The diffusely involved kidney is usually nonfunctional. Ultrasound findings of diffuse XGP include renal enlargement, maintenance of a reniform shape, and lack of corticomedullary differentiation. Multiple hypoechoic areas correspond to dilated calices or inflammatory parenchymal masses.41 Through transmission is variable and depends on the degree of liquefaction of the parenchymal masses. Occasionally, the large, complex cystic masses may mimic pyonephrosis. A staghorn calculus will result in extensive shadowing from the central renal sinus (Fig. 9.26). Perinephric extension may occur, but this is often best appreciated with CT. Diffuse XGP has no specific sonographic features but is suggested when parenchymal thinning, hydronephrosis, stones,

debris in a dilated collecting system, and perinephric fluid collections are present.44 Segmental XGP will be seen as one or more hypoechoic masses, often associated with a single calyx.41,45 An obstructing calculus may be seen near the papilla. Focal XGP arises in the renal cortex and does not communicate with the renal pelvis. It cannot be distinguished sonographically from tumor or abscess.41

Papillary Necrosis Causative factors implicated in the ischemia that leads to papillary necrosis include analgesic abuse, diabetes, UTI, renal vein thrombosis, prolonged hypotension, urinary tract obstruction, dehydration, sickle cell anemia, and hemophilia.46 Initially, the papilla swells (Fig. 9.27); then a communication with the caliceal system occurs. The central aspect of the papilla cavitates and may slough. With papillary cavitation, ultrasound shows cystic collections within the medullary pyramids. If the papilla sloughs, the affected adjacent calyx will be clubbed. The sloughed papilla can be seen in the collecting system as an echogenic nonshadowing structure. If the sloughed papilla calcifies, distal acoustic shadowing simulating medullary nephrocalcinosis will be seen.47

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FIG. 9.26  Xanthogranulomatous Pyelonephritis.  (A) Sagittal sonogram shows an enlarged hypoechoic kidney and a large showing staghorn calculus. (B) Corresponding contrast-enhanced CT demonstrates a diffusely enlarged left kidney, multiple intrarenal abscesses, and a large, central obstructing calculus.

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Sonographic Findings of Papillary Necrosis Swollen pyramids Papillary cavitation Adjacent clubbed calix Sloughed papilla in collecting system that can calcify and simulate a stone Sloughed papilla may cause obstruction

Hydronephrosis may develop if the sloughed papilla obstructs the ureter.

Tuberculosis Urinary tract tuberculosis (TB) occurs with hematogenous seeding of the kidney by Mycobacterium tuberculosis from an extraurinary

source (typically lung). Urinary tract TB usually manifests 5 to 10 years after the initial pulmonary infection. Chest radiographs may be normal (35%-50% of patients) or may show active TB (10%) or inactive healed TB (40%-55%). Most patients present with lower urinary tract signs and symptoms that include frequency, dysuria, nocturia, urgency, and gross or microscopic hematuria, whereas 10% to 20% of patients are asymptomatic.48 Urinalysis findings include sterile pyuria, microscopic hematuria, and acidic pH. TB is definitively diagnosed with acid-fast bacilli urine cultures; however, this usually requires 6 to 8 weeks for growth. Although both kidneys are seeded initially, clinical manifestations of urinary tract TB are typically unilateral. The early or acute changes include development of multiple small bilateral tuberculomas. Das et al.49 found that the most frequently encountered sonographic abnormality was focal renal lesions

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(Fig. 9.28). Small focal lesions (5-15 mm) were echogenic or were hypoechoic with an echogenic rim. Larger, mixedechogenicity focal lesions (>15 mm) were poorly defined. Bilateral disease was noted in 30% of patients. Most tuberculomas will heal spontaneously or after antituberculous therapy. At some later date (perhaps years later), one or more of the tubercles may enlarge. With enlargement, cavitation and communication with the collecting system will occur. The resultant pathologic changes resemble papillary necrosis; papillary involvement is noted when a sonolucent linear tract is shown extending from the involved calix into the papilla. Soft tissue caliceal masses representing sloughed papilla may be seen. After rupture into the collecting system, M. tuberculosis bacilluria develops and allows the spread of the renal infection to other parts of the urinary tract. Spasm or edema in the region of the UVJ may occur, giving rise to hydronephrosis and hydroureter. Ureteric linear ulcers may also occur, typically within the distal ureter. Bladder involvement is seen in 33% of patients with genitourinary tract TB.49 Early bladder manifestations include mucosal edema and ulceration. Early clinical symptoms (dysuria and frequency) are also nonspecific. If edema occurs at the bladder trigone, ureteric obstruction may occur. At ultrasound, early bladder involvement will appear as focal or diffuse wall thickening; the thickening can be quite extensive (Fig. 9.29). The later or more chronic changes of genitourinary tract TB include fibrotic strictures, extensive cavitation, calcification, mass lesions, perinephric abscesses, and fistulas.48 The chronic changes, in particular those related to fibrotic strictures, result in functional renal damage. Strictures may occur anywhere in the intrarenal collecting system and ureter. The obstruction then results in proximal collecting system dilatation and pressure atrophy of

the renal parenchyma. With time, calcification in the areas of caseation or sloughed papilla may occur. If renal infection ruptures into the perinephric space, an abscess may develop. Perinephric abscesses may ultimately result in fistulas to adjacent viscera. The hallmark of chronic, upper tract renal TB is a small, nonfunctional, calcified kidney, the “putty” kidney. In the bladder, chronic infection and fibrosis result in a thickened, small-capacity bladder.48 Speckled or curvilinear calcification of the bladder wall may rarely occur.50 Most cases of genitourinary tract TB can be diagnosed with a combination of intravenous/retrograde urography, ultrasound, CT, and CT urography.51 Premkumar et al.52 demonstrated in 14 patients with advanced urinary tract TB that detailed morphologic information and functional renal status are best assessed with CT and urography. Das et al.53 reported that ultrasoundguided, fine-needle aspiration (1) may be diagnostic in patients with negative urine cultures and (2) may confirm a diagnosis of upper genitourinary tract TB in those patients with suspicious lesions and positive cultures.

FIG. 9.28  Progressive Renal Tuberculosis.  Sagittal sonogram shows small, irregular hypoechoic medullary lesions. Areas of cavitation ultimately connect to the collecting system. (With permission from Wasnik AP. Tuberculosis, urinary tract. In: Kamaya A, Wong-You-Cheong J, editors. Diagnostic ultrasound: abdomen and pelvis. Philadelphia: Elsevier; 2016. pp. 490-493.51)

FIG. 9.29  Urinary Bladder Tuberculosis.  Transverse sonogram shows irregular mucosal thickening, particularly at the ureteric orifice—a characteristic feature of early bladder tuberculosis. (With permission from Wasnik AP. Tuberculosis, urinary tract. In: Kamaya A, Wong-YouCheong J, editors. Diagnostic ultrasound: abdomen and pelvis. Philadelphia: Elsevier; 2016. pp. 490-493.51)

Fungal Infections Patients with a history of diabetes mellitus, chronic indwelling catheters, malignancy, hematopoietic disorders, chronic antibiotic or steroid therapy, transplantation, and intravenous drug abuse are at risk for developing fungal infections of the urinary tract.54

Candida Albicans Candida albicans is the most common fungal agent that affects the urinary tract. Renal parenchymal involvement, typically manifested by small parenchymal abscesses, occurs in the context of diffuse systemic involvement. The abscesses may calcify over

CHAPTER 9  The Kidney and Urinary Tract time.55 Extension into the perinephric space is also possible. Invasion of the collecting system ultimately results in fungus balls. Collecting system mycetomas may be differentiated from blood clots, radiolucent stones, transitional cell tumors, sloughed papillae, fibroepithelial polyps, cholesteatomas, and leukoplakia based on clinical history and urine cultures.56-58 On sonography, candidal microabscesses are typically small, hypoechoic cortical lesions; the appearance is similar to other bacterial abscesses. Fungus balls appear as echogenic, nonshadowing soft tissue masses within the collecting system59 (Fig. 9.30). Fungus balls are mobile and may cause obstruction and hydronephrosis.

Parasitic Infections A wide variety of parasitic infections are common in developing countries. Sonographers should be particularly familiar with schistosomiasis and echinococcal (hydatid) disease.

Schistosomiasis Schistosoma haematobium is the most common agent to affect the urinary tract. The worms enter the human host by penetrating the skin. They are then carried via the portal venous system to the liver, where they mature into their adult form. S. haematobium likely enters the perivesical venous plexus from the hemorrhoidal plexus.60 The female worm then deposits eggs into the venules of the bladder wall and ureter. Granuloma formation and obliterative endarteritis occur. Serologic tests demonstrating ova allow diagnosis. Hematuria is the most frequent complaint.60 At sonography, the kidneys are normal until late in the disease. Pseudotubercles develop in the ureter and bladder, and the urothelium becomes thickened (Fig. 9.31).61 Over time the pseudotubercles calcify; the calcification may be fine, granular and linear, or thick and irregular. If repeated infections occur, the bladder will become small and fibrotic. Bladder stasis results in an increased incidence of ureteral and bladder calculi.60 Patients with chronic disease also have an increased incidence of squamous cell carcinoma.60

FIG. 9.30  Fungus Ball.  Sagittal sonogram shows an echogenic soft tissue mass within a dilated upper-pole cortex.

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Echinococcal (Hydatid) Disease The two major types of hydatid disease that affect the urinary tract are caused by Echinococcus multilocularis and the more common Echinococcus granulosus. Renal hydatid disease is found in 2% to 5% of patients with hydatid disease,60 is usually solitary, and typically involves the renal poles.62 Hydatid cysts may occur along the ureter or within the bladder. Each hydatid cyst consists of three layers: the pericyst, ectocyst, and endocyst. Echinococcal disease is often silent until the cyst grows large enough to rupture or compress adjacent structures. The ultrasound manifestation of early hydatid disease is an anechoic cyst. Mural nodularity suggests scolices. When daughter cysts are present, a multiloculated cystic mass will be seen (Fig. 9.32). The membranes from the endocyst may detach and precipitate to the bottom of the hydatid fluid to become “hydatid sand.”63 Varying patterns of calcification occur, ranging from eggshell to dense reticular calcification. Ring-shaped calcifications inside a larger, calcified lesion suggest calcified daughter cysts.60,63 A specific ultrasound diagnosis is difficult without an appropriate clinical history. However, several features may suggest hydatid disease, including floating membranes, daughter cysts, and thick, double-contour cyst walls.64

Acquired Immunodeficiency Syndrome The disease course and imaging manifestations of human immunodeficiency virus (HIV) infection, acquired immunodeficiency syndrome (AIDS), and HIV-associated nephropathy have rapidly evolved largely because of advances in the care of HIV-positive patients. Highly active antiretroviral therapy (HAART) has resulted in a decreased incidence of opportunistic infections and improved survival.

FIG. 9.31  Bladder Schistosomiasis.  Transverse sonogram shows mild bladder wall thickening and linear anterior wall echogenicity due to early calcification. (With permission from Wasnik AP. Schistosomiasis, bladder. In: Kamaya A, Wong-You-Cheong J, editors. Diagnostic ultrasound: abdomen and pelvis. Philadelphia: Elsevier; 2016. pp. 548-549.61)

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FIG. 9.32  Renal Hydatid Cyst.  (A) Sagittal sonogram shows a complex multiloculated lower-pole cystic mass (arrows). (B) Contrast-enhanced CT shows multiple confluent daughter cysts. (Courtesy of Drs. Vikram Dogra and Suleman Merchant.)

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FIG. 9.33  Proven Pneumocystis Nephropathy in a Patient With AIDS.  (A) Sagittal and (B) transverse sonograms show multiple scattered echogenic foci within the renal parenchyma. Some foci demonstrate the distal acoustic shadowing of calcification. Similar findings are seen in the liver. (With permission from Spouge AR, Wilson S, Gopinath N, et al. Extrapulmonary Pneumocystis carinii in a patient with AIDS: sonographic findings. AJR Am J Roentgenol. 1990;155:76-78.66)

Early literature noted the increased incidence of opportunistic genitourinary infections (cytomegalovirus [CMV], Candida albicans, Cryptococcus, Pneumocystis jiroveci [formerly P. carinii], Mycobacterium avium-intracellulare, Mucormycosis) and tumors (lymphoma, Kaposi sarcoma) in these immunocompromised patients.65 The appearance of these infections is often nonspecific (and now rare), but diffuse visceral/renal calcifications suggest disseminated P. jiroveci, CMV, or M. avium-intracellulare infections66-68 (Fig. 9.33). The genitourinary infections that now occur in these patients, including pyelonephritis, renal abscesses, and cystitis, are similar to those seen in non–HIV-infected individuals. Use of HAART has also changed the spectrum of chronic renal diseases seen in HIV-positive patients. The incidence of ESRD in HIV patients decreased initially after the institution of

HAART; however, the increased prevalence of HIV in the US population has resulted in an increased number of patients with HIV-associated nephropathy (HIVAN).69 In HIV-positive patients, HIVAN is the most common cause of chronic kidney disease; black patients are at particular risk. The histologic hallmark of HIVAN is focal segmental glomerulosclerosis. Nephropathy in HIV-positive patients may also be caused by HIV immune complex disease and HIV thrombotic microangiopathy. Adverse renal effects of various drugs also complicate the diagnosis of chronic renal failure.70 However, other disease processes not directly associated with HIV infection (e.g., hypertension, diabetic nephropathy, interstitial nephritis) may result in ESRD in patients successfully treated with HAART.71 Definitive diagnosis of HIVAN is usually made after renal biopsy. Renal sonography is useful in these patients to exclude obstruction

CHAPTER 9  The Kidney and Urinary Tract and determine renal size. Early reports also suggested that greatly increased renal echogenicity is a fairly specific finding of HIVAN (and heroin nephropathy)65,72,73 (Fig. 9.34). Other features in HIV-positive patients with renal insufficiency include globularappearing kidneys, decreased corticomedullary differentiation, decreased renal sinus fat, and parenchymal heterogeneity.74

Cystitis Infectious Cystitis Women are at increased risk for cystitis because of colonization of the short female urethra by rectal flora. Bladder outlet obstruction or prostatitis results in cystitis in men. The most common pathogen is E. coli.75 Mucosal edema and decreased bladder capacity are common. Findings may be more prominent at the trigone and bladder neck. Patients will present with bladder irritability and hematuria. The most common finding at sonography is diffuse bladder wall thickening. If cystitis is focal, pseudopolyps may form, which are impossible to differentiate from tumor76 (Fig. 9.35A). Malacoplakia Malacoplakia is a rare granulomatous infection with a predilection for the urinary bladder. The disease is seen more often in women (4 : 1), with a peak incidence in the sixth decade.77 The pathogenesis of malacoplakia is not known; however, an association with diabetes mellitus, alcoholic liver disease, mycobacterial infections, sarcoidosis, and transplantation suggests an altered immune response.78 Patients may present with hematuria and symptoms of bladder irritability. At sonography, single or multiple mucosal-based masses ranging from 0.5 to 3.0 cm are seen, typically at the bladder base. Malacoplakia may be locally invasive77 (Fig. 9.35B).

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Emphysematous Cystitis Emphysematous cystitis occurs most often in female patients and those with diabetes. Patients present with symptoms of cystitis and occasionally have pneumaturia.75 The most common offending organism is E. coli. Both intraluminal and intramural gas are present. In these severely ill patients, the urothelium is ulcerated and necrotic and may slough completely. Emphysematous cystitis is suggested at sonography when echogenic foci within the bladder wall are associated with ring-down artifact or dirty shadowing79 (Fig. 9.36A and B). Gas may be seen in the bladder lumen as well. The bladder wall is usually thickened and echogenic.34 A lack of bladder wall thickening may be a helpful sonographic feature to distinguish the gas of emphysematous cystitis from gas introduced by catheterization (Fig. 9.36C). Chronic Cystitis Chronic inflammation of the bladder may be caused by various agents. Although the histology may also vary, the imaging manifestations, including a small, thickened bladder, are nonspecific. Chronic cystitis may result in invagination of solid “nests” of urothelium into the lamina propria (Brunn epithelial nests), which may result in morphologic changes that mimic neoplasia.80 If the central portion of a Brunn nest degenerates, a cyst results (cystitis cystica). If chronic irritation persists, the Brunn nests may develop into glandular structures (cystitis glandularis). These may be precursors of adenocarcinoma.75 Cystitis cystica and cystitis glandularis may be manifested at ultrasound as bladder wall cysts or solid papillary masses (see Fig. 9.35C). Because the appearance of these conditions on imaging can be mistaken for malignancy, cystoscopy with biopsy is necessary for diagnostic confirmation.

Causes of Bladder Wall Thickening FOCAL Neoplasm Transitional cell carcinoma Squamous cell carcinoma Adenocarcinoma Lymphoma Metastases Infectious/Inflammatory Tuberculosis (acute) Schistosomiasis (acute) Cystitis Malacoplakia Cystitis cystica Cystitis glandularis Fistula Medical Diseases Endometriosis Amyloidosis FIG. 9.34  HIV-Associated Nephropathy (HIVAN).  Sagittal sonogram shows an enlarged, markedly echogenic kidney. Biopsy confirmed focal segmental glomerulosclerosis.

Trauma Hematoma

DIFFUSE Neoplasm Transitional cell carcinoma Squamous cell carcinoma Adenocarcinoma Infectious/Inflammatory Cystitis Tuberculosis (chronic) Schistosomiasis (chronic) Medical Diseases Interstitial cystitis Amyloidosis Neurogenic Bladder Detrusor hyperreflexia Bladder Outlet Obstruction With muscular hypertrophy

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FISTULAS, STONES (CALCULI), AND CALCIFICATION Bladder Fistulas Bladder fistulas can be congenital or acquired. Causes of acquired fistulas include trauma, inflammation, radiation, and neoplasm. Fistula from the bladder to the vagina, gut, skin, uterus, and the ureter may occur. Vesicovaginal fistulas are most often related to gynecologic or urologic surgery, bladder carcinoma, and carcinoma of the cervix. Vesicoenteric fistulas typically occur as a complication of diverticulitis or Crohn disease. Vesicocutaneous fistulas result from surgery or trauma. Vesicouterine fistulas are a rare complication of cesarean section. Vesicoureteral fistulas are also rare and usually occur after hysterectomy.81 All these fistulas are difficult to identify directly by sonography because the tracts are often thin and short. Occasionally, linear bands of varying echogenicity may be seen.82,83 If the bladder

FIG. 9.35  Infectious Cystitis.  (A) Transverse decubitus sonogram reveals bladder wall thickening (arrowheads) with pseudopolyp formation (arrows). (B) Bladder malacoplakia. Transverse sonogram shows a mucosal-based mass with focal invasion of the prostate gland. (C) Cystitis glandularis. Transverse sonogram shows a solid papillary mass.

communicates with gut, vagina, or skin, an abnormal collection of gas may be seen in the bladder lumen. At ultrasound, this appears as a nondependent linear echogenic focus with distal dirty shadowing. Palpation of the abdomen during scanning may cause gas to percolate through the fistula, enhancing its detection83 (Fig. 9.36D). For depicting often short vesicovaginal fistulas, color Doppler sonographic flow jets may be shown with diluted microbubble contrast agents in the bladder.84

Renal Calculi Renal stones are common, with a reported prevalence of 12% in the general population.85 Stone disease increases with advancing age, and white men are most often affected. From 60% to 80% of calculi are composed of calcium.86 Multiple predisposing conditions, including dehydration, urinary stasis, hyperuricemia, hyperparathyroidism, and hypercalciuria, may result in renal calculi, but no cause is identified in most patients. Caliceal

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FIG. 9.36  Gas Within the Bladder; Emphysematous Cystitis.  (A) Transverse sonogram shows intraluminal gas along left anterior bladder wall. Note “dirty” posterior shadowing. (B) Corresponding CT in this patient with confirmed emphysematous cystitis shows mild bladder wall thickening and adjacent gas. (Courtesy of Shweta Bhatt, MD.) (C) Iatrogenic air introduced at cystoscopy appears as a nondependent bright echogenic focus with multiple reflection artifacts. (D) Enterovesical fistula (arrow) showing gas in the bladder as multiple bright echogenic foci on a transvaginal sonogram.

calculi that are nonobstructing are usually asymptomatic. Patients with small caliceal calculi may have gross or microscopic hematuria and may have colic symptoms despite the lack of imaging findings suggestive of obstruction.87 A calculus that migrates and causes infundibular or UPJ obstruction often results in clinical signs and symptoms of flank pain. If a stone passes into the ureter, the calculus may lodge in three areas of ureteric narrowing: just past the UPJ; where the ureter crosses the iliac vessels; and at the UVJ. The very small diameter of the UVJ (1-5 mm) accounts for the large percentage of calculi that lodge within the distal ureter.86 Approximately 80% of stones smaller than 5 mm will pass spontaneously.

Renal calculi can be detected using many different imaging modalities, including plain films, tomography, intravenous urography, ultrasound, and unenhanced CT. Sensitivities of 12% to 96% for the ultrasound detection of calculi have been reported. This wide discrepancy is a result of differing definitions (renal or ureteral), composition, and sizes of calculi.88 Stones greater than 5 mm were detected with 100% sensitivity by ultrasound. Ultrasound with or without plain radiography competes favorably with unenhanced CT in select patients with ureteral colic.89-91 The sensitivity of ultrasound detection of urinary calculi in patients with acute flank pain is 77% to 93%.92-94 The 2016 European Association of Urology guidelines for diagnosis and

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treatment of urolithiasis list ultrasound as the primary diagnostic imaging tool.95 However, noncontrast-enhanced low-dose CT has higher sensitivity (95%) and specificity (97%) for urolithiasis than does ultrasound.96 Thus many centers use low-dose CT, particularly in patients in whom ureteral stones are suspected or patients whose initial screening ultrasound examination is negative or equivocal but clinical suspicion remains elevated. Operator technique clearly impacts the ability of ultrasound to depict renal calculi. On sonography, renal calculi are seen as echogenic foci with sharp, distal acoustic shadowing (Fig. 9.37). Even in favorable locations, however, small urinary tract calculi may be difficult to detect if they have a weak posterior acoustic shadow. The trade-off between tissue penetration and resolution should be considered when selecting probe frequency, with appropriate focal zones applied to maximize signature shadowing. Harmonic imaging should also be routinely used, particularly in obese patients. The application of color Doppler may also improve the detection of small, minimally shadowing calculi.97 Lee et al.98

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demonstrated that most urinary tract stones (83%) show color and power Doppler sonographic twinkling artifacts, although the artifact at least partially depends on stone composition99 (Fig. 9.38). The relevance of this adjunct technique in the screening of patients with potential urinary colic has been questioned, however. In a recent retrospective study, Dillman et al. demonstrated a high (51%) false positive rate for the twinkle artifact when using noncontrast-enhanced CT as a reference standard.100 Several features that mimic renal calculi at ultrasound can result in false positive examination results, including intrarenal gas (see Fig. 9.23), renal artery calcification (Fig. 9.39), calcified sloughed papilla, calcified transitional cell tumor, alkalineencrusted pyelitis, and encrusted ureteral stents. Although the ultrasound evaluation of the secondary manifestation of an obstructing ureteral calculus—collecting system dilatation—is usually straightforward, pitfalls include (1) evaluation before hydronephrosis develops, leading to a false negative result, and (2) mistaking parapelvic cysts and nonobstructive pyelocaliectasis as hydronephrosis.101

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FIG. 9.37  Renal Calculi.  Sagittal sonograms. (A) Small, midpole echogenic foci with shadowing representing nonobstructing calculi. (B) Multiple lower-pole and renal pelvic calculi with associated mild hydronephrosis. (C) Large staghorn calculus with severe upper-pole caliectasis (arrowheads).

CHAPTER 9  The Kidney and Urinary Tract

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FIG. 9.38  Twinkle Artifacts Indicating Renal Calculi.  (A) Transverse sonogram and simultaneous Doppler image show shadowing calculi, posterior shadowing, and color Doppler twinkle artifact. (B) A follow-up CT shows the larger calculus. The color Doppler twinkle artifact may sometimes aid in detection of small calculi, although often no corresponding calculi are shown on noncontrast-enhanced CT. The reason for this discrepancy is not clear, although it may be due to relatively large (5-mm) collimation typically used for the CT evaluation of calculi.

FIG. 9.39  Sonographic Feature Mimicking Renal Calculus. Transverse sonogram shows a linear distal renal artery calcification.

Entities That Mimic Renal Calculi Intrarenal gas Renal artery calcification Calcified sloughed papilla Calcified transitional cell tumor Alkaline-encrusted pyelitis Encrusted calcification of ureteric stent

Ureteral Calculi The search for ureteral calculi may be particularly difficult at sonography because of overlying bowel gas and the deep retroperitoneal location of the ureter (Fig. 9.40). However, transvaginal or transperineal scanning aid in detection of distal ureteral calculi that are not seen with a transabdominal suprapubic approach.83,102,103

When the ureter is dilated, the distal 3 cm will be seen as a tubular hypoechoic structure entering the bladder obliquely. A stone will be identified as an echogenic focus with sharp, distal acoustic shadowing within the ureteric lumen (Fig. 9.41). There may be associated mucosal edema at the bladder trigone. Transabdominal evaluation of the ureteral orifices for jets is helpful to assess for obstruction (Video 9.1).104 At gray-scale ultrasound, a stream of low-level echoes can be seen entering the bladder from the ureteral orifice. The jet is likely shown at ultrasound because of both motion and a density difference between the jet and urine in the bladder.105 Good hydration before the study maximizes the density difference between ureteral and bladder urine and aids in jet visualization.106 In addition to gray-scale evaluation, Doppler ultrasound improves detection of ureteric jets. Color Doppler allows for simultaneous visualization of both ureteral orifices104 (Fig. 9.42). Depending on the state of hydration, jet frequency may vary from less than one per minute to continuous flow; however, jets should be symmetric in a healthy individual. Patients with highgrade ureteral obstruction will have either a completely absent jet or a continuous, low-level jet on the symptomatic side. Patients with low-grade obstruction may or may not have asymmetric jets.104 Semiqualitative assessment of relative jet frequency from the affected side107 may improve diagnostic accuracy, but this technique has not been widely adopted. Thus centers that evaluate ureteral jets with color Doppler use the technique as an adjunct for assessing ureteric obstruction and the possibility of spontaneous ureteral stone passage. Initial studies suggested that the addition of renal duplex Doppler to the gray-scale ultrasound examination would allow diagnosis of both acute and chronic urinary tract obstruction.108 Several studies indicated that the complex hemodynamics that occur with unrelieved obstruction can be semiquantitatively assessed by measuring intrarenal arterial resistive indices (RI =

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FIG. 9.40  Distal Ureteral Calculi.  Sagittal sonograms of the distal ureters in two patients. (A) Calculus is 1 cm from the ureterovesical junction (UVJ), with extensive edema of the distal ureteric mucosa. (B) Tiny calculus at UVJ with no obvious edema. Note posterior acoustic shadowing.

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FIG. 9.41  Ureterovesical Calculus.  Transvaginal sonograms in two patients show the value of this technique. (A) Small calculus obstructs a mildly dilated ureter at UVJ. (B) Larger calculus with extensive surrounding ureteric edema.

peak systolic velocity–end diastolic velocity/peak systolic velocity). It is believed that with obstruction, renal pelvic wall tension increases, initially resulting in a short period of prostaglandinmediated vasodilation.109 With prolonged obstruction, many hormones, including renin-angiotensin, kallikrein-kinin, and prostaglandin-thromboxane, reduce vasodilation and produce diffuse vasoconstriction. Geavlete et al.110 found that if there was an intravesical ureteric jet on the renal colic side associated with arcuate or intralobar RI values of 0.7 or less and difference between renal RI values of 0.06 or less, spontaneous passage of the stone occurred in 71% of cases. Platt et al.108 used a threshold RI greater than 0.70 to indicate obstruction, noting a difference in RI of

0.08 to 0.1 when comparing the patients’ obstructed and nonobstructed kidneys. Initial reports advocating the Doppler assessment of renal obstructive physiology were tempered by a series of less promising studies.101,109 The RI is largely dependent on tissue/vascular compliance (diminished compliance results in elevated RI, and vice versa) and driving pulse pressures, and thus is not uniformly affected by obstruction.111-114

Bladder Calculi Bladder calculi most often result from either stone migration from the kidney or bladder stasis. Urinary stasis is usually related to a bladder outlet obstruction, cystocele, neurogenic bladder,

CHAPTER 9  The Kidney and Urinary Tract

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FIG. 9.42  Color Doppler Evaluation of Ureteral Colic.  Transverse images of the bladder in two patients. (A) Normal symmetrical bilateral ureteral jets. (B) Persistent left ureteral jet distal to a partially obstructing left UVJ calculus. Note twinkle artifact posterior to ureteral calculus.

Nephrocalcinosis

FIG. 9.43  Bladder Calculus.  Sagittal sonogram shows a small dependent echogenic focus with posterior sharp acoustic shadowing. Note bladder wall trabeculation.

or a foreign body in the bladder. Bladder calculi may be asymptomatic. If symptomatic, patients will complain of bladder pain or foul-smelling urine with or without hematuria. At sonography, a mobile, echogenic mass with distal acoustic shadowing will be seen (Fig. 9.43). If the stone is large, edema of the ureteral orifices and thickening of the bladder wall may be visualized. Occasionally, stones can adhere to the bladder wall because of adjacent inflammation; these calculi are known as “hanging” bladder stones.

Nephrocalcinosis refers to renal parenchymal calcification. The calcification may be dystrophic or metastatic. With dystrophic calcification, there is deposition of calcium in devitalized (ischemic or necrotic) tissue.115 This type of parenchymal calcification occurs in tumors, abscesses, and hematomas. Metastatic nephrocalcinosis occurs most often with hypercalcemic states caused by hyperparathyroidism, renal tubular acidosis, and renal failure. Metastatic nephrocalcinosis can be further categorized by the location of calcium deposition as cortical or medullary. Causes of cortical nephrocalcinosis include acute cortical necrosis, chronic glomerulonephritis, chronic hypercalcemic states, ethylene glycol poisoning, sickle cell disease, and renal transplant rejection. Causes of medullary nephrocalcinosis include hyperparathyroidism (40%), renal tubular acidosis (20%), medullary sponge kidney, bone metastases, chronic pyelonephritis, Cushing syndrome, hyperthyroidism, malignancy, renal papillary necrosis, sarcoidosis, sickle cell disease, vitamin D excess, and Wilson disease.115 The Anderson-Carr-Randall theory of stone progression postulates that the concentration of calcium is high in the fluid around the renal tubules. The calcium is removed by lymphatics, and if the amount exceeds lymphatic capacity, deposits of calcium in the fornical tips and margins of the medulla will result. The ultrasound manifestation of early medullary calcification are nonshadowing echogenic rims surrounding medullary pyramids.116 However, increased medullary echogenicity can also be caused by medullary sponge kidney117 (Fig. 9.44); it can be a normal transient finding in neonates.118 Further calcium deposition results in acoustic shadowing (Fig. 9.45). The calcifications may perforate the calix and form a nidus for further stone growth.119 Although the physiology of cortical nephrocalcinosis differs from that of medullary nephrocalcinosis, its ultrasound

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manifestations are similar; early cortical calcification may be suggested by increased cortical echogenicity. With progressive calcification, a continuous, shadowing calcified rim develops.

GENITOURINARY TUMORS Renal Cell Carcinoma Renal cell carcinoma (RCC) accounts for approximately 3% of all adult malignancies and 86% of all primary malignant renal parenchymal tumors.120 There is a 2 : 1 male predominance, and peak age is 50 to 70 years. The cause is unknown, although weak associations with smoking,121 chemical exposure, asbestosis, obesity, and hypertension have been shown. The vast majority of RCCs are sporadic, but an estimated 4% occur in the context of inherited syndromes.122,123 These “inherited” RCCs occur at an earlier age, are multifocal and bilateral, and affect

FIG. 9.44  Medullary Sponge Kidney.  Sagittal sonogram shows markedly increased renal medullary echogenicity (“medullary rings”).

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men and women equally.122 Von Hippel–Lindau (VHL) disease is the best known inherited RCC syndrome; 24% to 45% of patients who have VHL disease will develop RCC. Most of these lesions are multicentric and bilateral and are clear cell carcinomas.124-126 Other inherited renal cancer syndromes include hereditary papillary renal cancer, Birt-Hogg-Dubé syndrome, hereditary leiomyoma RCC, familial renal oncocytoma, hereditary nonpolyposis colon cancer, and medullary RCC. An increased incidence of RCC in patients with tuberous sclerosis has also been reported.123 Another important but nonsyndromic risk factor for RCC is the acquired cystic kidney disease that occurs in patients receiving long-term hemodialysis or peritoneal dialysis. The RCCs in these patients are small and hypovascular and tend to be relatively less aggressive.127,128 Histologic subtypes of RCC include clear cell (70%-75%), papillary (15%), chromophobe (5%), oncocytic (2%-3%), and collecting duct or medullary (12 cm in diameter) and contain numerous large, thin-walled cysts, which may replace most of the ovary. The associated ascites and pleural effusions may lead to depletion of intravascular fluids and electrolytes, resulting in hemoconcentration with hypotension, oliguria, and electrolyte imbalance.46 Severe OHS is usually treated conservatively to correct the depleted intravascular volume and electrolyte imbalance and usually resolves within 2 to 3 weeks. Theca lutein cysts are the largest of the functional ovarian cysts and are associated with high hCG levels. These cysts typically occur in patients with gestational trophoblastic disease. However, theca lutein cysts are typically not seen in first-trimester

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diagnosis of gestational trophoblastic disease, because the hCG level will not have been sufficiently high for a long enough time for them to develop.47 Theca lutein cysts can also be seen in OHS as a complication of drug therapy for infertility. Sonographically, theca lutein cysts are usually bilateral, multilocular, and very large. They may undergo hemorrhage, rupture, and torsion. Hyperreactio luteinalis is caused by an abnormal response to circulating hCG in the absence of ovulation induction therapy. Approximately 60% of hyperreactio luteinalis cases occur in singleton pregnancies with normal circulating levels of hCG. Hyperreactio luteinalis usually occurs in the third trimester or less often in the puerperium. The majority of patients are asymptomatic, although maternal virilization may be seen in up to 25% of patients. The incidence of hyperreactio luteinalis increases in women with polycystic ovarian disease.48 In contrast to OHS, body fluid shifts are rare. Sonographically, there are bilaterally enlarged ovaries with multiple cysts similar to OHS, although the ovaries tend not to be as large and the condition occurs later in pregnancy. Hyperreactio luteinalis is a self-limited condition that resolves spontaneously. Luteoma of pregnancy is the only solid mass in this group of pregnancy-related processes. It is a rare benign process unique to pregnancy that is due to stromal cells that may become hormonally active, producing androgens and replacing the normal ovarian parenchyma. Most patients are asymptomatic, although maternal virilization may occur in up to 30%. These patients have a 50% risk of virilization of the female fetus.49 Sonographically, luteomas usually present as nonspecific, heterogeneous, predominantly hypoechoic masses that may be highly vascular. An ovarian mass in a pregnant patient with signs of virilization should suggest this diagnosis, because luteoma is the most common cause of maternal virilization during pregnancy. Surgery is not indicated since the condition resolves spontaneously, typically after delivery.

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FIG. 16.8  Ovarian Hyperstimulation Syndrome.  (A) TVS shows a greatly enlarged ovary with multiple cysts, some hemorrhagic. (B) Sagittal sonogram in right upper quadrant shows large volume of free intraperitoneal fluid.

CHAPTER 16  The Adnexa

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Surface Epithelial Inclusion Cysts Surface epithelial inclusion cysts are nonfunctional cysts usually seen in postmenopausal women, although they may be seen at any age, and are usually located peripherally in the cortex. They arise from cortical invaginations of the ovarian surface epithelium.50 When very small, the cysts themselves may not be seen, but rather they may appear as punctate echogenicities in the surface of the ovary. Although usually tiny, unilocular, and thin walled, these cysts can measure up to several centimeters in diameter. Occasionally, surface epithelial inclusion cysts may be hemorrhagic, particularly if torsion has occurred.

Paraovarian and Paratubal Cysts Paraovarian and paratubal cysts are wolffian or müllerian duct remnants in the mesosalpinx, often located superior to the uterine fundus. They are generally epithelium-lined simple cysts, rarely multiloculated or containing small wall nodularities. Echoes may also be occasionally seen with the cyst sonographically because of hemorrhage. They show no cyclic changes. There is an estimated incidence of 3%, accounting for about 10% to 20% of all adnexal masses. Typically, these cysts are small but may range in size up to 8 cm. They may occur at any age but are most commonly visualized in the third and fourth decades. Most are asymptomatic although patients with large cysts may have pelvic pain or the cysts may act as a fulcrum for torsion.51-53 A specific diagnosis of a paraovarian cyst is possible only by demonstrating a normal ipsilateral ovary adjacent to, but separate from, the cyst.54,55 Benign neoplasms such as cystadenomas and cystadenofibromas of paraovarian origin are uncommon. Malignancy has been reported in 2% to 3% of parovarian cystic masses on histopathologic examination,56,57 although it occurs even less often in masses smaller than 5 cm.54,58

Peritoneal Inclusion Cysts Peritoneal inclusion cysts are seen in patients with peritoneal adhesions, occurring mostly in premenopausal women with a history of previous abdominal surgery, but they may also be seen in patients with a history of trauma, PID, or endometriosis. In patients with peritoneal adhesions, fluid produced by the ovary (which is the main producer of peritoneal fluid in women13) may accumulate within the adhesions and entrap the ovaries, resulting in an adnexal mass.59-62 Peritoneal inclusion cysts are lined with mesothelial cells. Clinically, most patients present with pain and/or a pelvic mass. On sonography, peritoneal inclusion cysts are multiloculated cystic adnexal masses, often with a bizarre shape frequently described as a spider web pattern63 (Fig. 16.9). The diagnostic finding is the presence of an intact ovary positioned eccentrically amid septations and fluid.60-62 The septations represent mesothelial and fibrous strands. The fluid is usually anechoic but may contain echoes in some compartments as a result of hemorrhage or proteinaceous fluid. Doppler evaluation may demonstrate vascularity within septations, at times mimicking a malignancy. Peritoneal inclusion cysts must be differentiated from other extraovarian conditions such as parovarian cysts and a hydrosalpinx. Paraovarian cysts are separate from the ovary, whereas

FIG. 16.9  Peritoneal Inclusion Cyst.  TVS image shows a multilocular cyst with linear septations attached to the right ovary that projects within the structure and contains a hemorrhagic cyst. This represents adhesions attached to the right ovary.

the ovary lies inside a peritoneal inclusion cyst. Parovarian cysts are usually round or ovoid and not associated with a history of pelvic surgery, trauma, or inflammation. A hydrosalpinx appears as a tubular or ovoid cystic structure often with visible folds, and the ovary is demonstrated as a separate entity. Accurate diagnosis of peritoneal inclusion cysts is important because the risk of recurrence after surgical resection is 30% to 50%.64 Conservative therapy, such as ovarian suppression with oral contraceptives or fluid aspiration, is recommended.62

Polycystic Ovarian Syndrome Polycystic ovarian syndrome (PCOS) is now known to be a multifaceted endocrinologic disorder of ovarian dysfunction that includes abnormal estrogen and/or androgen production resulting in chronic anovulation and hyperandrogenism. Pathologically, the ovaries contain an increased number of follicles in various stages of maturation and atresia, and increased local concentration of androgens produces stromal abnormality. PCOS is a common cause of infertility and a higher-than-usual rate of early pregnancy loss.65,66 Clinical manifestations of PCOS range from mild signs of hyperandrogenism in thin, normally menstruating women to the classic Stein-Leventhal syndrome (oligomenorrhea or amenorrhea, hirsutism, and obesity). The typical sonographic findings of PCOS are bilaterally enlarged ovaries containing multiple small, 2- to 9-mm follicles and increased stromal echogenicity (Fig. 16.10). The ovaries have a rounded shape, with the follicles usually located peripherally (“string of pearls”), although they can also occur randomly throughout the ovarian parenchyma. Because of its superior resolution, TVS is more sensitive than TAS in detecting the small follicles. However, many women with PCOS will not have these typical sonographic findings. Ovarian volume may be normal in 30% of patients.67,68 Using TVS, increased stromal echogenicity has also been reported as a sensitive and specific sign of polycystic ovaries.69,70 In a small number of patients, the sonographic findings may be unilateral.66,71

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FIG. 16.10  Polycystic Ovaries: Typical Appearance on TVS in Woman With Hirsutism and Oligomenorrhea.  (A) and (B) Enlarged ovaries (cursors) with mildly increased stromal echogenicity and multiple peripheral follicles, “string of pearls” sign.

A 2003 consensus meeting of the American Society for Reproductive Medicine and European Society of Human Reproduction and Embryology defined PCOS as requiring two of three criteria: (1) oligo-ovulation and/or anovulation, (2) hyperandrogenism (clinical and/or biochemical), and (3) polycystic ovaries.72 An elevated serum luteinizing hormone (LH) level and insulin resistance have also been characteristic features. Historically, an elevated serum LH level and elevated LH/FSH ratio had been used as diagnostic tools. However, based on data that include the variability of LH depending on proximity to ovulation and its questionable importance in management, recommendations no longer support its necessity for clinical diagnosis.73 According to decisions made at the 2003 Rotterdam consensus workshop, the sonographic findings of polycystic ovaries should include either 12 or more follicles within the entire ovary measuring 2 to 9 mm in diameter72 or increased ovarian volume greater than 10 mL. Although increased stromal echogenicity has been considered specific for polycystic ovaries, because of its subjective nature it was not included in the criteria. The consensus makers thought that measurement of ovarian volume worked as well as stromal evaluation in clinical practice. These criteria are not considered valid if the patient is taking oral contraceptives or has a dominant follicle greater than 10 mm. More recently, it has been reported that with the use of newer, higher resolution ultrasound technology and an offline reliable grid system to count follicles, a significantly higher follicle count threshold within the entire ovary is necessary to support the diagnosis of PCOS. Lujan et al.74 advocated the use of a count of 26 and Christ et al.75 a count of 28 follicles measuring 2 to 9 mm within the entire ovary as a better predictor of PCOS. Because anovulation plays a key role in this disorder, the follicles will persist on serial studies. Long-term follow-up is recommended in patients with PCOS because the resulting high-unopposed estrogen levels can be associated with an increased risk of endometrial and breast carcinoma.

Endometriosis Endometriosis is considered the most common benign gynecologic disorder. It is estimated that endometriosis affects between 5% and 45% of women in the reproductive age group, causes significant morbidity, and represents a major public health concern.76,77 Clinical symptoms include pelvic pain, dysmenorrhea, dyspareunia, dyschezia, urinary symptoms, and infertility.78 The process is defined as the presence of functioning endometrial tissue outside the uterus. Endometriosis may present in different forms that include adnexal cysts (endometriomas), peritoneal plaques and adhesions, and deep infiltrating endometriosis consisting of implants or nodules that contain glands and stroma. Besides the ovary, the most commonly involved areas in the pelvis are the fallopian tube, broad ligament, and posterior cul-de-sac, but endometriosis can occur almost anywhere in the body, including the bladder and bowel. The correct diagnosis and evaluation of the extent of disease are key in determining the best treatment approach. Ultrasound is well accepted as the initial imaging modality of choice, whereas MRI is considered the problem-solving tool. The most common manifestation of endometriotic tissue is the endometrioma, which is readily diagnosed by its appearance sonographically with diffuse homogenous low level internal echoes. Endometriomas, often referred to as chocolate cysts, are frequently multiple, with a variety of appearances, from an anechoic cyst to a solid-appearing mass caused by the degradation of blood products over time.79 The characteristic sonographic appearance is that of a well-defined, unilocular or multilocular, predominantly cystic mass containing diffuse, homogeneous, low-level internal echoes (Fig. 16.11, Video 16.3).80 Color Doppler typically shows little if any vascularity within cyst walls (as opposed to the corpus luteum, which typically has pronounced flow). The low-level internal echoes may be seen diffusely throughout the mass or in the dependent portion. Occasionally, a fluid-fluid level may be seen, particularly if the woman has been lying in a similar position for sufficient time for the blood

CHAPTER 16  The Adnexa

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FIG. 16.11  Endometriosis: Spectrum of Appearances.  TVS images. (A)-(D) Uniform low-level echoes within a cystic ovarian mass. (A) Typical peripheral echogenic foci. (B) Fluid-fluid level. (C) Avascular marginal echogenic nodules. (D) Bilateral disease. (E) Deep penetrating implant on posterior surface of uterus (arrows). (F) Filling the pouch of Douglas (arrows). U, Uterus. See also Videos 16.3, 16.4, and 16.5.

products to settle into layers. In a retrospective study, Patel et al.81 found diffuse, low-level internal echoes in 95% of endometriomas. They concluded that this finding in the absence of neoplastic features is highly likely to be an endometrioma, especially if multilocularity or hyperechoic wall foci are present, whereas an endometrioma is highly unlikely when no component of the mass contains low-level echoes. A prospective study by Dogan et al.82 found a positive predictive value of 97% for typically appearing endometriomas with low-level internal echoes, regular margins, round shape, and thick walls. Differentiation of endometriosis from benign and malignant neoplasms is occasionally required. Papillary wall projections have been frequently described. Patel et al. demonstrated small, linear, hyperechoic foci sometimes present in the wall of the cyst that were thought to represent cholesterol deposits accumulating in the cyst wall.81 Guerriero et al.83 described papillations projecting within the cyst with a height of greater than 3 mm and no internal Doppler flow that were felt to represent adjacent fibrin or blood products (Video 16.4). In rare cases in pregnant women, decidualization of the wall of an endometrioma may occur, resulting in a solid vascular mural mass that cannot be differentiated from malignancy84,85 (Fig. 16.12). Calcification is occasionally present in an endometrioma and can be confused with a dermoid.86 Endometriomas may serve as precursors of borderline endometrioid and clear cell tumors that may eventually become low-grade invasive carcinoma and therefore, if not surgically removed, these are followed yearly.50,87

Endometriomas may be present in postmenopausal women, although their appearance generally differs. Instead of the unilocular cyst containing low-level echoes, the postmenopausal endometrioma more often has the appearance of a multilocular mass. When cyst fluid is present, it is more frequently anechoic or comprised of a more heterogeneous echogenicity.88 The appearance of an endometrioma may be similar to a hemorrhagic ovarian cyst because both are cystic masses that contain blood products of variable age. However, a hemorrhagic cyst more frequently demonstrates a reticular internal pattern rather than the pattern of homogeneous low-level echoes and is more frequently associated with free fluid in the cul-de-sac. A hemorrhagic cyst will resolve or show a significant decrease in size over the next few menstrual cycles, whereas endometriomas tend to show little change in size and internal echo pattern. Clinically, most women with a symptomatic hemorrhagic cyst present with acute pelvic pain, whereas women with an endometrioma have more chronic discomfort associated with their menses. Endometriosis is frequently accompanied by the presence of pelvic adhesions. The evaluation of adhesions of the uterus and ovaries as well as obliteration of the pouch of Douglas can be challenging with ultrasound although techniques have been reported that can be performed successfully by experienced operators.89,90 Movement of the normally mobile uterus and ovaries by abdominal palpation or pressure with the abdominal probe can show adherence of these structures to the adjacent

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FIG. 16.12  Decidualization of Endometrioma in Pregnancy.  (A) and (B) Sagittal gray-scale and color Doppler TVS images of a cyst containing low-level echoes and a peripheral echogenic nodule. The nodule demonstrates color Doppler flow, a finding seen in a borderline neoplasm or a decidualized endometrioma in a pregnant patient.

broad ligament, pouch of Douglas, bladder, rectum, or peritoneum. The use of the sliding sign on TVS has been described to diagnose the obliteration of the pouch of Douglas.91,92 This procedure entails the placement of gentle pressure against the cervix with the TVS probe to determine if the posterior cervix slides easily along the anterior rectal and vaginal wall. Additionally, if fluid is present within the pelvis, fine linear structures representing adhesions may be seen joining the ovary with attached endometrioma, uterus and cul-de-sac peritoneum. Deep infiltrating endometriosis is the most severe form of the disease although the extent of disease based laparoscopic staging may not correlate with the severity of symptoms.78 Variable accuracy of TVS in the identification of deep infiltrating endometriosis has been reported. Most implants are found in dependent areas of the pelvis that is divided into the anterior and posterior compartment according to the deep infiltrating endometriosis classification by Chapron et al.93 The anterior compartment is composed of the urinary bladder, and the posterior compartment includes the cul-de-sac, the uterosacral ligament, bowel wall, rectum and recto-sigmoid junction, vagina, and rectovaginal septum. Sonographically, implants appear as hypoechoic nodules or as diffuse or nodular retroperitoneal thickening. Within the bowel wall, the lesion often takes on the appearance of a fusiform swelling (Fig. 16.11E and F, Video 16.5). Few, if any, vessels are apparent using color Doppler evaluation.94-97

Adnexal Torsion Adnexal torsion is a relatively infrequent gynecologic emergency requiring prompt surgical intervention with a reported incidence of 3% in some series. The process primarily affects women of reproductive age or younger and is uncommon in the postmenopausal age group.98,99 Initially, there is twisting of the ovary, the fallopian tube, or both structures, causing venous and lymphatic compromise with resulting ovarian edema and adnexal enlargement. However, until venous and arterial thrombosis has occurred, reperfusion may permit complete recovery. Complete and unalleviated torsion can progress rapidly from interference with

venous and lymphatic drainage to arterial occlusion and eventually necrosis. Torsion may be partial or complete, and acute or chronic. Not infrequently, torsion may be intermittent with periods of spontaneous remission of symptoms. The diagnosis of torsion is complicated by its vague clinical presentation. The most consistent presenting symptom is abdominal and pelvic pain, with other nonspecific signs and symptoms such as fever and nausea and vomiting more variably present. Early diagnosis and intervention prior to infarction permit ovarian preservation and prevent peritonitis. Because the only consistent symptom cited in most studies is abdominal pain, usually intense and progressive, and localized to a lower quadrant, differential considerations include other gynecologic causes such as PID, ovarian cysts, and ectopic pregnancy as well as nongynecologic causes. Although often difficult to palpate, a demonstrable mass may be present. A right-sided predominance also exists that is attributed to the protective presence of the sigmoid colon on the left and the hypermobility of the right-sided cecum. As a result, the presentation of ovarian torsion may mimic that of appendicitis.100,101 Most cases of ovarian torsion (50%-80%) are associated with adnexal pathologic conditions such as ovarian tumors or cysts. This usually involves an ipsilateral ovarian mass 5 to 10 cm in diameter that acts as a fulcrum to potentiate torsion due to increased ovarian volume or weight within adnexal structures. Although associated with a neoplasm in as many as 50% of cases, previous studies have indicated that the lesions are usually benign since the inflammatory and invasive changes caused by malignant lesions may be protective against ovarian mobility.102 It is associated with 1 in 1800 pregnancies, most commonly in the first trimester or immediately postpartum.103 Women undergoing ovulation induction are at high risk secondary to the development of large theca lutein cysts.100 The initial role of sonography in the evaluation of patients at risk for ovarian torsion is to not only diagnose torsion but also exclude other causes of acute abdominal pain such as appendicitis,

CHAPTER 16  The Adnexa PID, ruptured ovarian cyst, and ectopic pregnancy. The most consistent finding of ovarian torsion is an enlarged edematous ovary (Fig. 16.13) or ovarian complex of ovary and adnexal mass. The location of the ovary is frequently medial and superior to its usual location (Fig. 16.14A).104 If the fallopian tube is involved, a hydrosalpinx will usually be demonstrated. Peripherally placed follicles and homogeneous echoes seen centrally consistent with areas of edema within enlarged ovaries have also been reported,105,106 although these descriptors are nonspecific (Video 16.6). Entities such as endometriomas, polycystic ovaries, hemorrhagic cysts, tubo-ovarian complexes, and hyperstimulated ovaries undergoing ovulation induction are often similarly described. The irregular internal texture of the ovary seems to correlate with intraovarian hemorrhage. Free fluid within the cul-de-sac is another nonspecific finding frequently associated with cases of ovarian torsion. The fluid may be a transudate from the ovarian capsule secondary to obstruction of veins and lymphatic vessels.107

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FIG. 16.13  Ovarian Torsion: Doppler Evaluation of Enlarged Ovaries.  TVS color Doppler image of a young woman presenting with acute pelvic pain shows no evidence of color Doppler flow within an enlarged ovary containing irregular parenchyma; flow is demonstrated distally within the iliac artery. See also Video 16.6.

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FIG. 16.14  Ovarian Torsion With Cyst as Fulcrum.  (A) TAS sagittal image of a young woman with acute pain shows a large, simple cyst (C) that lies anterior to the uterus (U) and cephalad to the bladder (B). This unusual position should raise the suspicion of torsion. (B)-(D) Another young female patient who is postpartum presenting with acute pelvic pain. (B) TAS shows a large simple ovarian cyst superior to the uterus. (C) and (D) TAS spectral Doppler images show normal arterial and venous waveforms within the wall of the cyst.

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Doppler findings vary depending on degree of torsion and its chronicity. Lack of arterial and venous Doppler flow should enable confident diagnosis although false positive diagnoses may be obtained as a result of the depth of penetration being greater than the capabilities of the ultrasound beam, improper Doppler or gray-scale priority settings, and too high filter pulse repetition frequency (PRF) settings.108 Thus it is helpful to scan the asymptomatic ovary first to ensure that Doppler settings are appropriate. Conversely, both arterial and venous ovarian spectral Doppler signal has been frequently reported in cases of surgically proven torsion. Absent venous Doppler flow has a positive predictive value as high as 94% for ovarian torsion despite persistence of arterial signal.107 Explanations proposed include venous occlusion leading to symptoms before arterial occlusion occurs and that persistent adnexal arterial flow is related to the dual-ovarian arterial blood supply (ovarian artery and ovarian branches of uterine artery).109 Occasionally, a twisted vascular pedicle (consisting of broad ligament, fallopian tube, and adnexal and ovarian branches of uterine artery and vein) may be demonstrated as a round hyperechoic structure with multiple concentric hypoechoic stripes (target appearance) or as an ellipsoid or tubular structure with internal heterogeneous echoes.110 Using color or power Doppler ultrasound, the presence of circular or coiled twisted vessels within the vascular pedicle (whirlpool sign) is helpful in diagnosing torsion.110 Absence of blood flow within the vascular pedicle suggests a nonviable ovary.110,111 Comparison with the morphologic appearance and flow patterns of the contralateral ovary can also be helpful since decreased or abnormal flow may be present in the torsed ovary.107,112 Massive edema of the ovary is a rare condition resulting from partial or intermittent torsion of the ovary, causing venous and lymphatic obstruction but not arterial occlusion, leading to marked stromal edema. The few cases described in the literature show a large, edematous multicystic adnexal mass.113-115 The use of duplex and color Doppler imaging is most useful in making the diagnosis in the absence of Doppler flow although the presence of Doppler signal cannot eliminate the diagnosis. In the appropriate clinical setting, an enlarged ovary or ovary and adnexal mass complex should suggest torsion even in the presence of ovarian Doppler flow112,116 Torsion is extremely unlikely if the ovary is morphologically normal and of normal size regardless of Doppler findings.

NEOPLASMS Ovarian Cancer Ovarian cancer is the fifth leading cause of cancer death among US women and causes more deaths than any other cancer of the female reproductive system. The American Cancer Society estimated 21,980 new cases of ovarian cancer in the United States in 2014, with about 14,270 deaths.117 Between 1987 and 2010, the incidence decreased at a rate of 0.9% a year.117,118 Ovarian cancer represents approximately 25% of all gynecologic malignancies, with peak incidence in the sixth decade of life. Ovarian cancer has the highest mortality rate of all gynecologic malignancies, mostly a result of late diagnosis. Because there are few

clinical symptoms, 60% to 70% of women have advanced disease (stages III or IV) at diagnosis. The overall 5-year survival rate is 20% to 30%, but with early detection in stage I, the rate rises to 80% to 90%. Therefore efforts have been directed at developing methods of early diagnosis of ovarian cancer. Increasing age, nulliparity, a family history of ovarian cancer, and a patient history of breast, endometrial, or colon cancer are associated with increased risk of ovarian cancer. The lifetime risk of a woman developing ovarian cancer is 1 in 70 (1.4%). However, if a woman has a first-degree relative (mother, daughter, sister) or second-degree relative (aunt or grandmother) who has had ovarian cancer, the risk is 5%. With two or more relatives who have had ovarian cancer, the lifetime risk increases to 7%.119 About 3% to 5% of women with a family history of ovarian cancer have a hereditary ovarian cancer syndrome. The three main hereditary syndromes associated with ovarian cancer are the breast-ovarian cancer syndrome, the most common, caused by mutations in the suppressor genes BRCA1 and BRCA2, with a high frequency of both cancers; the hereditary nonpolyposis colorectal cancer syndrome (Lynch II), in which ovarian cancer occurs in association with nonpolyposis colorectal cancer or endometrial cancer, or both; and site-specific ovarian cancer syndrome, the least common, without an excess of breast or colorectal cancer.120 Hereditary ovarian cancer syndromes are thought to have an autosomal dominant inheritance, and the lifetime risk of ovarian cancer in these patients is 40% to 50%. They have an earlier age of onset (10-15 years earlier) than do other ovarian cancers.120 Therefore oophorectomy is commonly advocated after child-bearing in these women. A number of clinical screening trials of asymptomatic women have been reported using TVS (either alone or in combination with Doppler sonography) and/or biologic markers such as cancer antigen (CA) 125.121-126 CA 125 is a high-molecular-weight glycoprotein recognized by the OC 125 monoclonal antibody. It has proved extremely useful in following the clinical course of patients undergoing chemotherapy and in detecting recurrent subclinical disease.127,128 Although serum CA 125 is elevated in approximately 80% of women with epithelial ovarian cancer, it detects less than 50% of stage I disease and is insensitive to mucinous and germ cell tumors.128 Other malignancies, as well as many benign conditions, are associated with elevated serum CA 125. The use of serum CA 125 and/or sonography as a screening test for ovarian cancer is not currently recommended for routine clinical use.129 Routine screening has resulted in unnecessary surgery with its attendant risks.129 The largest screening trial to date is the United Kingdom Collaborative Trial of Ovarian Cancer Screening (UKCTOCS), a randomized study evaluating annual screening using either TVS or serum CA 125 with TVS as a second-line test (multimodal screening). Preliminary results are encouraging, with superior sensitivity and positive predictive value reported with the multimodal screening strategy compared to TVS alone for detecting primary invasive epithelial ovarian and fallopian tube cancers.130 Histologically, epithelial neoplasms represent 65% to 75% of ovarian tumors and 90% of ovarian malignancies50 (Table 16.1). The remaining neoplasms consist of germ cell tumors (15%-20%), sex cord–stromal tumors (5%-10%), and metastatic

CHAPTER 16  The Adnexa TABLE 16.1  Ovarian Neoplasms Tumor

Incidence

Examples

Surface epithelial– stromal tumors

65%-75%

Germ cell tumors

15%-20%

Sex cord–stromal tumors

5%-10%

Metastatic tumors

5%-10%

Serous cystadenoma/ carcinoma Mucinous cystadenoma/ carcinoma Endometrioid carcinoma Clear cell carcinoma Transitional cell tumor Teratoma Dysgerminoma Yolk sac tumor Granulosa cell tumor Sertoli-Leydig cell tumor Thecoma and fibroma Uterus Stomach, colon, breast Lymphoma

tumors (5%-10%). Sonographically, ovarian cancer usually presents as an adnexal mass. Well-defined anechoic cysts are more likely to be benign, whereas lesions with irregular walls, thick irregular septations, mural nodules, and solid elements with flow are more likely to be malignant.131,132 Many scoring systems and mathematical models based on the morphologic characteristics have been proposed for distinguishing between benign and malignant masses. However, subjective evaluation of the ultrasound morphologic features (pattern recognition) by an experienced interpreting physician has been shown to be the superior method.133,134 Using this method, a physician should be able to distinguish benign from malignant masses in approximately 90% of cases.135 Color and pulsed Doppler sonography have been advocated for distinguishing benign from malignant ovarian masses. Support is based on the premise that malignant masses, because of internal neovascularization, will have high diastolic flow. Malignant tumor growth depends on angiogenesis, with the development of abnormal tumor vessels.136 These abnormal vessels lack smooth muscle within their walls, which, along with arteriovenous shunting, leads to decreased vascular resistance and thus higher diastolic flow velocity. Therefore the pulsatility index (PI) and resistive index (RI) should be lower in malignant lesions. Although many reports have found a tendency for both PI and RI to be lower in malignant lesions, there is too much overlap to differentiate reliably between benign and malignant lesions in individual patients.137-142 Other parameters such as vessel location have been suggested to improve the specificity of Doppler ultrasound assessment of ovarian masses.143 Malignant lesions tend to have more central flow, whereas benign lesions tend to have more peripheral flow. However, Stein et al.138 found considerable overlap, with 21% of malignant lesions having only peripheral flow and 31% of benign lesions having central flow. Guerriero et al.144 found a higher accuracy in predicting malignancy when color Doppler ultrasound demonstrated arterial flow within the solid portions of the mass.

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Studies comparing the morphologic features on sonography with the Doppler findings found that Doppler ultrasound showed no more diagnostic information than morphologic assessment alone.133,139,140,145 Valentin133 concluded that, in experienced hands, morphologic assessment is the best method for discriminating between benign and malignant masses. The main advantage of adding Doppler ultrasound would be to increase the confidence with which a correct diagnosis is made. Others have found that Doppler ultrasound, when added to sonographic morphologic assessment, improves specificity and positive predictive value.142,146148 Brown et al.149 found that a nonhyperechoic solid component was the most statistically significant predictor of malignancy. Schelling et al.150 also found that a solid component in an adnexal mass with central vascularity achieved high accuracy, sensitivity, and specificity in predicting malignancy. A meta-analysis of 46 published studies concluded that ultrasound techniques that combine morphologic assessment with color Doppler flow imaging is significantly better in characterizing ovarian masses than morphologic assessment, color Doppler flow imaging, or Doppler indices alone.151 Doppler ultrasound is probably not needed if the mass has a characteristic benign morphology, because morphologic assessment is highly accurate in this group of lesions.138,141 Doppler ultrasound is likely valuable in assessing the mass that is morphologically indeterminate or suggestive of malignancy. Doppler findings should be combined with morphologic assessment, clinical findings, patient age, and phase of menstrual cycle for optimal evaluation of an adnexal mass.152 Recently, contrast-enhanced TVS (CE-TVS) has been used to evaluate ovarian tumor neovascularity. With dynamic CE-TVS, malignant tumor neovascularity usually demonstrates more prolonged contrast washout compared with benign tumors. The difference in contrast enhancement patterns between benign and malignant ovarian masses results in potential improvement in differentiating benign from malignant lesions with CE-TVS compared with conventional TVS.153

Surface Epithelial–Stromal Tumors In the past, epithelial-stromal tumors were generally considered to arise from the surface epithelium that covers the ovary and the underlying ovarian stroma. It has since been proposed that epithelial ovarian cancer is a collection of diseases arising from varying cells of origin. Evidence suggests that the majority of primary ovarian cancers (in particular, high-grade serous cancers) are derived from the fallopian tube rather than the ovary. A dualistic model that categorizes ovarian cancer into two groups (type I and type II) has been described. Type I tumors usually present at a low stage and include low-grade serous, low-grade endometrioid, clear cell, and mucinous carcinomas. Type II tumors include high-grade serous carcinomas, high-grade endometrioid carcinomas, carcinosarcomas, and undifferentiated carcinomas. Type I tumors tend to be clinically indolent, whereas type II tumors are typically highly aggressive.154,155 Epithelial-stromal tumors can be divided into five broad categories based on epithelial differentiation: serous, mucinous, endometrioid, clear cell, and transitional cell (Brenner).50 This group of tumors accounts for 65% to 75% of all ovarian neoplasms and 80% to 90% of all ovarian malignancies. The mode of spread

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of the malignant tumors is primarily intraperitoneal, although direct extension to contiguous structures can occur. Lymphatic spread is predominantly to the paraortic nodes. Hematogenous spread usually occurs late in the course of the disease.

Serous Cystadenoma and Cystadenocarcinoma Serous tumors are the most common surface epithelial–stromal tumors, representing 30% of all ovarian neoplasms. Approximately 50% to 70% of serous tumors are benign. Serous cystadenomas account for about 25% of all benign ovarian neoplasms, and serous cystadenocarcinomas account for about 50% of all malignant ovarian neoplasms.50 The peak incidence of serous cystadenomas is in the fourth and fifth decades, whereas serous

cystadenocarcinomas most frequently occur in perimenopausal and postmenopausal women. Approximately 20% of benign serous tumors and 50% of malignant serous tumors are bilateral. Their sizes vary greatly, but in general they are smaller than mucinous tumors. Sonographically, serous cystadenomas are usually large, thin-walled cysts. They are typically unilocular, but may contain thin septations (Fig. 16.15A and B). Papillary projections are occasionally seen. Serous cystadenocarcinomas may be quite large and usually present as multilocular cystic masses containing multiple papillary projections arising from the cyst walls and septa (Fig. 16.15G-I) The septa and walls may be thick. Echogenic solid material may be seen within the loculations. Papillary

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FIG. 16.15  Epithelial Ovarian Neoplasms: Spectrum of Appearances.  (A) and (B) Serous cystadenomas. (A) Septations within a cystic mass are fairly thin. (B) Septations are thicker. (C) Serous cystadenoma of low malignant potential. Low-level echogenic particles and mural nodules. (D) and (E) Mucinous cystadenomas. (F) Mucinous cystadenocarcinoma. Large size and septations are characteristic; septal nodularity is marked (arrows). (G)-(I) Patient with serous cystadenocarcinoma. Extensive nodularity shows vascularity, confirming the morphologic suspicion of a malignant mass. There is high diastolic flow resulting in a low resistive index.

CHAPTER 16  The Adnexa

FIG. 16.16  Mucinous Cystadenoma.  Gross pathologic specimen shows multiple cystic loculations.

projections may form on the surface of the cyst and surrounding organs, resulting in fixation of the mass. Ascites is frequently seen.

Mucinous Cystadenoma and Cystadenocarcinoma Mucinous tumors are the second most common ovarian epithelial tumor, accounting for 20% to 25% of ovarian neoplasms. Mucinous cystadenomas constitute 20% to 25% of all benign ovarian neoplasms, and mucinous cystadenocarcinomas make up 5% to 10% of all primary malignant ovarian neoplasms.50 Mucinous cystadenomas occur most often in the third to sixth decades but may be seen in very young women, whereas mucinous cystadenocarcinomas most frequently occur in the fourth to seventh decades. Mucinous tumors are less frequently bilateral than their serous counterparts, with only 5% of the benign and 15% to 20% of the malignant lesions occurring on both sides. A high percentage, 80% to 85%, of mucinous tumors are benign.156 Mucinous cystadenomas can be huge cystic masses, measuring up 30 cm and filling the entire pelvis and abdomen (Figs. 16.15D and E and 16.16). Multiple thin septa are present, and low-level echoes caused by the mucoid material may be seen in the loculations. Papillary projections are less frequently seen than in the serous counterpart. Mucinous cystadenocarcinomas are usually large, multiloculated cystic masses containing papillary projections and echogenic material; they generally have a sonographic appearance similar to that of serous cystadenocarcinomas (Fig. 16.15F). Penetration of the tumor capsule or rupture may lead to intraperitoneal spread of mucin-secreting cells that fill the peritoneal cavity with a gelatinous material. This condition, known as pseudomyxoma peritonei, may be similar sonographically to ascites or may contain multiple septations or floating debris in the fluid that fills much of the pelvis and abdomen. This condition may occur in mucinous cystadenomas and in mucinous cystadenocarcinomas. A ruptured mucocele of the appendix and mucinous tumors of the appendix and colon can also lead to pseudomyxoma peritonei. Borderline (Low Malignant Potential) Tumors There is an intermediate group of epithelial tumors that are histologically categorized as “borderline” or of “low malignant

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potential.” They occur in about 10% to 15% of serous and mucinous tumors. These tumors have cytologic features of malignancy but do not invade the stroma and, although malignant, have a much better prognosis. They present at an earlier age than cystadenocarcinomas and have 5-year and 20-year survival of 95% and 80%, respectively. They may be treated by ovarysparing surgery to preserve fertility. Sonographic features suggestive of low malignant potential tumors are a small- to medium-sized cyst containing low-level echoes (similar to an endometrioma) with vascular mural nodules (Figs. 16.15C) or a cystic mass with a well-defined multilocular (honeycomb) nodule.157,158 Normal ovarian tissue may be seen adjacent to the lesion and may be helpful in excluding invasive ovarian cancer.157,159 This has been referred to as the ovarian crescent sign.159 Although the presence of this sign decreases the likelihood of invasive adnexal malignancy, it was found to be a poor discriminator between benign and malignant adnexal masses in a prospective study by Van Holsbeke et al.160

Endometrioid Tumor Almost all endometrioid tumors are malignant. They are the second most common epithelial malignancy, representing 20% to 25% of ovarian malignancies; 25% to 30% are bilateral, and they occur most frequently in the fifth and sixth decades. Their histologic characteristics are identical to those of endometrial adenocarcinoma, and approximately 30% of patients have associated endometrial adenocarcinoma, which is thought to represent an independent primary tumor. Approximately 15% to 20% of endometrioid cancer is associated with endometriosis, which may occur within the endometriosis, the ipsilateral or contralateral ovary.50 The endometrioid tumor has a better prognosis than other epithelial malignancies, probably related to diagnosis at an earlier stage. Sonographically, it usually presents as a cystic mass containing papillary projections, although some endometrioid tumors are predominantly a solid mass that may contain areas of hemorrhage or necrosis.156 Clear Cell Tumor This tumor is considered to be of müllerian duct origin and a variant of endometrioid carcinoma. Clear cell tumor is almost always malignant and constitutes 5% to 10% of primary ovarian carcinomas. It occurs most frequently in the fifth to seventh decades and is bilateral in about 20% of patients. Associated pelvic endometriosis is present in 50% to 70% of clear cell carcinomas, and approximately one-third arise within the lining of endometriomas.50 Sonographically, it usually presents as a nonspecific, complex, predominantly cystic mass (Fig. 16.17, Video 16.7).156 Transitional Cell Tumor Also known as Brenner tumor, transitional cell tumor is derived from the surface epithelium that undergoes metaplasia to form typical uroepithelial-like components.156 It is uncommon, accounting for 2% to 3% of all ovarian neoplasms, and is almost always benign; 6% to 7% are bilateral. Most patients are asymptomatic, and the tumor is discovered incidentally on sonographic examination or at surgery. About 30% are associated with cystic neoplasms,

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Abdominal and Pelvic Sonography neoplasms, with 95% being benign cystic teratomas (dermoids). The others, including dysgerminomas and endodermal sinus (yolk sac) tumors, occur mainly in children and young adults and are almost always malignant. Germ cell tumors are the most common ovarian malignancies in children and young adults. When a large, predominantly solid ovarian mass is present in a girl or young woman, the diagnosis of a malignant germ cell tumor should be strongly considered163 (Video 16.8).

FIG. 16.17  Clear Cell Carcinoma in Endometrioma.  TVS shows a complex cyst with homogenous low-level internal echoes centrally and solid nodules peripherally. See also Video 16.7

C

Cystic Teratoma Cystic teratomas make up approximately 15% to 25% of ovarian neoplasms; 10% to 15% are bilateral. They are composed of well-differentiated derivatives of the three germ layers: ectoderm, mesoderm, and endoderm. Because ectodermal elements generally predominate, cystic teratomas are virtually always benign. Cystic teratomas are frequently seen in the reproductive years but can occur at any age and can be seen in postmenopausal women. These tumors may present as a palpable mass. Cystic teratomas are usually asymptomatic and often are discovered incidentally during sonography. In approximately 10% of cases, the tumor is diagnosed during pregnancy.50 Torsion is the most common complication, whereas rupture is uncommon, occurring in 1% of patients and causing a secondary chemical peritonitis. Malignant transformation is also uncommon, occurring in 2% of patients, usually older women,50 and is almost exclusively due to squamous cell carcinoma.28 Sonographically, cystic teratomas have a variable appearance ranging from completely anechoic to completely hyperechoic. However, certain features are considered specific (Fig. 16.19). These include a predominantly cystic mass with a highly echogenic mural nodule, the dermoid plug.164 The dermoid plug usually contains hair, teeth, or fat and frequently casts an acoustic shadow. In many cases the cystic component is pure sebum (which is liquid at body temperature) rather than simple fluid.165 Cystic Teratomas: Sonographic Features

FIG. 16.18  Transitional Cell (Brenner) Tumor in Wall of Mucinous Cystadenoma.  TAS shows a large, well-defined cystic mass (C) with a solid hypoechoic mural nodule (arrow). Pathologic examination showed a Brenner tumor within the wall of a large, mucinous cystadenoma.

usually serous or mucinous cystadenomas or cystic teratomas, frequently in the ipsilateral ovary161 (Fig. 16.18). Sonographically, Brenner tumors are hypoechoic solid masses. Calcification may occur in the outer wall. A cystic component is uncommon, but when present, usually results from a coexistent cystadenoma.156,162 Pathologically, transitional cell masses are solid tumors composed of dense fibrous stroma. They appear similar to ovarian fibromas and thecomas and to uterine leiomyomas, both sonographically and pathologically.

Germ Cell Tumors Germ cell tumors are derived from the primitive germ cells of the embryonic gonad. They account for 15% to 20% of ovarian

Dermoid plug “Tip of the iceberg” sign Dermoid mesh Mobile spherules (rare) Fat-fluid level

A mixture of matted hair and sebum is highly echogenic because of multiple tissue interfaces, and it produces poorly defined acoustic shadowing that obscures the posterior wall of the lesion. This has been termed the “tip of the iceberg” sign166 (Fig. 16.19B). Highly echogenic foci with well-defined acoustic shadowing may arise from other elements, including teeth and bone. Multiple linear hyperechogenic interfaces, often described as lines and dots, may be seen floating within the cyst and have been shown to be hair fibers.167 This is also considered a specific sign and has been referred to as the dermoid mesh168 (Fig. 16.19G). A fat-fluid or hair-fluid level may also be seen (Fig. 16.19D and E). In most cases, as in other lesions such as endometriomas and hemorrhagic cysts, the dependent layer will be more echogenic. However, in approximately 30% of dermoids,

CHAPTER 16  The Adnexa

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FIG. 16.19  Dermoid Cysts: Spectrum of Appearances.  (A) Small, highly echogenic mass in an otherwise normal ovary. (B) Transverse TAS shows the uterus (U). In the right adnexal region, there is a highly echogenic and attenuating mass (arrows), the “tip of the iceberg” sign. (C) Highly echogenic intraovarian mass with no normal ovarian tissue. (D) Mass of varying echogenicity with hair-fluid level (straight arrow) and highly echogenic, fat-containing dermoid plug (curved arrow) with shadowing. (E) Mass with fat-fluid level (arrow), with dependent layer more echogenic. (F) Mass containing uniform echoes, small cystic area, and calcification (arrows) with shadowing. (G) Combination of dermoid mesh and dermoid plug appearances. (H) Dermoid mesh, multiple linear hyperechogenic interfaces (lines and dots) floating within cystic mass. (I) Multiple mobile spherical echogenic structures floating in a large, cystic pelvic mass.

the nondependent layer will be more echogenic.169 Another rare but characteristic feature is multiple mobile spherical echogenic structures floating in a large, cystic pelvic mass170 (Fig. 16.19I). These spheres are typically composed of desquamative keratincontaining fibrin, hemosiderin, and hair. Patel et al.171 found that an adnexal mass showing two or more characteristic sonographic dermoid features had a positive predictive value of 100%. Pitfalls in the diagnosis of cystic teratomas have been described.172 Acute hemorrhage into an ovarian

cyst or an endometrioma may be so echogenic that it resembles a dermoid plug. However, posterior sound enhancement is usually seen with acute hemorrhage, whereas the dermoid plug tends to attenuate sound. Other pitfalls include pedunculated fibroids, especially lipoleiomyomas, and perforated appendicitis with an appendicolith. An echogenic dermoid may appear similar to bowel gas and may be overlooked. If a definite pelvic mass is clinically palpable and the sonogram appears normal, the patient should be reexamined, to carefully assess for a dermoid.

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Doppler evaluation of a benign teratoma may show peripheral flow, but malignancy should be considered if flow is seen centrally and/or within solid areas. Additional findings suggesting malignancy include isoechoic branching structures within the lesion and invasion into adjacent organs.28 Struma ovarii is a teratoma composed entirely or predominantly of thyroid tissue. It occurs in 2% to 3% of teratomas. Color Doppler sonography detected central blood flow in solid tissue in four reported cases of struma ovarii, compared with absent central blood flow in benign cystic teratomas.173 This is likely caused by the highly vascularized thyroid tissue in struma ovarii, compared with the avascular fat and hair found in benign cystic teratomas. Although associated hormonal effects are rare, sonography may be valuable in identifying a pelvic lesion in a hyperthyroid patient when there is no evidence of a thyroid lesion in the neck.174 Immature teratoma is uncommon, representing less than 1% of all teratomas, and contains immature tissue from all three germ-cell layers. It is a rapidly growing malignant tumor that most often occurs in the first two decades of life. Sonographically,

the tumor usually presents as a solid mass, but cystic structures of varying size may also be seen.163 Calcifications are typically present.

Dysgerminoma Dysgerminomas are malignant germ cell tumors that constitute 1% to 2% of primary ovarian neoplasms and 3% to 5% of ovarian malignancies.50 They are composed of undifferentiated germ cells and are morphologically identical to the male testicular seminoma. Dysgerminomas are highly radiosensitive and have a 5-year survival of 75% to 90%. This tumor occurs predominantly in women younger than 30 years and is bilateral in approximately 15% of cases. Sonographically, they are solid masses that are predominantly echogenic but that may contain small anechoic areas caused by hemorrhage or necrosis163 (Fig. 16.20). CT and MRI have shown these solid masses to be lobulated with fibrovascular septa between the lobules.175 A report using color Doppler ultrasound in three dysgerminomas showed prominent arterial flow within the fibrovascular septa of a multilobulated, solid, echogenic mass.176

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FIG. 16.20  Dysgerminomas in Three Young Women.  (A) Transverse TAS shows large, solid pelvic mass (M) adjacent to the uterus (U). This appearance could be easily confused with a uterine fibroid. (B) TVS shows large solid ovarian mass with thin linear hyperechoic areas. (C) Transverse TAS shows large bilateral ovarian masses with increased vascularity seen in the right-sided tumor, which extends over the uterus (U). Note also the enlarged left ovary (L) due to tumor. See also Video 16.8.

CHAPTER 16  The Adnexa Yolk Sac Tumor This rare, rapidly growing tumor, also called endodermal sinus tumor, is the second most common malignant ovarian germ cell neoplasm after dysgerminoma. Yolk sac tumor has a poor prognosis. It is thought to arise from the undifferentiated, multipotential embryonal carcinoma by selective differentiation toward yolk sac or vitelline structures.50 It usually occurs in females under 20 years of age and is almost always unilateral. Increased levels of serum alpha-fetoprotein may be seen in association with endodermal sinus tumor. The sonographic appearance is similar to that of the dysgerminoma163 (see Video 16.8).

Sex Cord–Stromal Tumors Sex cord–stromal tumors arise from the sex cords of the embryonic gonad and from the ovarian stroma. The main tumors in this group include granulosa cell tumor, Sertoli-Leydig cell tumor (androblastoma), thecoma, and fibroma. This group accounts for 5% to 10% of all ovarian neoplasms and 2% of all ovarian malignancies.

Granulosa Cell Tumor Representing 1% to 2% of ovarian neoplasms, granulosa cell tumor has a low malignant potential. About 95% are of the adult type and occur predominantly in postmenopausal women; almost all are unilateral. Granulosa cell tumors are the most common estrogenically active ovarian tumor,50 and clinical signs of estrogen production can occur, including development of endometrial carcinoma (in 10%-15%). The juvenile type makes up 5% of granulosa cell tumors, occurring mainly in patients younger than 30 years. Granulosa cell tumors have a variable appearance, ranging from small solid masses to tumors with variable degrees of hemorrhage or fibrotic changes, to multilocular cystic lesions.177 Sertoli-Leydig Cell Tumor This rare tumor, also called androblastoma and arrhenoblastoma, constitutes less than 0.5% of ovarian neoplasms. It generally occurs in women younger than 30 years of age; almost all are unilateral. Malignancy occurs in 10% to 20% of these tumors. The malignant tumors tend to recur relatively soon after initial diagnosis, with few recurrences after 5 years.178 Clinically, signs and symptoms of virilization occur in about 30% of patients, although about half will have no endocrine manifestations.50 Occasionally, these tumors may be associated with estrogen production. Sonographically, Sertoli-Leydig cell tumors usually appear as solid hypoechoic masses or may be similar in appearance to granulosa cell tumors.178 Thecoma and Fibroma Thecoma and fibroma arise from the ovarian stroma and may be difficult to distinguish from each other pathologically. Tumors with an abundance of thecal cells are classified as thecomas, whereas those with fewer thecal cells and abundant fibrous tissue are classified as thecofibromas and fibromas. Thecomas constitute approximately 1% of all ovarian neoplasms, and 70% occur in postmenopausal females. They are unilateral, almost always benign, and frequently show clinical signs of estrogen production.

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Fibromas represent about 4% of ovarian neoplasms, are benign, usually unilateral, and occur most often in perimenopausal and postmenopausal women. Unlike thecomas, fibromas are rarely associated with estrogen production and therefore are frequently asymptomatic, despite reaching a large size. Ascites is present in up to 50% of patients with fibromas larger than 5 cm in diameter.179 Meigs syndrome (associated ascites and pleural effusion) occurs in 1% to 3% of patients with ovarian fibromas but is not specific, having been reported in association with other ovarian neoplasms as well. Fibromas also occur in approximately 17% of patients with the basal cell nevus (Gorlin) syndrome. In this condition the fibromas are usually bilateral, calcified, and occur in younger women (mean age, 30 years).178 Sonographically, these tumors have a characteristic appearance of a fibrous lesion (Fig. 16.21). A hypoechoic mass with marked posterior attenuation of the sound beam is seen.179 The main differential diagnosis is a pedunculated uterine fibroid. Not all fibromas and thecomas show this characteristic appearance, and a variety of sonographic appearances have been noted, probably because edema and cystic degeneration tend to occur within these tumors.180

Metastatic Tumors About 5% to 10% of ovarian neoplasms are metastatic in origin. The most common primary sites of ovarian metastases are tumors of the breast and gastrointestinal tract. The term Krukenberg tumor should be reserved for those tumors containing the typical mucin-secreting “signet ring” cells, usually of gastric or colonic origin. Endometrial carcinoma frequently metastasizes to the ovary, but it may be difficult to distinguish from primary endometrioid carcinoma, as discussed earlier. Sonographically, ovarian metastases are usually bilateral solid masses (Fig. 16.22A-C), but they may become necrotic and may have a complex, predominantly cystic appearance that simulates primary cystadenocarcinoma181,182 Testa et al.183 found that almost all ovarian metastases from primary tumors of the breast, stomach, and uterus were solid, whereas those from the colon and rectum were more heterogeneous, most being multicystic with irregular borders. Ascites may be seen in either primary or metastatic tumors. Lymphoma may involve the ovary, usually in a diffuse, disseminated form that is frequently bilateral. The sonographic appearance is that of a solid hypoechoic mass similar to lymphoma elsewhere in the body (Fig. 16.22D-F).

FALLOPIAN TUBE With careful TVS examination, a normal fallopian tube may be identified as an undulating structure measuring less than 10 mm in thickness that extends from the uterine cornu posterolaterally to the ipsilateral ovary. This assessment is not included as part of a routine pelvic sonogram. Identification becomes easier when the fallopian tube is dilated or surrounded by fluid. The contour of the lumen is not seen unless it is obstructed and fluid-filled184 (Fig. 16.23). Diagnosis of an asymptomatic hydrosalpinx is important because it allows for what might otherwise be considered to be a concerning adnexal cyst to be ignored rather than followed (Videos 16.9 and 16.10). Developmental

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FIG. 16.21  Ovarian Fibroma.  (A) and (B) TVS gray-scale and spectral Doppler images. (A) Hypoechoic mass with some posterior attenuation. (B) Spectral Doppler evaluation of the mass demonstrates internal flow confirming a solid mass. (C) Pathologic specimen shows the homogeneous, solid nature of a fibroma. (A and B courtesy of Mindy Horrow MD, Einstein Medical Center.)

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FIG. 16.22  Solid Malignant Adnexal Masses in Two Patients: Metastatic Disease and Lymphoma.  (A)-(C) Bilateral solid ovarian masses or Krukenberg tumors in young woman with colon cancer (A and B, right ovary; C, left ovary). (D)-(F) Bilateral predominantly solid masses in young woman with lymphoma (D and E, right ovary; F, left ovary).

CHAPTER 16  The Adnexa

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FIG. 16.23  Hydrosalpinx.  TVS images show tubular fluid-filled structures with sonographic characteristics of the fallopian tube. (A) Incomplete septation related to the folding of the tube (arrows). (B) A waist sign also associated with tubal folds (arrows) and endosalpingeal folds forming surface nodularities. See also Videos 16.9 and 16.10.

abnormalities of the fallopian tube are rare. Abnormalities of the tube include pregnancy, infection, torsion, and neoplasm as well as scarring and obstruction due to other causes.

Pelvic Inflammatory Disease PID is a common condition that is increasing in frequency. It consists of inflammation of the endometrium, fallopian tubes, pelvic peritoneum, and adjacent structures. Typically, the primary infection is a sexually transmitted disease most often associated with gonorrhea and chlamydia, although with previous disruption of endometrial and tubal tissue due to prior infection, or postsurgical or postpartum changes, the patient can be infected by her own vaginal flora. The infection typically spreads by ascent from the cervix and endometrium. The disease is manifested by tuboovarian complexes, peritonitis, and abscess formation and is usually bilateral. Long-term sequelae include chronic pelvic pain, infertility, and increased risk of ectopic pregnancy. Less common causes include direct extension from appendiceal, diverticular, or postsurgical abscesses that have ruptured into the pelvis, as well as puerperal and postabortion complications. Hematogenous spread is rare but can occur from tuberculosis. When caused by direct extension of an adjacent inflammatory process, it is most often unilateral. The presence of an intrauterine device (IUD) increases the risk of PID, although only during a period of a few weeks following its placement. PID may be unilateral in patients with IUDs. Patients usually present clinically with pain, fever, cervical motion tenderness, and vaginal discharge. A pelvic mass may be palpated. TVS with color or power Doppler is highly specific in the diagnosis of the disease process.185 However, because the success of the technique is dependent on the level of operator expertise and also because early changes can be subtle, TVS usually only detects complications of the disease. The sonographic findings may be normal early in the course of PID.186 Increased echogenicity of peritoneal fat and indistinctness of the uterus may be seen early in the disease process but may be difficult to appreciate. Sonographic findings of the fallopian tubes are the most specific and conspicuous indicators of PID (Table 16.2).

TABLE 16.2  Sonographic Findings of Pelvic Inflammatory Disease Endometritis Purulent material in cul-de-sac Periovarian inflammation Salpingitis

Tubo-ovarian complex Tubo-ovarian abscess

Endometrial thickening Intracavitary fluid Fluid containing low-level echoes Enlarged ovaries with multiple cysts and indistinct margins Fluid-filled fallopian tube with (pyosalpinx) or without (hydrosalpinx) internal echoes Increased echogenicity of peritoneal fat Indistinctness of the uterus Fusion of inflamed, fluid-distended tube and ovary Multiloculated mass with variable septations, irregular margins, and low-level internal echoes

When imaging a normal appearing fallopian tube, hypervascularity with color Doppler flow within the tubal wall is a valuable early finding. As the disease progresses, a spectrum of findings may occur (Fig. 16.24). With inflammation, the tube swells and endosalpingeal folds thicken. With progressive inflammation and distal occlusion of the lumen, the tube fills with purulent echogenic fluid, becoming a pyosalpinx. In the presence of a fluid-distended fallopian tube, common findings include wall thickness greater than 5 mm, incomplete septa seen as the tube folds back on itself, and thickening of endosalpingeal folds (cogwheel sign).187,188 Color or power Doppler allows for detection of hyperemia in the walls and incomplete septi associated with fallopian tube inflammation (Fig. 16.24B).189 On TAS, dilated tubes appear as complex, predominantly cystic masses that are often indistinguishable from other adnexal masses. However, TVS allows for depiction of the fluid-filled tube with a tubular shape, somewhat

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FIG. 16.24  Progression of Pelvic Inflammatory Disease.  (A) TVS gray-scale and (B) color Doppler images show a normal appearing left fallopian tube by gray-scale imaging but markedly increased associated vascularity using color Doppler, consistent with salpingitis. (C) TVS image of a tubo-ovarian complex, a complex mass of fallopian tube and ovary that can still be identified as separate structures. (D) TVS color Doppler image of a tubo-ovarian abscess, a cystic, vascular mass containing thick septations in which the fallopian tube and ovary are no longer identifiable. See also Video 16.11.

folded configuration, and well-defined walls.190 The dilated tube can be distinguished from a fluid-filled bowel loop by the lack of peristalsis. A fluid-pus level may occasionally be seen (Fig. 16.24A). Anechoic fluid within the tube indicates hydrosalpinx. In assessing 14 acute and 60 chronic cases of PID, Timor-Tritsch et al.188 described three appearances of tubal wall structure: (1) cogwheel sign, an anechoic cogwheel-shaped structure visible in the cross section of the tube with thick walls, seen mainly in acute disease; (2) “beads on a string” sign, hyperechoic mural nodules measuring 2 to 3 mm on cross section of the fluid-filled distended tube, caused by degenerated and flattened endosalpingeal fold remnants and seen only in chronic disease; and (3) incomplete septa, hyperechoic septa that originate as a triangular protrusion from one of the walls, but do not reach the opposite wall, seen frequently in both acute and chronic disease and not discriminatory. Patel et al.191 found that the presence of a tubular fluid-filled mass with diametrically opposed indentations in the wall (“waist sign”) had the highest likelihood ratio in discriminating hydrosalpinx from other adnexal masses (Fig. 16.23B).191

Other findings include thick tubal walls and bilateral adnexal masses appearing as small solid masses or thick-walled cystic masses.192 Nonspecific findings of PID include fluid in the endometrial cavity and/or cul-de-sac, and ill-defined ovarian enlargement often. Endometrial thickening or fluid may indicate endometritis. Fluid containing low-level echoes may be demonstrated in the cul-de-sac consistent with purulent material. With progression of disease, there is exudation of pus from the distal fallopian tube, periovarian adhesions may form, with fusion of the inflamed dilated tube and ovary, forming an inflammatory tubo-ovarian complex (Fig. 16.24C, Video 16.11). The ovary is still recognizable but cannot be separated from the tube by applied pressure using the vaginal transducer.186 Further progression results in complete breakdown of tubal and ovarian architecture so that separate structures are no longer identified and there is obscuration of the posterior and lateral margins of the uterus resulting in a tubo-ovarian abscess (Fig. 16.24D). Sonographically, this appears as a multiloculated mass with incomplete septations, irregular margins, and low-level internal

CHAPTER 16  The Adnexa echoes. There is usually posterior acoustic enhancement, and a fluid-debris level or gas may occasionally be seen within the mass. The sonographic appearance may be indistinguishable from other benign and malignant adnexal masses. Clinical correlation is necessary to suggest the correct diagnosis. Regions of identifiable ovarian tissue may be seen within the inflammatory mass by TVS since the ovaries are relatively resistant to infection.3 Both TAS and TVS are useful in making the initial diagnosis in patients with PID and determining management. The TAS approach is helpful in assessing the extent of the disease, whereas the TVS approach is more sensitive in detecting dilated tubes, periovarian inflammatory change, and the internal characteristics of tubo-ovarian abscesses.186,193 However, because of cervical motion tenderness, it may be quite difficult to perform a good quality TVS examination. Although the use of outpatient antibiotic therapy has become the standard of care for mild to moderate cases of PID, according to guidelines from the Centers for Disease Control and Prevention,185 hospitalization for intravenous antibiotic therapy would be prompted by the presence of a tubo-ovarian abscess. By making this diagnosis, TVS is pivotal in determining management. Sonography is also used to follow the disease process following antibiotic therapy. If antibiotic therapy fails, sonographically guided drainage of tubo-ovarian abscesses in combination with antibiotics has been shown to be highly successful.194 This initial approach allows for decreased need for surgical intervention.

Tubal Torsion Tubal torsion is usually seen in conjunction with ovarian torsion, but isolated torsion of the fallopian tube is an infrequent finding. This may be seen in cases of paratubal cysts but also can be seen in association with chronic hydrosalpinx.195 The patient usually presents with sudden onset of severe pelvic pain. Hydrosalpinx and tubal torsion have also been reported as late complications in patients who have undergone tubal ligation.196

Fallopian Tube Carcinoma The fallopian tube is now thought to be the location for the initial development of high-grade serous cystadenocarcinomas.

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Thus whereas fallopian tube cancer used to be considered a rare finding, it is now managed similarly to ovarian cancer. Serous tubal intraepithelial carcinoma, a lesion too small to visualize using imaging modalities, represents the acknowledged precursor of these neoplasms.154 A minority of patients have a profuse watery discharge, known as hydrops tubae profluens. The tumor usually involves the distal end, but it may involve the entire length of the tube. Sonographically, carcinoma of the fallopian tube has been described as a sausage-shaped, solid, or cystic mass with papillary projections.197-200 Patlas et al.201 stated that this diagnosis should be considered when a solid vascular mass corresponding to the expected location of the fallopian tube is seen in association with normal ovaries, especially if the mass is mobile.201

VASCULAR ABNORMALITIES IN THE ADNEXA Ovarian Vein Thrombosis or Thrombophlebitis Ovarian vein thrombosis or thrombophlebitis is an uncommon condition that is usually seen 48 to 96 hours postpartum (Fig. 16.25). Symptoms include fever, lower abdominal pain, and a palpable mass. The underlying cause is venous stasis and spread of bacterial infection from endometritis. The right ovarian vein is involved in 90% of cases. Retrograde venous flow occurs in the left ovarian vein during the puerperium, which protects this side from bacterial spread from the uterus.50 The condition may be diagnosed by sonography although CT and MRI usually perform better in this diagnosis.202,203 Sonography may demonstrate an inflammatory mass lateral to the uterus and anterior to the psoas muscle. The ovarian vein may be seen as a tubular structure directed cephalad from the mass and containing echogenic thrombus. The thrombus usually affects the most cephalic portion of the right ovarian vein and can be demonstrated sonographically at the junction of the right ovarian vein with the inferior vena cava, sometimes extending into the inferior vena cava.204 Doppler ultrasound will demonstrate complete or

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FIG. 16.25  Ovarian Vein Thrombophlebitis.  (A) Transverse gray-scale and (B) color Doppler images of the right ovarian vein containing echogenic material representing thrombus. Color Doppler image shows Doppler signal surrounding the thrombus.

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FIG. 16.26  Pelvic Congestion Syndrome.  Transverse TVS images, (A) without and (B) with color Doppler, of the left adnexa demonstrating multiple large vascular structures consistent with varices.

partial absence of flow in these veins.205 Most patients respond to anticoagulant and antibiotic therapy, and follow-up sonography may show resolution of the thrombus and normal flow by duplex and color Doppler imaging.

Pelvic Congestion Syndrome Pelvic congestion syndrome is a condition that consists of dilatation of pelvic veins (pelvic varices) and reduced venous return causing dull chronic pain that is exacerbated by prolonged standing and relieved by lying down and elevating the legs. Although venography remains the reference standard for diagnosis, sonography can demonstrate an ovarian vein diameter of greater than 5 to 10 mm with reflux, uterine vein engorgement, congestion of ovarian plexuses (tortuous and dilated pelvic venous plexuses in the adnexa with individual varices measuring greater than 5 mm in diameter, Fig. 16.26), filling of the pelvic veins across the midline, or filling of vulvovaginal and thigh varicosities.206 Dilated arcuate veins may also be seen crossing the myometrium. Spectral Doppler evaluation of ovarian veins may demonstrate reversed caudal flow.

SONOGRAPHIC EVALUATION OF AN ADNEXAL MASS IN ADULT WOMEN Sonography in the setting of certain clinical features is often used to evaluate an ovarian/adnexal mass. Clinical features to be considered when evaluating an adnexal mass include symptoms, patient age, menstrual status, and family history. Comparison with previous examinations, if available, is often critical and may save the patient a surgical intervention, since many of these masses are hormonally driven and will resolve. A prior study will also demonstrate if there has been any change in size or internal characteristics. When a mass is found by sonography, it should be characterized by the following: • Location (intraovarian or extraovarian) • Size

• External contour (thin or thick walled and regularity of borders) • Internal consistency (cystic unilocular or multilocular with or without solid components, predominantly solid, or solid) Generally, ovarian masses are predominantly cystic, whereas uterine masses are usually solid tumors, benign leiomyomas. Even solid adnexal masses are usually exophytic or interligamentous leiomyomas. Demonstrating a uterine origin by grayscale and color Doppler is diagnostic and excludes a solid ovarian tumor. Occasionally, it may be difficult to determine the exact origin of the mass by sonography in which case MRI may be a problem-solving tool. In 2010 the Society of Radiologists in Ultrasound published results of a consensus conference regarding the reporting and follow-up needed for asymptomatic adnexal cysts (Table 16.3). Use of these guidelines allows for decreased need for follow-up of benign adnexal cysts.207,208 The vast majority of ovarian masses are functional in nature. Ovarian masses that are simple cysts are almost always benign. In premenopausal asymptomatic women, simple cysts or typical hemorrhagic cysts less than 5 cm can be considered functional. The simple adnexal cyst less than or equal to 1 cm in a postmenopausal woman is also very likely benign. These findings should be considered of no clinical significance in asymptomatic women and do not require follow-up. Simple cysts greater than 5 cm in premenopausal women are also likely functional, but resolution should be confirmed with a follow-up examination. In postmenopausal women, simple cysts greater than 1 cm are most often benign cystadenomas or hydrosalpinges or paraovarian/paratubal cysts that demonstrate no significant malignant potential. Cysts that are greater than 7 cm cannot be adequately evaluated sonographically for mural nodules, so MRI or surgical evaluation is recommended.28 Larger masses, especially those greater than 10 cm, and those with solid components have a higher incidence of malignancy. Solid ovarian masses that are not classic for fibromas are typically surgically removed because of association with malignancy. Cystic

CHAPTER 16  The Adnexa TABLE 16.3  Society of Radiologists in Ultrasound Recommendations for Follow-Up of Asymptomatic Adnexal Cysts Patient Population

Description in Report

Recommended Follow-Up

Premenopausal women

Simple or hemorrhagic cysts 3-5 cm

Simple or hemorrhagic cysts > 5 cm, 6 weeks to document resolution Yearly

Postmenopausal Cysts > 1 cm women Any age Hydrosalpinx No follow-up needed Any age Dermoid, Yearly endometrioma With permission from Levine D, Brown DL, Andreotti RF, et al. Management of asymptomatic ovarian and other adnexal cysts imaged at US: Society of Radiologists in Ultrasound Consensus Conference Statement. Radiology. 2010;256(3):943-954.28

masses with solid components may be either benign or malignant and should be further assessed for wall contour, septations, and mural nodules. Irregular borders, thick irregular septations, papillary projections, and echogenic solid nodules favor malignancy. Color and spectral Doppler ultrasound may demonstrate vascularity within the septa or nodules. Although ascites may be associated with benign masses such as the mucinous cystadenoma or fibroma, it is more commonly seen with malignant disease. Malignant ascites often contains echogenic particulate matter. If a pelvic mass is suspected of being malignant, the abdomen should also be evaluated for evidence of ascites and peritoneal implants, obstructive uropathy, lymphadenopathy, and hepatic and splenic metastases. Hepatic and splenic metastases are uncommon in ovarian carcinoma, but when they occur, they are usually peripheral on the surface of the liver or spleen as a result of peritoneal implantation. Hematogenous metastases within the liver or splenic parenchyma may occur late in the course of the disease. Attempts have been made to standardize reporting of adnexal features and preoperatively classify these masses. The largest study to date analyzing features of ovarian and adnexal masses has been performed by the International Ovarian Tumor Analysis (IOTA) group.209 Timmerman et al.210 used these ultrasound-based features to develop simple rules that can correctly classify the majority of masses as benign or malignant (Table 16.4). If one or more of the malignant (M) rules or one or more of the benign (B) rules are present, the mass is classified as benign or malignant. If both M and B rules are present or no rules are present, the mass cannot be classified.

NONGYNECOLOGIC ADNEXAL MASSES Pelvic masses and pseudomasses may not be of gynecologic origin. To make this diagnosis, it is important to visualize the

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TABLE 16.4  Ten Simple Rules for Identifying a Benign or Malignant Tumor Rules for Predicting a Malignant Tumor (M-Rules)

Rules for Predicting a Benign Tumor (B-Rules)

M1 Irregular solid tumor M2 Presence of ascites

B1 Unilocular B2 Presence of solid components where the largest solid component has a largest diameter 100 ms) is detected within the hepatic parenchyma (Fig. 18.10). Within the hilum, no arterial flow is demonstrated, or if periportal arterial collaterals are present, a tardus-parvus waveform may be detected. Therefore demonstration of arterial flow in the hepatic parenchyma does not exclude the presence of hepatic arterial thrombosis, and meticulous inspection of the parenchymal waveform is warranted29,30 (see Fig. 18.10). Occasionally, a false-positive diagnosis of hepatic artery thrombosis can occur with severe hepatic edema, systemic hypotension, and high-grade hepatic artery stenosis.8 In situations with poor visibility of the porta hepatis because of abdominal girth or overlying bowel gas, lack of detectable flow within the hepatic artery should be viewed with caution and confirmed on computed tomography angiography (CTA).

Hepatic Artery Stenosis Hepatic artery stenosis has been reported in up to 11% of transplant recipients and most often occurs at or within a few centimeters of the surgical anastomosis. Risk factors for development of stenosis include faulty surgical technique, clamp injury, rejection, and intimal trauma caused by perfusion catheters.27 Clinically, patients have biliary ischemia and/or abnormal LFT values. Doppler ultrasound can provide direct and indirect evidence of hepatic artery stenosis. Direct evidence involves identifying and localizing a hemodynamically significant narrowing within the vessel. The porta hepatis should be initially screened with color Doppler ultrasound to detect a focal region of color aliasing within the hepatic artery, which indicates high-velocity turbulent flow produced by the stenotic segment. If the stenosis is hemodynamically significant, spectral tracing will reveal peak systolic velocity (PSV) of greater than 2 to 3 m/sec, with associated turbulent flow distally. Indirect evidence of hepatic artery stenosis includes a tardus-parvus waveform anywhere within the hepatic artery (RI < 0.5; AT > 100 ms). This waveform suggests the presence of a more proximally located stenotic region.27 Indirect evidence of stenosis is much more common in clinical practice than documentation of the stenosis itself (Figs. 18.11 and 18.12). The presence of an intraparenchymal tardus-parvus waveform indicates alterations in the intrahepatic arterial bed from impaired arterial perfusion of the liver. Although it is detected most often in patients with hepatic artery stenosis, tardus-parvus waveform may also result from collateral vessels arising from hepatic artery thrombosis or, less frequently, from severe aortoiliac atherosclerosis. Therefore an intraparenchymal tardus-parvus waveform cannot distinguish between hepatic artery stenosis and thrombosis if the hepatic arterial trunk is not visualized and meticulously investigated.31 Mild degrees of hepatic artery narrowing may also be present without Doppler abnormalities. Therefore if clinical suspicion is high, a normal Doppler study should not preclude further

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FIG. 18.9  Bile Duct: Stones.  (A) Sonogram and (B) correlative noncontrast-enhanced CT show the presence of a large obstructing stone (arrow) in the common hepatic duct. (C) Transverse sonogram shows an echogenic focus (arrow) consistent with an intraductal calculus in this patient with recurrent primary sclerosing cholangitis. (D) Corresponding axial SPGR (spoiled gradient echo) T1-weighted pregadolinium-enhanced magnetic resonance image shows intraductal high-frequency signal (arrow) consistent with a stone. (E) Transverse sonogram at level of the common hepatic duct shows a nonshadowing echogenic focus (arrow) in the duct, consistent with a soft stone. (F) Corresponding T2-weighted magnetic resonance image shows a well-defined filling defect (arrow), confirming the presence of a calculus within the proximal common duct.

CHAPTER 18  Organ Transplantation

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FIG. 18.10  Hepatic Artery: Thrombosis in Three Patients.  Patient 1: (A) Transverse sonogram shows a right lobe infarct appearing as a solid-cystic region (arrows), resulting from hepatic arterial thrombosis. (B) Corresponding CT scan shows the infarct as a low-attenuating wedgeshaped region. (C) On spectral Doppler, no flow could be detected in the main hepatic artery. A tardus-parvus waveform detected within the liver indicates an upstream hepatic arterial problem—in this case, hepatic artery thrombosis with collateral arterial vessels supplying the hepatic tissue. Patient 2: (D) Transverse sonogram shows a greatly distended bile duct (arrows) with echogenic material within the lumen secondary to sloughed mucosa and blood. (E) Corresponding CT scan shows dramatically dilated intrahepatic bile ducts (arrows). The biliary necrosis is less well appreciated on CT. (F) Percutaneous cholangiogram shows contrast filling shaggy, intrahepatic ducts with multiple filling defects. The filling defects correspond to the sloughed biliary mucosa. Patient 3: (G) Transverse sonogram demonstrates multiple collateral vessels (arrow) at the porta hepatis. (H) Spectral Doppler sonogram within the liver shows a tardus-parvus waveform. (I) CT angiogram shows occlusion of the hepatic artery (arrow) caused by acute thrombosis. Multiple arterial collateral vessels (arrowheads) are identified, as seen on (G).

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C FIG. 18.11  Hepatic Artery Stenosis: Doppler Features.  (A) Intrahepatic spectral waveform and (B) hepatic artery waveform at porta hepatis show a prolonged acceleration time and low resistance, a tardus-parvus waveform, suggesting an upstream problem. (C) Spectral waveform at the anastomosis shows high-velocity flow greater than 400 cm/sec. The corresponding color Doppler sonogram shows aliasing as turquoise and yellow between the red and blue at the stenosis, with turbulence beyond.

investigation with other cross-sectional techniques, although the stenosis, if detected, may be mild in these patients. Although detection of a tardus-parvus waveform should incite further assessment, false-positive diagnoses can occur, particularly in the early postoperative period (within 48 hour of surgery), possibly because of postoperative edema. In one study, approximately 30% of false-positive tardus-parvus waveforms were idiopathic and not associated with any causative factors.32

Elevated Hepatic Arterial Resistive Index In the early postoperative period, a normal hepatic artery may display a high-resistance arterial flow (RI > 0.8) or a complete lack of flow in diastole (RI = 1.0) on Doppler interrogation. In these patients the flow within the hepatic artery usually returns to normal in a few days. The cause of this waveform is uncertain, although it may be related to older donor age or prolonged cold ischemic time of the graft. RIs may also be higher in normal grafts with an infrarenal aortohepatic anastomosis compared with those grafts with an end-to-end anastomosis. Thus a high RI of the hepatic artery on Doppler assessment frequently has no clinical relevance and should not be misinterpreted as a sign of a hepatic artery abnormality.33,34 Hepatic Artery Pseudoaneurysms Hepatic artery pseudoaneurysms are uncommon complications of transplantation (1%) and occur most frequently at the vascular anastomosis or as a result of prior angioplasty. Intrahepatic pseudoaneurysms are rare, usually peripherally located, and associated with percutaneous needle biopsies, infection, or biliary

procedures. Intrahepatic aneurysms are often asymptomatic but can cause life-threatening arterial hemorrhage or, in mycotic pseudoaneurysms, produce fistulas between the aneurysm and the biliary tree or portal veins.8 Extrahepatic pseudoaneurysms occur at the donor-recipient arterial anastomosis and may be caused by infection or technical failure. Gray-scale ultrasound of hepatic artery pseudoaneurysms shows a hypoechoic structure (at times simulating a cyst), typically following the course of the hepatic artery, with intense swirling flow on color Doppler and a disorganized spectral waveform (Fig. 18.13). Management options are dictated by the location of the pseudoaneurysm. Extrahepatic pseudoaneurysms can be treated by surgery, transcatheter embolization, or stent insertion, whereas intrahepatic pseudoaneurysms are often treated with endovascular coil embolization.

Celiac Artery Stenosis Celiac artery stenosis may be caused by atheromatous disease or impingement of the celiac axis by the median arcuate ligament of the diaphragm. If severe, celiac stenosis can result in decreased arterial flow to the allograft. Patients are often asymptomatic before transplantation, presumably because of rich collateral networks, usually through the pancreaticoduodenal arcade. After transplantation, patients may become symptomatic, with evidence of biliary ischemia and abnormalities in serum LFT values, a result of the greater flow demand imposed on the celiac artery by the newly transplanted liver. Doppler ultrasound may be normal or may reveal a lowresistance tardus-parvus waveform in the transplanted hepatic

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FIG. 18.12  Hepatic Artery Stenosis in Two Patients.  Patient 1: (A) Intraparenchymal spectral Doppler ultrasound shows a low-resistance waveform (resistive index [RI] = 0.4). (B) Corresponding contrast-enhanced CT angiogram shows subtle stenosis of the proximal hepatic artery (arrow). Patient 2: (C) Intraparenchymal spectral Doppler shows a tardus-parvus, low-resistance waveform with a delayed acceleration time of 120 ms. (D) Corresponding CT angiogram shows long stenosis of the hepatic artery (between arrows).

artery and high-velocity jet across the celiac stenosis. Patients are treated with division of the median arcuate ligament or, in the case of atheromatous disease, an aortohepatic interposition bypass graft35,36 (Fig. 18.14).

Portal Vein Complications Portal vein stenosis or thrombosis is uncommon, with a reported incidence of 1% to 13%.30,37,38 Risk factors include faulty surgical technique, misalignment of vessels, excessive vessel length, hypercoagulable states, and previous portal vein surgery.30

Factors extrinsic to the portal vein may also contribute, such as increased downstream resistance caused by a suprahepatic stricture of the IVC or diminished portal venous blood flow. Clinical presentations include hepatic failure and signs of portal hypertension (gastrointestinal hemorrhage from varices or massive ascites). Gray-scale ultrasound of portal vein stenosis may show narrowing of the vessel lumen, usually at the anastomosis. Doppler interrogation shows a focal region of color aliasing, reflecting turbulent, high-velocity flow, with a threefold to fourfold velocity

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FIG. 18.13  Hepatic Artery Pseudoaneurysms in Two Patients.  Patient 1: (A) Gray-scale sonogram shows a small cystic mass close to the porta hepatis (arrowheads). (B) Color Doppler ultrasound confirms vascularity within the pseudoaneurysm (arrowheads) arising from the hepatic artery (arrow). (C) Corresponding enhanced CT confirms the pseudoaneurysm arising at the hepatic artery anastomosis. Patient 2: (D) Transverse and (E) sagittal sonograms show a midline oval mass (arrows). (F) On color and spectral Doppler ultrasound, disorganized flow is identified in a portion of the mass, representing a partially thrombosed pseudoaneurysm. Arrows mark the thrombosed portion of the pseudoaneurysm. (A-C with permission from Crossin JD, Muradali D, Wilson SR. US of liver transplants: normal and abnormal. Radiographics. 2003;23[5]:1093-1114.5)

increase at the site of stenosis relative to the prestenotic segment on spectral interrogation (Fig. 18.15). Chong and colleagues39 showed that the presence of elevated portal vein anastomotic velocities greater than 125 cm/sec, or a velocity ratio of 3 : 1 at the anastomosis, was greater than 95% specific for portal vein stenosis. True portal vein stenosis must be distinguished from a pseudostenosis of the portal vein. This entity is seen when the recipient portal vein is larger than the donor portal vein and no associated differential gradient exists across the site of narrowing. Portal vein thrombosis manifests as echogenic solid material within the portal vein lumen (Figs. 18.16 and 18.17). In the acute state the thrombus may be anechoic, making detection difficult on gray-scale ultrasound and emphasizing the necessity for careful Doppler assessment of the entire portal venous system. As with portal vein thrombosis in the native liver, the thrombus may decrease in size and eventually recanalize, showing multiple venous flow channels within the thrombus. Treatment options for portal vein thrombosis or stenosis include thrombectomy,

segmental portal vein resection, percutaneous thrombolysis, stent placement, and balloon angioplasty.

Inferior Vena Cava Complications Stenosis of the IVC is a rare complication of liver transplantation and may occur at the suprahepatic or infrahepatic anastomosis. IVC stenosis occurs more frequently in pediatric recipients and patients undergoing retransplantation.40 Causes of IVC stenosis include anastomotic discrepancy, IVC kinking, fibrosis, or neointimal hyperplasia. On gray-scale ultrasound, the IVC may show obvious narrowing at the site of anastomosis, associated with a focal region of aliasing on color Doppler. On spectral interrogation, a threefold to fourfold greater velocity gradient is observed across the stenosis compared with the prestenotic segment. The hepatic veins may show reversal of flow or may lose their normal phasicity, with a monophasic waveform8 (Figs. 18.18 and 18.19). Thrombosis of the IVC has been reported in less than 3% of recipients and is caused by technical difficulties at surgery, hypercoagulable states, or compression from adjacent fluid

CHAPTER 18  Organ Transplantation

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collections.26,40 Gray-scale ultrasound shows echogenic thrombus within the IVC that may continue into the hepatic veins. In cases of recurrent HCC, tumor thrombus may extend from the hepatic veins into the IVC (Fig. 18.20).

Hepatic Vein Stenosis Hepatic vein stenosis occurs with a frequency of 1% in orthotopic liver transplant and 2% to 5% in living donor transplants. This discrepancy in frequency is primarily related to different surgical techniques. In orthotopic liver transplants, an anastomosis is performed between the donor and recipient IVC without touching the hepatic veins. In living donor transplants, however, the donor hepatic vein is anastomosed to either the hepatic vein stump or the IVC of the recipient. This results in the hepatic veins being rigidly fixed in position, such that any movement of the graft produces a buckling and narrowing of the hepatic veins. In addition, progressive growth of partial liver grafts after surgery may result in stretching or twisting of the hepatic veins, further contributing to narrowing of the venous outlet.41,42

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FIG. 18.14  Celiac Artery Stenosis: Impingement by Median Arcuate Ligament.  (A) Transverse sonogram shows narrowing of the celiac artery secondary to impingement by the median arcuate ligament (arrow). (B) Spectral trace of the region of narrowing shows elevated peak systolic velocities of 412 cm/sec. (C) Spectral trace of left lobe intrahepatic arterial branch shows low-resistance tardus-parvus waveform. After surgical ligation of the median arcuate ligament, the spectral waveforms returned to normal.

Clinically, hepatic vein stenosis manifests with liver congestion, hepatomegaly, ascites, and/or pleural effusions. Hepatic venous obstruction in the early postoperative state is a surgical emergency, and reoperation is usually necessary for correction or for retransplantation, if substantial hepatic necrosis has occurred. Late-onset hepatic venous obstruction may be associated with a more insidious deterioration in liver function. These patients may benefit from metallic stent insertion or balloon venoplasty, because surgical correction is often difficult as a result of fibrotic changes around the anastomotic sites.41,42 Direct signs of hepatic vein stenosis include focal narrowing on gray-scale ultrasound associated with turbulent flow on color and spectral Doppler interrogation (Fig. 18.21). A persistent, monophasic spectral waveform is suggestive of, but not diagnostic of, hepatic vein stenosis; monophasic waveforms may also be present in normal, nonobstructed hepatic veins. However, the presence of a triphasic or biphasic waveform rules out clinically important hepatic vein stenosis.42

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F 120.1 cm/s

E 156.0 cm/s

D 32.8 cm/s

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FIG. 18.15  Portal Vein Stenosis: Anastomotic Stricture.  (A) Gray-scale sonogram of main portal vein shows narrowing at the anastomosis (arrowhead). (B) Color Doppler shows aliasing at the region of stenosis caused by high-velocity turbulent flow. (C) Spectral Doppler shows velocities of 32.8 cm/sec proximal to the stenosis. (D) Velocities at the stenosis are elevated at 156 cm/sec. (E) Poststenotic high-velocity turbulent flow is identified, measuring 120.1 cm/sec. (F) Beyond the turbulent flow, velocities of 53 cm/sec are obtained. This represents a threefold increased velocity gradient across the anastomosis, indicating that the stenosis is hemodynamically significant.

Extrahepatic Fluid Collections Perihepatic fluid collections and ascites are frequently observed after transplantation. In the early postoperative period a small amount of free fluid or a right pleural effusion may be observed, but these usually resolve in a few weeks. Fluid collections and hematomas are common in the areas of vascular anastomosis (hepatic hilum and adjacent to IVC) and biliary anastomosis, in the lesser sac, and in the perihepatic and subhepatic spaces.7 Because the peritoneal reflections surrounding the liver are ligated at transplantation, fluid collections can occur around the bare area of the liver, a location for fluid that is not encountered in the preoperative liver5 (Fig. 18.22). Ultrasound is highly sensitive in detecting these fluid collections, although it lacks specificity with regard to etiology because bile, blood, pus, and lymphatic fluid can all have a similar sonographic appearance. The presence of internal echoes in a fluid collection suggests blood or infection. Particulate ascites may also be observed in peritoneal carcinomatosis, although this would seem less likely in the transplant recipient population.5

Adrenal Hemorrhage Right-sided adrenal hemorrhage may be observed in the immediate postoperative period and results from (1) venous engorgement caused by ligation of the right adrenal vein during the removal of a portion of the IVC or (2) a coagulopathy caused by the

patient’s preexisting liver disease.26 On ultrasound, adrenal hemorrhage may be seen as a hypoechoic nodular structure or as a fluid collection in the right suprarenal region (Fig. 18.23).

Intrahepatic Fluid Collections Sterile postoperative fluid collections are often located along the falciform ligament and ligamentum venosum, usually appearing as fluid-filled anechoic collections surrounding the echogenic ligaments (Fig. 18.24). Bilomas may manifest as a hypoechoic or complex cyst. Intraparenchymal hematomas may result from the transplant surgery or percutaneous biopsy or may be a sequela of donor trauma (e.g., motor vehicle crash).

Abscess Versus Infarct In the early stages it may be difficult to differentiate a liver abscess from an infarct. Initially, both abscesses and infarcts may appear as a subtle hypoechoic region, associated with a localized coarsening of the parenchymal echotexture. Infarcts may subsequently organize into avascular round or wedge-shaped lesions, which can eventually develop central hypoechoic areas reflecting liquefaction and necrosis. A focal liver infarct should be diagnosed with accompanying Doppler evidence of hepatic arterial compromise. As with infarcts, the ultrasound appearance of a liver abscess also varies with its maturation. The classic appearance of a mature transplant liver abscess is a complex, cystic structure with thick,

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FIG. 18.16  Portal Vein: Bland Thrombus in Two Patients.  Patient 1: (A) Transverse sonogram and (B) corresponding contrast-enhanced CT show nonocclusive thrombus in the main portal vein (arrows). Patient 2: (C) Transverse sonogram and (D) corresponding contrast-enhanced CT scan show nonocclusive thrombus in the ascending ramus of the left portal vein (arrows).

irregular walls and particulate internal fluid, with or without associated septations. Both infarcts and abscesses may contain bubbles of air, visualized as bright echogenic foci with or without posterior acoustic shadowing (Fig. 18.25). Occasionally, bubbles of air within the lumen of an intraparenchymal abscess can be confused with benign pneumobilia or may be mistaken for air outside the liver within the gastrointestinal tract. A high index of suspicion is critical in patients at risk for either abscess or infarct to avoid these misinterpretations.

Intrahepatic Solid Masses The differential diagnosis of a solitary mass in the transplanted liver is similar to that in the native liver. For example, benign lesions, such as hemangiomas and cysts, are relatively common

in the transplanted liver, with the same range of appearances as described for the native liver. However, several pathologies unique to the transplanted liver may also appear as a solid or complex mass on gray-scale ultrasound, including infarcts (Fig. 18.26), abscesses, hematomas, recurrent or metastatic HCC, and posttransplant lymphoproliferative disorder (PTLD). Recurrent hepatocellular carcinoma is a serious complication that can potentially develop after transplantation in patients with a preoperative history of end-stage cirrhosis with known or occult hepatomas. The most common site of recurrent HCC is the lung, presumably caused by embolization with tumor cells through the hepatic veins before or during transplantation. The second most common location of recurrent hepatomas is within the allograft, followed by regional or distant lymph nodes. Early detection of recurrent hepatomas in the transplanted liver is

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FIG. 18.17  Portal Vein: Malignant Thrombus in Two Patients.  Patient 1: (A) Transverse sonogram of malignant thrombus (arrows) in right portal vein with (B) extension into main portal vein (arrow). (C) Triphasic CT of the liver shows the recurrent hepatocellular carcinoma (arrows) that accounts for the portal vein thrombus. Patient 2: (D) Transverse sonogram demonstrates malignant thrombus in the main portal vein (arrows). The background liver is extremely abnormal, with a large echogenic mass (arrowheads). (E) Portal venous phase of a triphasic CT scan confirms recurrent hepatocellular carcinoma (arrowheads) accompanied by expansile, enhancing malignant thrombus in the main portal vein (arrows). (A and B with permission from Crossin JD, Muradali D, Wilson SR. US of liver transplants: normal and abnormal. Radiographics. 2003;23[5]:1093-1114.5)

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FIG. 18.18  Inferior Vena Cava (IVC) Infrahepatic Anastomosis: Normal and Abnormal in Two Patients.  Sagittal sonograms of IVC show (A) a normal caliber at the anastomosis (arrows) and (B) narrowing at the anastomosis (arrows).

FIG. 18.19  Inferior Vena Cava (IVC) Suprahepatic Anastomotic Stricture.  Sagittal color Doppler sonogram of a stenosed segment of the IVC shows aliasing produced by high-velocity turbulent flow in both the IVC and the hepatic vein. Spectral tracing shows a greater than threefold velocity increase at the stenotic region (left arrow).

dialysis. The only contraindications to transplantation are unsuitability for general anesthesia or surgery, preexisting infection or malignancy, and a risk of recurrent renal disease (e.g., active vasculitis or oxalosis). Before transplantation, a suitable donor must be obtained with appropriate human lymphocyte antigen (HLA) matching with the recipient.44 As the number of patients with CRF continues to rise, the major limitation for expanding transplant programs is the shortage of suitable donor kidneys. This organ shortage has resulted in an increasing number of renal transplantations from living related donors. These donors may include family members or close friends with a long-standing relationship with the recipient. The average life expectancy for a cadaveric allograft is 7 to 10 years, whereas that for a live donor allograft is 15 to 20 years.44 Regardless of whether a cadaveric or live donor allograft is used, the cost-benefit ratio of a functioning successful transplant far outweighs that of a patient with persistent CRF, so multiple health care resources are targeted to ensure high rates of success. Ultrasound is the most valuable noninvasive imaging modality in monitoring the renal transplant.

Surgical Technique essential to facilitate early resection, ablation, or chemotherapy26,43 (Fig. 18.27). As in the general population, transplant recipients can develop any type of primary or secondary neoplasm within the liver.

RENAL TRANSPLANTATION Transplantation is the treatment of choice for many patients with chronic renal failure (CRF) severe enough to warrant

Detailed sonography of the renal transplant requires knowledge of the surgical procedure used in most institutions as well as the postsurgical anatomic relationships. The right or left lower quadrant is selected for the incision, based on the patient’s prior surgical history and the surgeon’s preference. Usually, the right lower quadrant is selected because the right iliac vein is more superficial and horizontal on this side of the pelvis, facilitating creation of a vascular anastomosis.45,46 The type of arterial anastomosis used depends on whether the allograft is cadaveric or living related and on the number

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FIG. 18.20  Inferior Vena Cava (IVC) Thrombosis in Three Patients.  (A) Transverse and (B) sagittal sonograms show malignant IVC and hepatic vein thrombus (arrows) in a patient with recurrent hepatocellular carcinoma after transplantation. (C) Transverse sonogram of the hepatic veins and (D) sagittal sonogram of IVC show bland thrombus (arrows) in each. (E) Sagittal sonogram and (F) corresponding contrast-enhanced CT show bland thrombus in the IVC (arrows). A, Ascites. (A and B with permission from Crossin JD, Muradali D, Wilson SR. US of liver transplants: normal and abnormal. Radiographics. 2003;23[5]:1093-1114.5)

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and size of donor renal arteries. In patients with cadaveric transplants, the donor artery, along with a portion of the aorta (Carrel patch) are anastomosed end to side to the external iliac artery. In patients with living donor transplants, the donor renal artery is anastomosed to either the internal iliac artery (end to end) or the external iliac artery (end to side) of the recipient. Multiple donor arteries of similar size may be joined together with a side-to-side anastomosis to form a common ostium. Alternatively, multiple arteries may be anastomosed as a Carrel patch, or anastomosed separately to the external iliac artery.45,46 The donor renal vein is almost always anastomosed end to side to the external iliac vein. In the case of multiple renal veins,

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FIG. 18.21  Hepatic Vein Stenosis.  (A) Color Doppler and (B) correlative CT show focal narrowing (arrow) of the right hepatic vein at junction with IVC. (C) Spectral Doppler shows monophasic flow in the right hepatic vein.

the smaller veins are usually ligated, resulting in a single donor vein.46 The ureter is usually anastomosed to the superolateral wall of the urinary bladder through a neocystostomy. Several techniques are used to create a neocystostomy, but the basic procedure involves tunneling the ureter through the bladder wall to prevent reflux to the transplant. For patients undergoing repeat surgery on the collecting system and those with complex surgeries, the recipient’s ureter may be used as a conduit to the bladder45 (Fig. 18.28). Because of the chronic shortage of donor organs, paired cadaveric kidneys from young (1.0) with reversal of flow in diastole. This is seen with severely increased vascular resistance in the kidney from rejection or renal vein thrombosis.

Gas can be observed within the collecting system in emphysematous pyelonephritis, appearing as a bright echogenic focus with distal dirty shadowing. Milk of calcium cysts can produce dirty shadowing, mimicking an intrarenal abscess. Scanning the patient in a decubitus position allows for differentiation; gas

Prerenal Vascular Complications Arterial Thrombosis Renal artery thrombosis occurs in less than 1% of transplants, usually within the first month of surgery, and is often initially asymptomatic. The most common cause is hyperacute or acute rejection, which results in occlusion of the intraparenchymal arterioles with retrograde main renal artery thrombosis. Other predisposing factors include a young pediatric donor kidney, atherosclerotic emboli, acquired renal artery stenosis, hypotension, vascular kinking, cyclosporine, hypercoagulable states, intraoperative vascular trauma, and poor intimal anastomosis.58 Global infarction of the allograft occurs when there is occlusive thrombosis of the main renal artery, with no perfusion to the renal parenchyma. On gray-scale ultrasound, the kidney may appear diffusely hypoechoic and enlarged. On color and spectral Doppler ultrasound, complete absence of arterial and venous flow distal to the occlusion, within both the hilar and the intraparenchymal vessels, is observed. Although surgical thrombectomy with arterial repair is often attempted, nephrectomy is frequently indicated in these patients.46 Segmental infarction of the allograft may occur in transplants with a single main renal artery with thrombosis of a major arterial branch (Fig. 18.40), in transplants with multiple renal arteries where a single artery is thrombosed, and in patients with systemic vasculitis. On gray-scale sonography, a segmental infarct may appear as a poorly defined hypoechoic region, a hypoechoic mass, or a hypoechoic mass with a well-defined echogenic wall.

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FIG. 18.36  Chronic Renal Failure in Six Patients.  (A) and (B) Cortical thinning. (A) Sagittal scan shows moderate cortical thinning with abundant renal sinus fat. (B) With progression, the kidney (arrows) becomes smaller and the cortex thinner. (C)-(F) Dystrophic calcifications. Sagittal sonograms show (C) a few punctuate peripheral cortical calcifications (arrows); (D) multiple peripheral and central cortical calcifications (arrows); and (E) linear calcifications that extend from the peripheral to deep cortex (arrows). (F) The end-stage kidney becomes calcified, appearing as an echogenic interface (arrow) associated with dirty shadowing (arrowheads). The kidney is frequently not identified on sonography at this stage.

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FIG. 18.37  Renal Transplant-Related Infections.  (A) Uroepithelial thickening. Sagittal sonogram shows mild uroepithelial thickening (arrowheads). (B) Sagittal scan shows mild uroepithelial thickening (arrows) surrounding a mildly dilated collecting system with internal echoes, secondary to early pyonephrosis. (C) Transverse sonogram shows moderate to severe uroepithelial thickening (arrow), which can be misinterpreted as a mass in the renal pelvis. (D)-(F) Focal pyelonephritis. (D) Sagittal sonogram shows subtle, focal echogenic region in the upper-pole cortex (arrowheads). (E) Intraparenchymal phlegmon appearing as a hypoechoic mass within the renal cortex (arrows). (F) On color Doppler, the phlegmon seen in image (E) is vascular. (G) and (H) Diffuse pyelonephritis. (G) Transverse sonogram shows a generous kidney with echogenic granular renal cortex, surrounded by inflamed echogenic perinephric fat (F). (H) Corresponding CT shows inflamed fat (F) as perinephric streaking. (I) Emphysematous pyelonephritis. Sagittal sonogram shows air (arrows) within collecting system, appearing as bright, echogenic linear foci with distal dirty shadowing.

On Doppler sonography, the infarcted region appears as a wedgeshaped area devoid of flow on color or spectral interrogation.57 Interpretation of the gray-scale and Doppler findings should not be influenced by urine output of the allograft or laboratory data, because segmental infarction may occur in the presence of preserved renal function. The absence of blood flow on Doppler interrogation in the kidney parenchyma may be observed in conditions other than arterial thrombosis, including hyperacute rejection and renal vein thrombosis. In these conditions, however, the main renal

artery is patent on spectral Doppler ultrasound and may exhibit reversal of diastolic flow.44

Renal Artery Stenosis Renal artery stenosis, the most common vascular complication of transplantation, occurs in up to 10% of patients within the first year, is more frequent in living donor allografts compared with cadaveric allografts, and should be suspected in cases of severe hypertension refractory to medical therapy. Transplants with multiple renal arteries are now being used more frequently

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FIG. 18.38  Renal Transplant-Related Infections.  (A) Perirenal Candida abscess. Transabdominal sagittal scan shows abscess (A) abutting the lower pole of the transplant kidney. (B) and (C) Subcapsular abscess on ultrasound and CT. Note the heterogeneous abscess (A) with gas (arrow) compressing the kidney (K). (D) and (E) Ureteritis. Sagittal sonograms of proximal (D) and midline (E) ureter show inflamed echogenic periureteral fat (arrows) secondary to an infected ureteral stent (arrowhead). (F) Cystitis. Transverse sonogram shows internal echoes and fluid-debris level (arrow) in urinary bladder, secondary to cystitis. Arrowheads show thickened bladder wall.

and show a very slightly higher rate of renal artery stenosis compared with those renal allografts with a single artery. Stenosis may occur in one of three regions of the transplanted artery: the donor portion (Fig. 18.41), most frequently observed in end-to-side anastomoses and thought to arise from either rejection or difficult surgical technique; the recipient portion (Fig. 18.42), which is more uncommon and usually the result of intraoperative clamp injury or intrinsic atherosclerotic disease; and the anastomosis (Fig. 18.43), which is more frequent in end-to-end anastomoses and is directly related to surgical technique or may be secondary to rejection.54,58-60 Initially, color Doppler ultrasound should be used to determine the location of the anastomosis, as well as to document focal regions of aliasing, which would indicate the presence of highvelocity turbulent flow and serve as a guide for meticulous spectral interrogation. A spectral tracing should then be obtained at the anastomosis and in any area where color aliasing is detected to determine the PSV in that region. The upper limit of normal for arterial PSV is unclear. Assigning a PSV upper limit of 200 cm/sec for diagnosing renal artery stenosis may result in a relatively high false-positive rate. Thus some authors have suggested using an arterial threshold PSV of 250 cm/sec for the diagnosis of renal artery stenosis.54,61

However, high velocities in the renal artery may be secondary to changes in the external iliac artery. Therefore the renal artery–external iliac artery PSV ratio can be calculated to determine if renal artery velocity measurements are a result of narrowing or high flow rates from the external iliac artery. A renal artery–external iliac artery PSV ratio greater than 1.8:1 is suggestive of renal artery stenosis.54,62 In addition, within the renal parenchyma, a tardus-parvus spectral waveform can be observed in the intraparenchymal arteries in patients with renal artery stenosis.46,57 If no flow abnormality is detected within the main renal artery after color and spectral Doppler interrogation, significant stenosis can be excluded.63

Doppler Criteria for Renal Artery Stenosis Color aliasing at the stenotic segment Distal turbulent flow Peak systolic velocity > 250 cm/sec Velocity gradient between the renal artery and external iliac artery greater than 1.8:1

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FIG. 18.39  Mimicker of Emphysematous Pyelonephritis.  (A) Emphysematous pyelonephritis. Transverse scan shows air in collecting system (arrow). (B) Milk of calcium cyst. Supine sonogram shows layering of the calcification (arrowheads) in the cyst, producing dirty shadowing. (C) Scanning this patient in a decubitus position changes the orientation of the layering of calcium to the most dependent portion of the cyst, allowing for differentiation from an air-filled collection.

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FIG. 18.40  Renal Artery Thrombosis.  (A) Sagittal sonogram shows normal gray-scale ultrasound on postoperative day 1. (B) However, power Doppler shows no flow in the lower pole because of thrombosis of a segmental artery. (C) Three months later, there is secondary scarring of the entire lower pole (arrow).

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C FIG. 18.41  Renal Artery Stenosis: Donor Portion.  (A) Color Doppler ultrasound of donor renal artery anastomosis shows focal area of aliasing (arrow). (B) Power Doppler shows area of narrowing in this region (arrow). (C) Spectral Doppler shows elevated angle-corrected velocities at the site of the arrow, greater than 400 cm/sec.

Intraparenchymal arterial stenosis may be observed in chronic rejection as a result of scarring in the tissues surrounding the involved vessels. On spectral Doppler ultrasound, a prolonged AT may be observed in the segmental and interlobar arteries, with a normal main renal artery waveform.45 Treatment options for renal artery stenosis include percutaneous transluminal angioplasty, endovascular stent placement, and surgery. Surgical management of these transplants involves resection and revision of the stenosis with insertion of a patch graft at the stenotic segment.46 A false-positive Doppler diagnosis of renal artery stenosis can occur if there is an abrupt turn in the main renal artery, if the artery is severely tortuous, or if there are errors in Doppler technique (Fig. 18.44). Inadvertent compression of the main renal artery by the sonographer while performing spectral interrogation may also produce transient narrowing of the artery and elevated PSV readings. Turning the patient in a decubitus position such that the anterior abdominal or pelvic wall tissues are displaced from lying over the transplant can reduce external pressure on the allograft during scanning.

Venous Thrombosis Occlusive renal vein thrombosis is slightly more common than arterial thrombosis, occurring in up to 4% of transplants, and is associated with acute pain, swelling of the allograft, and an abrupt cessation of renal function between the third and eighth postoperative day. Risk factors include technical difficulties at surgery, hypovolemia, propagation of femoral or iliac thrombosis, and compression by fluid collections.58,64

On gray-scale ultrasound, the allograft may appear enlarged, and in rare cases intraluminal thrombus may be detected in a dilated main renal vein or within the intraparenchymal venous system. Spectral and color Doppler ultrasound will show a lack of venous flow in the renal parenchyma, absence of flow in the main renal vein, and reversal of diastolic flow in the main renal artery, as well as sometimes in the intraparenchymal arteries65,66 (Fig. 18.45). The sonographer should be aware that reversal of flow in diastole in the main renal artery or the intraparenchymal arterial branches is highly suggestive of renal vein thrombosis only in the absence of venous flow in the renal parenchyma and main renal vein. Reversed diastolic arterial flow, with preservation of venous flow, is a nonspecific finding indicating extremely high vascular resistance in the small intrarenal vessels or main hilar vessels. The outcome for these patients is generally poor, with allograft loss rates of 33% to 55%. Potential causes of reversed diastolic flow include acute rejection, ATN, peritransplant hematomas (compressing renal graft or hilar vessels), and glomerulosclerosis.67

Renal Vein Stenosis Renal vein stenosis most often occurs from perivascular fibrosis or external compression by adjacent fluid collections. The renal cortex appears either normal or hypoechoic, and on color Doppler, aliasing is identified at the stenotic region because of focal, high-velocity turbulent flow. On spectral Doppler sonography, a threefold to fourfold increase in velocity across the region of

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FIG. 18.42  Renal Artery Stenosis: Recipient Portion.  (A) Color Doppler ultrasound shows focal area of aliasing (arrow) proximal to the renal artery anastomosis. (B) Spectral Doppler of the region of aliasing seen in image (A) shows angle-corrected peak velocities of 400 cm/sec. (C) Angiography shows a focal area of stenosis (arrow) arising from the external iliac artery. (D) Angiogram performed after angioplasty shows resolution of the stenotic region (arrow).

narrowing indicates a hemodynamically significant stenosis63 (Fig. 18.46).

Postrenal Collecting System Obstruction Collecting system obstruction is unusual in renal transplants, occurring in less than 5% of patients.45,63 Because the allograft is denervated, the collecting system dilates without clinical signs of pain or discomfort. The diagnosis is often made as an incidental finding on routine screening sonography or in the workup of

the transplant patient for asymptomatic deterioration of renal function parameters. The most common cause of ureteral obstruction is from ischemic strictures, usually involving the terminal ureter at the ureterovesical junction. The transplanted ureter is particularly susceptible to ischemic events because of its limited vascular supply from the renal artery. The ureterovesical junction is usually the region of most pronounced involvement because it is farthest anatomically from the renal

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FIG. 18.43  Renal Artery Stenosis: Anastomosis.  (A) Color Doppler ultrasound shows focal area of narrowing and aliasing at the anastomosis (arrows). (B) Spectral Doppler at the anastomosis shows elevated angle-corrected velocity of 775.4 cm/sec. (C) Renal arterial angiogram confirms stenosis at the anastomosis (arrow). (D) Angiogram performed after angioplasty shows resolution of the anastomotic stenosis.

hilum, where the ureteral branch originates.46 Other causes of ureteral obstruction include strictures from iatrogenic injury, intraluminal lesions (e.g., stones, blood clots, sloughed papillae), perigraft fibrosis, and ureteral kinking (Figs. 18.47 and 18.48). Extrinsic compression of the ureter from peritransplant collections can also result in collecting system obstruction. Patients with renal transplants are at higher risk for stone development compared with the general population. In approximately 15% of these patients, the stone development is related

to hypercalcemia. Because the transplant is denervated, patients with stone-related collecting system obstruction may not have typical symptoms of renal colic.54 Evaluation of the collecting system with fundamental grayscale imaging may be difficult because of side-lobe and scatter artifact, which can potentially obscure optimal evaluation of the calyceal system and ureter. Harmonic imaging, however, uses a narrower ultrasound beam with smaller side lobes and is less susceptible to scatter artifact. These parameters make harmonic imaging ideal for evaluating anechoic structures,

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FIG. 18.44  Mimickers of Renal Artery Stenosis.  (A) Abrupt turn in renal artery. On color Doppler ultrasound, aliasing is identified in this region (arrow), with peak systolic velocities of 429 cm/sec on spectral Doppler. (B)-(D) Misaligned angle correction. (B) Initial spectral Doppler shows elevated renal artery anastomotic velocity of 298 cm/sec. This elevated velocity reading is artifactual because the spectral angle correction is not aligned with the direction of the renal artery. (C) Follow-up spectral Doppler ultrasound shows a normal renal artery velocity of 189 cm/sec, with appropriate angle correction in the direction of the artery. (D) Renal angiogram confirms a normal renal artery (arrows) with no evidence of stenosis.

such as the renal collecting system for regions of subtle dilation, and the presence of small intraluminal stones (Fig. 18.49). Mild pelvicaliectasis may be secondary to nonobstructive causes such as overhydration, decreased ureteric tone (from denervation of transplant), and ureteric-vesical reflux or can occur transiently in the immediate postoperative period from perianastomotic edema.45,68 In addition, multiple parapelvic cysts can mimic a dilated collecting system (Fig. 18.50).

Arteriovenous Malformations and Pseudoaneurysms Intraparenchymal arteriovenous malformations (AVMs) result from vascular trauma to both artery and vein during percutaneous biopsies and are usually asymptomatic with few clinical sequelae. Because most of these are small and resolve spontaneously, the incidence of posttransplant AVMs is unknown, although rates of 1% to 18% have been reported. In rare cases, large AVMs may manifest with bleeding, high-output cardiac failure, or decreased

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FIG. 18.45  Renal Vein Thrombosis.  (A) Sagittal sonogram shows increased cortical echogenicity with a coarse echotexture. (B)-(D) Spectral Doppler ultrasound images of (B) cortical arteries, (C) renal sinus arterial branches, and (D) main renal artery show reversal of flow in diastole. No venous flow was detected in the transplant.

renal perfusion caused by the large shunt. In these patients, treatment usually involves percutaneous embolization therapy.44 Gray-scale ultrasound may not reveal small AVMs. Color Doppler sonography shows a focal region of aliasing with myriad intense colors, often associated with a prominent feeding artery or draining vein. Turbulent flow within the AVM produces vibration of the perivascular tissues, resulting in these tissues being assigned a color signal outside the borders of the renal vasculature. Spectral Doppler ultrasound is typical of that for all AVMs, with low-resistance, high-velocity flow and difficulty differentiating between artery and vein within the malformation.

If a dominant draining vein is detected, the waveform may be pulsatile or arterialized58,68-70 (Fig. 18.51, Video 18.3). On color Doppler ultrasound, focal regions of cortical dystrophic calcifications or small stones can mimic an AVM by producing an intense color signal known as a twinkling artifact.71 These artifacts can be differentiated from a true AVM on spectral tracing because both calcifications and stones produce characteristic linear bands on spectral interrogation. In our clinical experience, we have also observed a linear band of color posterior to these regions of calcium that extend to the limits of the color box. We have not observed this phenomenon with AVMs and

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FIG. 18.46  Renal Vein Stenosis.  Color Doppler of renal vein anastomosis shows focal area of aliasing (white arrow). Spectral interrogation in region of aliasing shows velocities of 200 cm/sec. Spectral interrogation proximal to aliasing shows velocities of 40 cm/sec (yellow arrow), indicating a hemodynamically significant stenosis of the renal vein.

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FIG. 18.47  Ureteral Strictures.  (A) Sagittal sonogram and (B) percutaneous nephrostogram show grade 3 pelvocaliectasis secondary to a stricture at the ureteropelvic junction (arrow). (C) Sagittal sonogram shows grade 4 pelvocaliectasis. The distal ureter was not seen on ultrasound. (D) Percutaneous nephrostogram shows a stricture at the ureterovesicular junction (arrow). (E) Sagittal sonogram shows grade 3 pelvocaliectasis, produced by (F) a stricture at the ureterovesicular junction (arrows). arrowheads, Tiny nonobstructing stone; B, bladder; U, ureter.

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FIG. 18.48  Multiple Obstructing Ureteral Stones.  (A) Sagittal sonogram of the kidney shows grade 3 pelvocaliectasis. (B) Sagittal sonogram of the distal ureter (U) shows multiple obstructing stones (arrows). (C) Coronal CT shows multiple obstructing ureteral stones (arrows). B, Bladder; K, kidney.

have found it a useful tool in differentiating vascular malformations from focal calcifications (Fig. 18.52). Pseudoaneurysms result from vascular trauma to the arterial system during percutaneous biopsy or, more frequently, occur at the site of the vascular anastomosis. They may be intrarenal or extrarenal (Figs. 18.53 and 18.54,Video 18.4). Pseuodaneurysms located in the renal hilum are somewhat more concerning than intrarenal pseudoaneurysms owing to their increased risk of rupture. On gray-scale sonography, pseudoaneurysms can mimic a simple or complex cyst. On color Doppler ultrasound, flow

can easily be obtained in the lumen of patent pseudoaneurysms, often with a swirling pattern, whereas on spectral Doppler, a central to-and-fro waveform or a disorganized arterial tracing may be obtained.45,54 Presumed cysts in the renal parenchyma or in the region of the hilum should be assessed with color Doppler to exclude the possibility of a pseudoaneurysm.

Fluid Collections Perinephric collections are demonstrated in up to 50% of transplant recipients.72,73 The most common collections include

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FIG. 18.49  Harmonic Imaging in Two Patients.  (A) Sagittal fundamental image shows barely detectable stones (arrows) and a dilated collecting system. (B) Harmonic image shows improved resolution of stones (arrows), now seen associated with distal acoustic shadowing, within anechoic dilated collecting system. (C) Fundamental image shows cortical cyst (arrowhead) with internal echoes and minimal through transmission. (D) Harmonic image shows cyst (arrowhead) to be anechoic and simple, now associated with an appropriate amount of through transmission.

hematoma, urinoma, lymphocele, and abscess. The ultrasound appearances of these peritransplant collections are often nonspecific, and clinical findings are warranted to determine their cause. However, the presence of air within a perirenal collection, without a history of recent percutaneous intervention, is highly suggestive of an abscess. The size and location of each collection should be documented on baseline scans because an increase in size may indicate the need for surgical intervention. Postoperative hematomas are variable in size but are often small, perirenal in location, and insignificant clinically and often resolve spontaneously.68 Their ultrasound appearance depends on the age of the collection. An acute hematoma will appear as an echogenic heterogeneous solid mass. With time the hematoma will liquefy, becoming a complex fluid collection with internal echoes, strands, or pseudoseptations. Postbiopsy hematomas have

a morphology similar to that of their postoperative counterparts (Figs. 18.55 and 18.56). Urine leaks, or urinomas, have been reported in up to 6% of renal transplants and occur within the first 2 weeks after surgery.44 They are usually secondary to either anastomotic leaks or ureteric ischemia. Rarely, urinomas can result from high-grade collecting system obstruction (Fig. 18.57). On sonography, urinomas are well defined and anechoic, may be associated with hydronephrosis, and in some cases can increase rapidly in size.57 Large urine leaks may result in widespread extravasation and gross intraperitoneal urinary ascites. Lymphoceles result from surgical disruption of the iliac lymphatics and have been reported in up to 20% of patients. They most often occur 4 to 8 weeks after surgery but may develop years after transplantation. Although most are discovered

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FIG. 18.50  Parapelvic Cysts Versus Pelvocaliectasis in Two Patients.  Patient 1: Parapelvic cysts. (A) Transverse and (B) sagittal sonograms show multiple parapelvic cysts mimicking pelvocaliectasis. Patient 2: Grade 3 pelvocaliectasis mimicking parapelvic cysts. (C) Sagittal sonogram shows multiple anechoic structures in the central aspect of the kidney, initially interpreted as multiple parapelvic cysts. (D) Contrast-enhanced magnetic resonance image shows contrast filling grossly dilated calyces (*). A single parapelvic cyst (arrow) is present.

incidentally and are asymptomatic, lymphoceles are the most common fluid collection to result in ureteric obstruction. Lymphoceles can become infected or can obstruct venous drainage, resulting in edema of the lower limb, scrotum, or labia.45 Symptomatic collections are drained (surgically or percutaneously) or undergo marsupialization. On sonography, lymphoceles are well-defined collections that are anechoic or that may contain fine internal strands (Figs. 18.58 and 18.59).

PANCREAS TRANSPLANTATION Pancreatic transplantation is performed in select patients who have major complications related to type 1 diabetes. Pancreas transplant represents the only form of self-regulating endocrine

replacement therapy, with more than 80% of recipients becoming free of exogenous insulin requirements within 1 year of surgery. Since 1988 in the United States, more than 15,000 kidney-pancreas transplants and 6000 pancreas transplants have been performed, with 1-year patient survival greater than 90%.3,74 Pancreatic transplantation aims to restore an adequate functioning beta cell mass and therefore to regain physiologic normoglycemic function, typically in the setting of insulin dependent diabetes. Recipients are typically type 1 diabetics in end-stage renal failure with other sequelae of long-term diabetes including neuropathy and atherosclerotic disease. Improvement in glycemic control diminishes the risk of long-term complications in diabetic patients.75 In particular, simultaneous pancreas

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FIG. 18.51  Arteriovenous Malformations (AVMs).  (A) Gray-scale ultrasound; AVM not detectable. (B) Corresponding color Doppler image shows large AVM. (C) Sagittal sonogram shows lower-pole AVM. (D) Spectral Doppler of AVM in image (C) shows high-velocity, low-resistance waveform. (E) Sagittal sonogram shows AVM with feeding vessel (arrow). (F) Sagittal scan shows lower-pole AVM with surrounding tissue vibration. See also Video 18.3.

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FIG. 18.52  Arteriovenous Malformation: Mimicker.  (A)-(C) Sagittal sonograms show twinkling artifact produced by (A) lower-pole dystrophic cortical calcification (arrow); (B) upper-pole stone; and (C) lower-pole stone. (D)-(F) Differentiation from AVM. On (D) color Doppler and (E) power Doppler, color artifact (arrows) may be seen posterior to border of kidney. Size of twinkling artifact varies with size of the color box. (F) On spectral Doppler ultrasound, the twinkling artifact shows linear bands as on these three spectral traces.

transplant in the setting of kidney transplants has been known to improve long-term patient survival.

Surgical Technique The simultaneous pancreas-kidney transplant is the most common form of pancreas transplantation in the United States and accounts of 80% of all pancreatic transplant procedures. To achieve optimum functioning beta cell mass, the procedure is a wholeorgan pancreas transplant performed in conjunction with a kidney transplant. Best results are achieved if the procedure is performed before the need for dialysis. This approach allows serum creatinine to be used not only as a marker of renal rejection, but also as a surrogate marker of pancreatic graft rejection. This is particularly important because serum amylase and lipase are not sensitive or specific markers of pancreatic rejection. Serum amylase has only 50% sensitivity for detection of rejection, and lipase may be elevated in both rejection and pancreatitis. The ultimate diagnosis of graft dysfunction is often made on biopsy. There are several further strategies for pancreas transplantation. A pancreas transplant can be performed as a second step following a successful renal transplant. The latter will typically be a living donor kidney and is usually advised for diabetic patients younger than age 5 with ongoing severe complications. The most severe complication is hypoglycemic unawareness wherein a patient

may be wholly lacking the normal stigmata or warning signs of a low glucose level (such as trembling, sweating, and tachycardia).76 This is the second most common mode of pancreatic transplant and contributes about 25% of all transplants in the United States. Finally, pancreas-only transplantation can be performed in diabetic patients who have no evidence of diabetic nephropathy. Only a minority of diabetic patients are eligible for this approach because it is limited to patients whose hypoglycemic awareness is challenging to manage medically. There are two well-established techniques for pancreas transplantation. Use of the bladder for exocrine drainage (duodenocystostomy) and use of the iliac vessels for arterial and venous supply were considered safer with regard to postoperative infection. This more traditional surgery, exocrine bladder drainage, involved anastomosing the donor duodenum to the urinary bladder and the donor portal vein to the recipient external iliac vein (systemic venous-endocrine drainage)77 (Fig. 18.60). In this circumstance the pancreas graft is placed in the right hemipelvis and the renal graft on the left. The chronic loss of pancreatic secretions into the bladder can result in problems with dehydration, metabolic acidosis, and allograft pancreatitis.3 There is also a higher risk of chemical cystitis secondary to the high amylase and lipase levels of pancreatic secretions. This can result in

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FIG. 18.53  Intrarenal Pseudoaneurysms in Two Patients.  Patient 1: (A) Sagittal sonogram shows lower-pole anechoic structure, mimicking a simple cyst. (B) On color Doppler ultrasound, however, swirling flow is identified in this structure, indicating that it represents a pseudoaneurysm. (C) Spectral Doppler ultrasound shows disorganized swirling flow within the pseudoaneurysm identified on image B. Patient 2: (D) Sagittal sonogram shows upper-pole anechoic structure. (E) On color Doppler ultrasound, swirling flow is identified in the anechoic structure identified on image (D) (arrow). This is adjacent to a large central arteriovenous malformation (AVM). (F) Spectral Doppler ultrasound shows disorganized flow in the pseudoaneurysm (yellow arrow) and low-resistance high-velocity flow in the central AVM (white arrow).

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FIG. 18.54  Extrarenal Pseudoaneurysm of Renal Artery.  (A) Transverse sonogram shows anechoic structure adjacent to renal hilum. (B) Color Doppler ultrasound shows that this structure contains swirling flow and represents a pseudoaneurysm. (C) Spectral Doppler ultrasound shows disorganized internal flow within pseudoaneurysm. (D) CT shows pseudoaneurysm arising from site of renal artery anastomosis. (E) and (F) In another patient, color Doppler images show a partially thrombosed pseudoaneurysm (arrows). See also Video 18.4.

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FIG. 18.55  Renal Transplant Subcapsular Hematoma Secondary to Biopsy.  (A) Sagittal sonogram shows acute hematoma appearing as solid heterogeneous structure. (B) After 1 week, cystic regions have developed within the hematoma. (C) After 1 month, hematoma has liquefied and is larger because of a hyperosmolar effect. Arrows mark the junction of the renal cortex and hematoma.

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FIG. 18.56  Hematomas in Three Patients.  Patient 1: (A) Transverse sonogram shows an intraparenchymal hematoma appearing as an anechoic cyst with mildly irregular walls (arrow). (B) Eight months later, the cyst has resolved. Patient 2: (C) Sagittal sonogram shows a hypoechoic solidappearing mass (arrows) abutting the upper pole of the transplant kidney (K). Patient 3: (D)-(F) Postoperative perirenal hematoma. (D) Sagittal sonogram shows hematoma 1 day after surgery, appearing as a solid echogenic heterogeneous mass. (E) Four weeks later, hematoma has begun to liquefy, with interspersed solid components. (F) Six weeks later, hematoma is almost completely liquefied; arrows mark the junction of the hematoma and renal cortex.

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recurrent urinary tract infections and hematuria. In male patients there is a higher risk of urethral infections and balanitis, which in turn may lead to urethral strictures. These complication risks have resulted in a move toward the intestinal or enteric-based drainage procedure whereby a duodenojejunostomy is created for exocrine drainage of pancreatic secretions. This is performed as either a side-to-side anastomosis or a Roux-en-Y anastomosis. The endocrine drainage is either systemic (anastomosis of donor portal vein to right common iliac vein or distal IVC) or portal venous (anastomosis of donor portal vein to SMV) (Fig. 18.61). This type of surgery provides a more physiologic transplant than the more traditional techniques and is not associated with dehydration or metabolic acidosis. In addition, it provides more appropriate glycemic control, with lower fasting insulin levels, and may be associated with a lower incidence of transplant rejection than the more traditional systemic venous-bladder drainage allografts.3,78 Table 18.1 shows the major differences between two types of pancreatic transplants (exocrine bladder drainage and exocrine enteric drainage).

FIG. 18.57  Urinoma Secondary to High-Grade Ureterovesical Junction Obstruction.  (A) Sagittal sonogram shows dilation of upper-pole calyx (arrow). (B) Dilation eventually ruptures through the adjacent cortex (arrow). (C) Obstruction forms a cortical defect (arrow) and subsequently a perinephric urinoma (U).

Venous Drainage The two methods for venous drainage can be categorized as systemic, wherein the transplanted portal vein is anastomosed to an iliac vein or vena cava, or alternately as using the portal technique, whereby it drains into the SMV of the recipient. The latter technique has over time been shown to confer no additional advantage in terms of outcome compared with the systemic technique.

Arterial Supply In both techniques (systemic and portal venous drainage) the arterial blood supply to the graft is via the donor common iliac artery being attached to the common or external iliac artery of the recipient. Most commonly at our institution, an arterial Y graft of the donor common iliac artery and external and internal iliac artery is anastomosed end to end with two separate anastomoses to the donor superior mesenteric and splenic arteries. There are some alternate methods, however, which include forming a single donor iliac arterial conduit (comprising either the common iliac and either the external or internal iliac artery),

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FIG. 18.58  Sterile Lymphoceles in Four Patients.  (A) Sagittal sonogram shows large, simple lymphocele abutting the transplant. (B) Sagittal scan shows small lymphocele (L) adjacent to the external iliac artery and vein. (C) Anechoic lymphocele (L) causes obstruction of the midureter (arrow) and dilation of the calyceal system (C). (D) Transverse sonogram shows septated perinephric lymphocele.

TABLE 18.1  Surgical Techniques for Pancreatic Transplantation Systemic Venous-Bladder Drainage

Portal Venous-Enteric Drainage

Venous drainage

Right lower quadrant Head caudad Y-shaped donor arterial graft anastomosed to recipient common iliac artery Donor portal vein is attached to external iliac vein

Endocrine drainage Exocrine drainage

Systemic venous En bloc donor duodenal stump to recipient bladder

Right upper quadrant Tail caudad Donor splenic artery to recipient common iliac artery Donor portal vein anastomosed to superior mesenteric vein Portal venous Duodenal segment anastomosed to Roux-en-Y loop of jejunum

Location Pancreatic orientation Arterial supply

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FIG. 18.59  Infected Lymphoceles in Five Patients.  Sagittal sonograms show infected lymphoceles with (A) a few thin internal strands; (B) multiple internal strands; (C) internal strands, draining to the skin through a cutaneous fistula (arrow); (D) thick septations and internal echoes; and (E) internal echoes and punctate wall calcifications (arrows). A, Ascites; K, kidney; L, lymphocele.

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FIG. 18.60  Pancreas Transplant: Systemic Venous-Bladder Drainage (Traditional Surgery).  (A) Donor portal vein (purple) is anastomosed to the external iliac vein, and donor artery Y graft (coral arrow) to the external iliac artery. Duodenal stump (D) is anastomosed to the bladder (B). (B) Sagittal sonogram shows duodenal stump anastomosed to the bladder (B). P, Pancreas.

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FIG. 18.61  Pancreas Transplant: Portal Venous-Enteric Drainage (New Technique).  (A) Donor portal vein (purple) is anastomosed to the superior mesenteric vein (blue), and donor artery (arrow) is anastomosed to the common iliac artery. Duodenal stump (D) is anastomosed to a Roux-en-Y (Y). (B) Transverse sonogram shows pancreas transplant (P) with fluid-filled duodenal stump (D).

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which is then anastomosed in an end-to-end fashion to the donor superior mesenteric artery (SMA) and end donor splenic artery to side donor iliac artery anastomosis. If the graft is portally drained, the arterial conduit is much longer than in a systemically drained graft.

Normal Pancreas Transplant Ultrasound To perform an ultrasound assessment of a transplanted pancreas, the sonographer should be aware of the surgical technique used, the position of the allograft in the abdomen at surgery, and the sites of vascular anastomosis. This often entails a detailed review of the intraoperative surgical notes or discussion with the surgeon before scanning the patient. With the systemic venous technique, the pancreatic head is placed in the iliac fossa, with the body and tail placed obliquely in the midabdomen. The pancreatic tail is therefore positioned superior to the head. With the portal venous technique, the orientation of the graft is such that the pancreatic head lies superiorly and the body and tail lie inferiorly. The graft is positioned within the right side of the abdomen within the inferior mesocolic space. This allows the recipient’s SMV to be anastomosed to the portal vein of the graft. In some instances the graft may be oriented in the transverse midline such that the recipient SMV is sagittally oriented to the transplant portal vein. The normal allograft retains the normal gray-scale morphology of a native pancreas with well-defined margins; a homogeneous echotexture, isoechoic or minimally echogenic to liver; and a thin, nondilated pancreatic duct (Fig. 18.62, Video 18.5 and Video 18.6). The peripancreatic fat shows a normal echogenicity. Occasionally a trace amount of peripancreatic fluid may be observed and usually resolves without complication. Color Doppler ultrasound is useful for locating the mesenteric vessels, particularly when the graft is poorly visualized because of overlying bowel gas. Spectral Doppler sonography of the normal graft shows continuous monophasic venous flow and low-resistance arterial waveforms.

FIG. 18.62  Normal Pancreas Transplant.  Gray-scale ultrasound of pancreas transplant shows normal echogenicity and echotexture of allograft, with nondilated pancreatic duct (arrowheads). See also Video 18.5 and Video 18.6.

If patient habitus is slim and the graft lies in a relatively superficial location within the right iliac fossa, a high-frequency linear probe in the range of 5 to 12 MHz can be used for interrogation. Probe compression as well as placement of the patient in a right anterior oblique position will help to displace overlying bowel gas. Color and power Doppler ultrasound are useful for locating the parenchymal and graft vessels, particularly when the graft is poorly visualized because of overlying bowel gas. Spectral Doppler sonography of the normal graft shows continuous monophasic venous flow and low-resistance arterial waveforms, with a rapid systolic upstroke and continuous diastolic flow.

Role of Contrast-Enhanced Ultrasound CT and MRI are often used for problem solving in the setting of postoperative complications; however, in the setting of associated renal impairment in this vulnerable patient group, the impact of iodinated contrast agents must be considered. Similarly, the potential risk of nephrogenic systemic fibrosis needs to be weighed against any possible diagnostic benefit when performing contrastenhanced MRI, particularly in patients with elevated creatinine. Contrast-enhanced ultrasound (CEUS) circumvents any underlying issues with renal impairment and facilitates the conspicuity of the graft relative to the surrounding tissues. It also allows assessment of areas of hypoperfusion. Its other inherent advantages have been well described and include safety, patient tolerance, and lack of ionizing radiation. Because the graft pancreas is highly vascularized, CEUS allows for visualization of areas of reduced or absent microcirculation. The contrast agent remains entirely intravascular, so focal areas of diminished perfusion or necrosis can be seen, and biopsy readily performed under ultrasound guidance. CEUS may also potentially allow an earlier diagnosis of graft rejection.79

Abnormal Pancreas Transplant The graft vasculature consists of the following: 1. The iliac arterial graft is connected to the donor SMA and splenic artery. A Doppler arterial waveform is usually obtained from the SMA, the proximal and distal splenic artery, the intrapancreatic arcade, and the transverse vessels. The waveform is assessed for peak systolic flow velocity as well as being evaluated for vascular resistance within the graft. A normal graft should have arterial flow with a sharp systolic upstroke and continuous antegrade diastolic flow. This is seen in conjunction with an RI of 0.5 to 0.7, which implies a relatively low intragraft vascular resistance. Because there is no capsule enveloping the graft pancreas, normal resistance may be seen in a transplanted pancreas with edema (in the setting of either pancreatitis or rejection). This is in contradistinction to the graft kidney, wherein intrarenal edema results in elevation of vascular resistance. 2. The graft splenic vein and SMV join together to form the donor portal vein. This can be anastomosed to the recipient iliac vein, vena cava (systemic drainage), or SMV (portal drainage). Cardiac phasicity can be seen in the venous waveform when there is systemic venous drainage. Relative flattening of the venous waveform at the site of the donor portal vein

CHAPTER 18  Organ Transplantation anastomosis to the recipient iliac or SMV is not an uncommon finding and is related to mild narrowing at this site. The most common complications are venous thrombosis and arterial pseudoaneurysm. Potential symptoms of graft thrombosis include unexplained hyperglycemia, graft tenderness, and, in the context of systemicbladder drainage technique, hematuria and diminished urinary amylase levels. Potential complications of graft thrombosis include graft dysfunction and necrosis, pancreatitis, leakage of pancreatic secretions, and sepsis.

Thrombosis Graft thrombosis, including both venous and arterial thrombosis, occurs in 2% to 19% of patients and is the second leading cause of transplant loss, after rejection. Pancreatic transplants are more vulnerable to graft thrombosis than renal transplants because the rate of blood flow in the transplanted pancreas is slower than that in a transplanted kidney.80,81 Although the clinical signs and symptoms of graft thrombosis are nonspecific, detection of vascular thrombosis is imperative for both salvaging the transplant and preventing life-threatening sequelae, such as sepsis and cardiovascular collapse. Venous thrombosis, which occurs with an estimated incidence of 5%, is a particular concern because of the increased risk of hemorrhagic pancreatitis, tissue necrosis, infection, thrombus propagation, and pulmonary embolism.81 Graft thrombosis can be categorized as early or late, depending on the time of diagnosis after surgery. Early graft thrombosis occurs within 1 month of transplantation and is secondary to either microvascular injury during preservation of the graft or technical error during surgery. Late graft thrombosis occurs 1 month after transplant surgery and is usually caused by alloimmune arteritis, in which gradual occlusion of the small blood vessels eventually culminates in complete proximal vessel occlusion.80 Other technical factors predisposing to graft thrombosis include coagulopathies, long preservation time, poor donor vessels, left-sided graft placement resulting in a deeper anastomosis, and the use of a venous extension graft.81 Prompt surgical intervention may be required depending on the severity of the thrombosis. Thrombosis of the graft splenic artery and vein results in infarction of the graft pancreatic body and tail. If there is thrombosis of the graft SMA and SMV, it may result in infarction of the pancreatic head and transplanted duodenum. In the context of acute thrombosis the graft may appear enlarged, whereas in more chronic thrombosis the graft appears diffusely atrophic. Venous thrombosis is far more common than arterial thrombosis and is either completely or partially occlusive. It can be localized to the SMV, the splenic vein, or both vessels. A venous thrombosis may form owing to a phlebitis related to an underlying pancreatitis. Alternate mechanisms include stasis caused by a perianastomotic fluid collection or a torque on the venous anastomosis related to a shift in position of the graft resulting in stretching or twisting. Stasis in a stump of the SMV distal to the pancreaticoduodenal vessels may be a nidus for venous thrombosis. Venous thrombi within the pancreatic graft may remain localized and not propagate into the portal vein, the iliac vein,

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or the IVC (systemic venous drainage) or the SMV (portal venous drainage). Normal graft function can therefore be maintained.82 However, the potential for propagation of venous thrombi always exists, and if not well seen on ultrasound may need to be imaged dynamically in the venous phase on multiphase computed tomography (CT) or magnetic resonance imaging (MRI). Splenic vein thrombosis results in reversal of arterial diastolic flow and absence of splenic venous flow on Doppler ultrasound. Diffuse narrowing of the transplanted portal vein can be visualized with either technique and is typically seen in association with elevation of venous pressure within the graft. A combination of systemic anticoagulation and/or thrombolytic therapy may be necessary to treat complete splenic vein occlusion.83 Endovascular thrombectomy may also be performed for partial or occlusive thrombus, provided there is no underlying pancreatitis or extrinsic vascular compression.84 Pseudoaneurysms occur at anastomotic sites or elsewhere as a result of pancreatitis or underlying infections or abscess. They can also occur secondary to biopsy or surgical trauma. The iatrogenic pseudoaneurysms may be seen in association with arteriovenous fistulas. Similar to the stump venous thrombi described earlier, stasis in low-flow surgically created vascular stumps can occur in peripheral superior mesenteric and splenic arterial segments and contributes to formation of stump thrombi. Arterial thrombosis involves the graft SMA, the graft splenic artery, or the donor Y construct. The pancreas has a smaller microcirculatory blood flow in comparison with other graft types, and this increases its risk for thrombosis. It is usually mitigated by the formation of intrapancreatic arterial collaterals, which means that patency of only one allograft artery (SMA or splenic artery) is sufficient for graft survival and function. These collaterals are often better appreciated on a modality such as CT owing to the relatively diminutive caliber of the vessels. Thrombosis is least common in the simultaneous pancreaskidney transplant as compared with the other techniques, as well as being less likely when the systemic-bladder drainage technique is used as compared with the portal-enteric drainage technique. However, kinking of the Y graft is more likely in the portal enteric technique and is related to the length of the vessel (the graft is placed higher in the abdomen). Many of these arterial complications can be managed via endovascular intervention, including coil embolization and covered stents. Surgical resection of aneurysms and grafting are usually reserved for patients who have infected grafts and pseudoaneurysms in the setting of abscesses in the transplant bed. On ultrasound, occlusive or nonocclusive thrombus may be visualized within the lumen of the transplanted arteries or veins (Fig. 18.63). We have also observed several cases of thrombus occurring at the suture line of blind-ending arteries or veins (Fig. 18.64). On spectral Doppler, no arterial flow is detected in transplants with occlusive arterial thrombus. In grafts with occlusive venous thrombus, a lack of venous flow is detected on spectral tracing, with high-resistance arterial flow showing either no flow in diastole (RI = 1) or reversal of diastolic flow.81 Surgically ligated arteries containing thrombus may show a cyclic pattern of flow adjacent to the thrombus, which we presume is secondary

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FIG. 18.63  Graft Thrombosis in Different Patients.  (A) Transverse sonogram, (B) sagittal sonogram, and (C) color Doppler image show nonocclusive venous thrombus (arrows). (D) Gray-scale ultrasound (arrow) and (E) correlative CT (arrows) show nonocclusive venous thrombus. (F) Sagittal sonogram shows occlusive arterial thrombus (arrows). (G) Sagittal sonogram, (H) transverse sonogram, and (I) color Doppler image show nonocclusive venous (arrowhead) and arterial (arrow) thrombus in the same transplant.

to local eddy currents, with a normal arterial waveform more proximally.

Arteriovenous Fistula and Pseudoaneurysms Arteriovenous fistulas and pseudoaneurysms are rare complications of pancreatic transplants and may be related to the blind ligation of mesenteric vessels along the inferior border of the pancreas during retrieval. In some patients, mycotic pseudoaneurysms may occur in the setting of graft infection.85 On gray-scale ultrasound, arterial malformations may not be detectable. On color Doppler sonography, however, a mosaic of intense colors may be identified, produced by the tangle of vessels within the malformation and adjacent tissue vibration.

Spectral Doppler ultrasound reveals high-velocity, low-resistance flow within the lesion, which is typical of arteriovenous shunting (Fig. 18.65). On gray-scale ultrasound, pseudoaneurysms usually appear as anechoic spherical structures, although mural-based intraluminal thrombus may be detected. On spectral Doppler ultrasound, the classic to-and-fro pattern may be observed.

Rejection Rejection is the most common cause of pancreatic graft loss after transplantation. This condition affects up to 40% of grafts and can be hyperacute, acute, or chronic.77 Early recognition of transplant rejection remains a challenge because clinical

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The usefulness of arterial RIs as an indicator of rejection is controversial. It has been shown that RIs of the arteries supplying the pancreatic transplant cannot differentiate allografts with mild or moderate rejection from normal transplants without rejection.90 The reason may be that the pancreatic transplant does not contain a discrete investing capsule, and therefore swelling from transplant rejection may not necessarily result in increased parenchymal pressures or elevated vascular resistance.91 Grossly elevated RIs greater than 0.8 have been observed in pancreatic allografts with biopsy-proven acute severe rejection. Although these elevated RIs may be sensitive, they are not specific in the detection of severe pancreatic transplant rejection.90 Similarly, graft enlargement and heterogeneity may be seen in acute pancreatitis and ischemia. In a small series of patients, CEUS played a useful role in the surveillance of pancreatic grafts and in particular helped in the earlier diagnosis of rejection. Time-intensity curves in patients during rejection showed a significantly slower ascent and diminished maximum intensity. Overall, there was a significantly reduced maximum intensity and time to reach peak intensity. After successful treatment of the episode of rejection, these parameters near normalized to initial values. Ultimately, image-guided biopsy is the reference standard for confirming and grading the severity of rejection. FIG. 18.64  Thrombus Adjacent to Suture Line.  Echogenic thrombus (arrowhead) at suture line (small arrows) of blind-ending ligated artery. Spectral trace adjacent to thrombus shows to-and-fro waveform (bottom), whereas spectral trace (top) more distally is normal.

parameters used to evaluate pancreas graft dysfunction have low sensitivity and specificity in detection of rejection. In particular, there is no individual biochemical marker that would permit acute rejection to be distinguished from vascular thrombosis or pancreatitis. Although current advances in immunosuppressives have had an impact on acute rejection rates, chronic rejection remains one of the major causes of long-term graft failure. Hyperacute rejection is rare and occurs in the immediate postsurgical period, usually as a result of preformed circulating cytotoxic antibodies in the recipient’s blood. Thrombosis and immediate graft loss occur with this condition. Acute rejection occurs as a result of an autoimmune vasculitis and develops 1 week to 3 months after transplantation. There is small vessel occlusion, which results in diminished perfusion and long-term infarction if not treated early.86 Recurrent episodes of inadequately treated or unrecognized rejection result in chronic rejection, with progressive endarteritis of small vessels with acinar atrophy, and eventually with fibrosis and parenchymal atrophy. Chronic rejection occurs in 4% to 10% of patients and is seen as gradual decline in exocrine and then endocrine function. On gray-scale ultrasound, the allograft may appear hypoechoic or may contain multiple anechoic regions, and the parenchymal echotexture may be patchy and heterogeneous87,88 (Fig. 18.66). In addition, there may be abnormal graft size, typically enlargement in acute rejection and atrophy in chronic rejection. Pancreatic enlargement in acute rejection has a sensitivity of 58% and a specificity of 100%.89

Pancreatitis Almost all patients develop symptoms of pancreatitis immediately after surgery, presumably caused by reperfusion injury and ischemia.91 This typically involves the entire graft. A temporary elevation of serum amylase 48 to 96 hours posttransplantation is therefore common and usually of no clinical consequence. There is also a mild transient elevation in amylase. Focal edema of the donor mesenteric fat attached to the arterial stump of the SMA should not be misdiagnosed as a focal pancreatitis. This finding is related to ligation of the donor’s lymphatic vessels. Other causes of pancreatitis include partial or complete occlusion of the pancreatic duct, poor perfusion of the allograft, and, in patients with systemic venous-bladder drainage, refluxrelated pancreatitis.87 Long term, graft pancreatitis is seen in up to 35% of transplants. Underlying predisposing factors include prolonged warm ischemia time, graft handling, and reperfusion injury. The major differential diagnoses to consider include graft rejection and ischemia. The ultrasound appearance of pancreatitis in the allograft is similar to that of pancreatitis in the native gland (Fig. 18.67). Gray-scale findings include a normal-sized or bulky edematous pancreas, poorly defined margins, increased echogenicity of the peripancreatic fat secondary to surrounding inflammation, peripancreatic fluid, and thickening of the adjacent gut wall. In cases of pancreatitis resulting from ductal obstruction, a dilated pancreatic duct may be observed.87,91 In nonacute cases of pancreatitis, pseudocysts adjacent to or distal from the transplant may be identified, usually appearing as a well-circumscribed fluid collection with minimal adjacent inflammatory changes. Needle aspiration of this structure typically demonstrates fluid with high amylase content. Pancreatitis may be seen in association with vascular sequelae such as a focal arterial aneurysm or venous thrombosis. Similarly,

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FIG. 18.65  Pancreas Transplant Vascular Malformations.  (A) and (B) Parenchymal arteriovenous malformation (AVM). Transverse gray-scale ultrasound shows no abnormality. (B) Color Doppler ultrasound, however, shows an intense mosaic of color within the pancreas, secondary to a parenchymal AVM. (C)-(F) Transplant-related arteriovenous fistula (AVF). Gray-scale (C) and color Doppler (D) show dilated vessels with arterial (E) and mixed atrial and venous (F) waveforms.

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FIG. 18.66  Pancreas Transplant Rejection.  (A) Transverse sonogram shows hypoechoic pancreas (arrows). The pancreatic parenchyma is also atrophied. (B) Oblique sonogram shows dilated pancreatic duct (D) secondary to surrounding parenchymal atrophy.

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severe graft pancreatitis is associated with a range of complications akin to those seen in a native pancreas such as pancreatic hemorrhage and necrosis, peripancreatic fluid collections, pseudocysts, abscesses, and pseudoaneurysms. Ultrasound can be used to guide aspiration of potential fluid collections and help discriminate pseudocysts from abscesses or seromas. If infection is demonstrated at the time of ultrasoundguided aspiration, CT is often performed to assess the graft in its entirety and in particular to evaluate for areas of duct disruption as well as to demonstrate the location of fluid collections in relation to the duodenal C loop and duodenojejunostomy. Early fluid collections are often surgically managed.

Fluid Collections Peripancreatic transplant-related fluid collections are associated with an increased likelihood of loss of allograft function and overall increased mortality and morbidity. Early diagnosis and characterization of these collections are imperative, because treatment in the acute stages is associated with improved graft function and decreased recipient morbidity.92 In the immediate postoperative period, peritransplant fluid may be caused by leakage of pancreatic fluid from transected ductules and lymphatics, an inflammatory exudate, blood, or urine (Fig. 18.68). These collections may require either close serial imaging follow-up or drainage, depending on the clinical status of the patient. Duodenal leaks in systemic venous-bladder drainage transplants occur from dehiscence of the duodenal-bladder anastomosis and result in the formation of urinomas, frequently at the medial aspect of the transplant. Urinomas may also result from infection or necrosis of the graft.92 Duodenal leaks in portal venous-enteric drainage transplants occur at the blind end of the donor duodenum or from the anastomosis with the recipient Roux-en-Y loop. On ultrasound, gross ascites, duodenal wall thickening, or free intraperitoneal air may be observed in patients with breakdown of the duodenal anastomoses. These leaks may result in overwhelming sepsis and can be life-threatening. Furthermore, the presence of digestive enzymes in contact with the graft may lead to substantial tissue necrosis.91 Patients with pancreatic transplants are also susceptible to infection because of their immunosuppressive therapy, as well as their underlying diabetes mellitus. Abscesses are occasionally identified and are often associated with hematomas, urinary tract infections, and pancreatitis. Although gas within a fluid collection may indicate the presence of a gas-forming organism, bubbles of air within a collection may also result from the presence of a fistula or tissue necrosis in cases of vascular thrombosis. On sonography these collections may demonstrate a thick irregular wall with peripheral hyperemia on Doppler interrogation. If gas is present, it typically is seen as echogenic foci with posterior reverberation artifact. Adjacent changes in the fat include increased echogenicity and fluid. In the posttransplant period, the development of a new collection or change in the sonographic morphology of the collection may result from a variety of causes, including infection; malfunction of the pancreatic duct, stent, or external drain; hemorrhage; or associated tissue infarction.92

Miscellaneous Complications Other complications of pancreatic transplants include intussusception of the Roux-en-Y loop, small bowel obstruction from adhesions, internal hernias (due to the surgically created mesenteric defect), and volvulus along the long axis of the graft. Because the patient is immunocompromised, there is a higher incidence of entities such as typhlitis or Clostridium difficile colitis.

POST TRANSPLANT LYMPHOPROLIFERATIVE DISORDER The global improvement in survival after transplantation can be attributed to a parallel improvement in immunosuppressant regimens. The depressed immune response to oncoviruses such as the Epstein-Barr virus (EBV) results in increased vulnerability of these patients to malignancies that are mediated by such oncoviruses. This contributes to a threefold to eightfold increased malignancy risk in transplant patients as compared with the baseline population.93-95 PTLD is the second most common malignancy in adult transplant patients, following skin malignancy (nonmelanoma).96 PTLD encompasses myriad disease processes ranging from lymphoid hyperplasia to poorly differentiated lymphoma. Biopsy is required to discriminate among the various subtypes. Many patients are asymptomatic or have vague symptomatology, resulting in a delayed diagnosis. It can be hard to discriminate PTLD from infection or allograft rejection. Imaging is therefore important in establishing the diagnosis, enabling tissue sampling, and monitoring response to treatment. EBV infection is relatively prevalent, with 90% to 95% of adults being seropositive; however, most immunocompetent hosts can eradicate B cells that display EBV antigens by using T cells. However, in immunocompromised patients as well as a small group of immunocompetent hosts, a small number of EBVinfected B cells escape and survive with resultant latent EBV infection.97 After solid organ transplantation, cytotoxic EBV-specific T cells may be completely lost within 6 months of transplantation as a result of immunosuppressive medication.98 Latently infected B cells have the potential to proliferate, resulting in PTLD.99 A variety of genetic mutations (including p53, NRAS) can result in PTLD. These genes are involved in the division, proliferation, and death of cells. Overproduction of cytokines such as interleukin-6 has also been implicated in the genesis of PTLD. Similarly, CMV-seronegative patients have a higher risk of developing PTLD after solid organ transplantation.100 The incidence of PTLD is thought to be related to the degree of immunosuppression and the type of allograft. The aggressive immunosuppressive therapy required to prevent heart-lung transplant rejection has resulted in a reported incidence of PTLD as high as 4.6%. However, the milder immunosuppression used in patients with liver transplant or renal transplant has resulted in a lower incidence of PTLD, reported as 2.2% and 1%, respectively.101,102 In addition, the numbers of lymphoid aggregates are higher in intestinal and lung transplants, both of which are associated with some of the highest incidences of PTLD.103 It is therefore

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FIG. 18.68  Fluid Collections.  (A)-(C) Hematoma. (A) Sagittal and (B) transverse sonograms show complex collection with internal echoes and strands. (C) Correlative CT shows hematoma in left upper quadrant that extends to pancreas (P). (D)-(I) Pseudocysts in three patients. Patient 1: (D) Sagittal sonogram shows complex epigastric cyst with internal septation. Patient 2: (E) Sagittal sonogram shows complex collection adjacent to pancreas (arrowheads). (F) Correlative CT scan shows collection extending into pancreatic head (P) and associated with free fluid (arrows). Patient 3: (G) Sagittal sonogram shows large pseudocyst with internal echoes surrounding pancreatic tail (P). (H) and (I) Seroma. Transverse sonogram and correlative CT scan show large, anechoic cystic structure surrounding pancreatic body (P). The wall enhanced on CT scan. The collection was sterile on aspiration.

not surprising that agents that suppress T-cell activity are associated with a higher risk of PTLD. By the same token, a larger total number of immunosuppressant agents used by a patient may result in an increased risk of PTLD.104 The incidence of PTLD is bimodal, with the initial peak in the first year after transplantation and the second peak approximately 4 to 5 years after transplantation.105 Biologically, the two peaks have a very different clinical course. The early-onset disease has a more favorable course, is pleomorphic in subtype, and has a positive response to reducing the level of immunosuppression.

Late-onset disease is more commonly seen in conjunction with EBV infection, a monomorphic subtype, and an aggressive disease course. There is a higher mortality, and the disease is often resistant to chemotherapy.106 PTLD can be categorized depending on its primary location into either nodal disease (22%) or extranodal disease (81%). Nodal disease is either mediastinal or retroperitoneal in location. The involved lymph nodes have an abnormal appearance, showing a hypoechoic thickened cortex with an absent or flattened fatty hilum (Figs. 18.69 to 18.72). Extranodal disease

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FIG. 18.69  Renal Posttransplant Lymphoproliferative Disorder in Two Patients.  Patient 1: (A) Sagittal sonogram shows infiltrative mass (arrows) in renal hilum. (B) Six months later, the mass (arrowheads) has infiltrated into the renal cortex. (C) Correlative CT shows hilar mass infiltrating into renal cortex. Patient 2: (D) Sagittal and (E) transverse sonograms show a hypoechoic to anechoic structure with low-level echoes (arrows) in the renal hilum that could be interpreted as a complex cyst. (F) Contrast-enhanced MRI shows that this structure represents a solid mass (arrows).

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FIG. 18.70  Renal Posttransplant Lymphoproliferative Disorder (PTLD): Extrarenal Manifestations in Two Patients.  Patient 1: (A) Sagittal sonogram shows a hypoechoic renal hilar mass (arrows). (B) Sagittal and (C) transverse sonograms of the spleen show a mass in the hilum (arrows) as well as an intraparenchymal mass (arrowheads). Patient 2: (D) Sagittal sonogram shows hilar mass (arrows). (E) Transverse sonogram shows that mass (arrows) encases transplanted renal artery. (F) Correlative magnetic resonance image shows hilar mass (arrows) encasing renal vessels. (G) Transverse sonogram shows malignant-appearing hepatic nodule (arrow). (H) Sagittal sonogram shows malignant lymphadenopathy. (I) CT shows tonsillar adenopathy in Waldeyer ring (arrows) secondary to PTLD.

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FIG. 18.71  Renal Posttransplant Lymphoproliferative Disorder (PTLD): Mimicker.  (A) Sagittal and (B) transverse sonograms show a poorly defined, hypoechoic region in the renal sinus (arrows), potentially representing an infiltrative mass. (C) Correlative magnetic resonance scan shows that the hypoechoic region represents sinus fat. K, Kidney.

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G FIG. 18.72  Hepatic Posttransplant Lymphoproliferative Disorder (PTLD) in Three Patients.  Patient 1: (A) Oblique sonogram shows malignant mass (arrows) encasing and narrowing main portal vein. (B) Correlative CT shows mass infiltrating liver. Patient 2: (C) Transverse and (D) sagittal color Doppler sonograms show avascular solid nodules (arrow). (E) Correlative CT scan shows solid hypovascular masses (arrows). Patient 3: (F) Transverse sonogram shows thick-walled gut (white arrow) adjacent to inflamed echogenic fat (black arrows). (G) Correlative CT scan shows thick-walled loop of small bowel (arrows).

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by definition involves three main sites—the central nervous system, solid organs, or the gastrointestinal tract. The liver is the most common site of intraabdominal involvement, occurring in 30% to 45% of patients with PTLD. In rare cases, intraosseous lesions may be present, with imaging features on CT and MRI similar to those of metastatic disease, infection, or primary bone lymphoma. Overall, PTLD should be considered in the differential diagnosis of any transplant patient with lymphadenopathy or a new lesion within a solid viscus or the skeletal system.107-110 When the solid organs are involved, there are four main patterns of disease: 1. Infiltrative pattern: There is an ill-defined mass or masses that are extrinsic to the hilum and can result in secondary mass effect and/or vascular compromise. For instance, within the liver it may cause biliary obstruction and obstruction of blood flow within the periportal space. In renal involvement the mass typically is located extrinsic to the renal pelvis with resultant mass effect and obstruction of the vessels and the collecting system. In both instances the mass is usually relatively hypoenhancing but fluorodeoxyglucose (FDG) avid on positron emission tomography (PET) imaging. 2. Parenchymal pattern: This is characterized by multiple lesions that are disseminated throughout the affected organ. These also tend to be hypoenhancing. In the lung they are typically solid and may rarely cavitate. There may also be ill-defined alveolar infiltrates. 3. Solitary mass: A solitary mass in the affected organ is seen on ultrasound as a hypoechoic lesion with no Doppler signal on color Doppler imaging. Calcification is unusual but seen in the context of posttreatment changes or tumor necrosis. 4. Infiltrative lesion: This lesion involves the organ in question but also extends to involve regional structures such as the chest, abdominal wall, and adjacent solid organs. As a secondary manifestation, there may be dysfunction of the other organ(s) that are involved. Pancreatic PTLD tends to produce diffuse glandular enlargement, with an appearance that is indistinguishable from pancreatitis or rejection.111 Gastrointestinal disease can involve either bowel or the peritoneal cavity. When there is peritoneal disease, it can be nodular or diffusely infiltrating.112 PTLD involving the gastrointestinal tract is seen in association with mural thickening, aneurysmal dilatation, ulceration, intussusception, and polypoidal lesions. Perforation is a rare manifestation of intestinal PTLD; the decline in perforation rates has been attributed to improved diagnosis and treatment of PTLD. As with any other lymphomatous-type lesions of the gut, obstruction of the bowel segments is rare.

Treatment Options Stratification and patient management are determined by the subtype of PTLD, the distribution of disease, and the type of allograft. Potential management options include modification of immunosuppression, chemotherapy, radiation, and rituximab therapy as well as surgical resection of isolated lesions. Rituximab

is a monoclonal antibody against B cell receptors, has a low toxicity profile, and has a response rate on the order of 60%. Preservation of graft function is an important goal of management while treating the PTLD.113,114 PET-CT has a pivotal role to play in monitoring response to therapy, particularly in patients in whom there are persistent focal lesions. In this scenario, FDG uptake allows discrimination between residual tumor and fibrosis. REFERENCES 1. Takemoto S, Terasaki PI, Cecka JM, et al. Survival of nationally shared, HLA-matched kidney transplants from cadaveric donors. The UNOS Scientific Renal Transplant Registry. N Engl J Med. 1992;327(12):834-839. 2. Berthoux FC, Jones EH, Mehls O, Valderrabano F. Transplantation report. 1: Renal transplantation in recipients aged 60 years or older at time of grafting. The EDTA-ERA Registry. European Dialysis and Transplant Association–European Renal Association. Nephrol Dial Transplant. 1996;11(Suppl. 1):37-40. 3. Cattral MS, Bigam DL, Hemming AW, et al. Portal venous and enteric exocrine drainage versus systemic venous and bladder exocrine drainage of pancreas grafts: clinical outcome of 40 consecutive transplant recipients. Ann Surg. 2000;232(5):688-695. 4. United Network for Organ Sharing. National data. Transplants by organ type January 1, 1988–June 30, 2016. Available from: https://www.unos.org/ data. Accessed 2016 July 18. 5. Crossin JD, Muradali D, Wilson SR. US of liver transplants: normal and abnormal. Radiographics. 2003;23(5):1093-1114. 6. Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334(11):693-699. 7. Quiroga S, Sebastia MC, Margarit C, et al. Complications of orthotopic liver transplantation: spectrum of findings with helical CT. Radiographics. 2001;21(5):1085-1102. 8. Nghiem HV. Imaging of hepatic transplantation. Radiol Clin North Am. 1998;36(2):429-443. 9. Kamel IR, Kruskal JB, Raptopoulos V. Imaging for right lobe living donor liver transplantation. Semin Liver Dis. 2001;21(2):271-282. 10. Wolfsen HC, Porayko MK, Hughes RH, et al. Role of endoscopic retrograde cholangiopancreatography after orthotopic liver transplantation. Am J Gastroenterol. 1992;87(8):955-960. 11. Keogan MT, McDermott VG, Price SK, et al. The role of imaging in the diagnosis and management of biliary complications after liver transplantation. AJR Am J Roentgenol. 1999;173(1):215-219. 12. Letourneau JG, Castaneda-Zuniga WR. The role of radiology in the diagnosis and treatment of biliary complications after liver transplantation. Cardiovasc Intervent Radiol. 1990;13(4):278-282. 13. Barton P, Maier A, Steininger R, et al. Biliary sludge after liver transplantation: 1. Imaging findings and efficacy of various imaging procedures. AJR Am J Roentgenol. 1995;164(4):859-864. 14. Miller WJ, Campbell WL, Zajko AB, et al. Obstructive dilatation of extrahepatic recipient and donor bile ducts complicating orthotopic liver transplantation: imaging and laboratory findings. AJR Am J Roentgenol. 1991;157(1):29-32. 15. Zajko AB, Campbell WL, Bron KM, et al. Cholangiography and interventional biliary radiology in adult liver transplantation. AJR Am J Roentgenol. 1985;144(1):127-133. 16. Sheng R, Zajko AB, Campbell WL, Abu-Elmagd K. Biliary strictures in hepatic transplants: prevalence and types in patients with primary sclerosing cholangitis vs those with other liver diseases. AJR Am J Roentgenol. 1993;161(2):297-300. 17. Ward EM, Wiesner RH, Hughes RW, Krom RA. Persistent bile leak after liver transplantation: biloma drainage and endoscopic retrograde cholangiopancreatographic sphincterotomy. Radiology. 1991;179(3):719720. 18. McDonald V, Matalon TA, Patel SK, et al. Biliary strictures in hepatic transplantation. J Vasc Interv Radiol. 1991;2(4):533-538.

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41. Kubo T, Shibata T, Itoh K, et al. Outcome of percutaneous transhepatic venoplasty for hepatic venous outflow obstruction after living donor liver transplantation. Radiology. 2006;239(1):285-290. 42. Ko EY, Kim TK, Kim PN, et al. Hepatic vein stenosis after living donor liver transplantation: evaluation with Doppler US. Radiology. 2003;229(3): 806-810. 43. Ferris JV, Baron RL, Marsh Jr JW, et al. Recurrent hepatocellular carcinoma after liver transplantation: spectrum of CT findings and recurrence patterns. Radiology. 1996;198(1):233-238. 44. Baxter GM. Ultrasound of renal transplantation. Clin Radiol. 2001; 56(10):802-818. 45. Brown ED, Chen MY, Wolfman NT, et al. Complications of renal transplantation: evaluation with US and radionuclide imaging. Radiographics. 2000;20(3):607-622. 46. Kobayashi K, Censullo ML, Rossman LL, et al. Interventional radiologic management of renal transplant dysfunction: indications, limitations, and technical considerations. Radiographics. 2007;27:1109-1130. 47. Memel DS, Dodd GD 3rd, Shah AN, et al. Imaging of en bloc renal transplants: normal and abnormal postoperative findings. AJR Am J Roentgenol. 1993;160(1):75-81. 48. O’Neill WC, Baumgarten DA. Ultrasonography in renal transplantation. Am J Kidney Dis. 2002;39(4):663-678. 49. Lachance SL, Adamson D, Barry JM. Ultrasonically determined kidney transplant hypertrophy. J Urol. 1988;139(3):497-498. 50. Babcock DS, Slovis TL, Han BK, et al. Renal transplants in children: long-term follow-up using sonography. Radiology. 1985;156(1):165-167. 51. Absy M, Metreweli C, Matthews C, Al Khader A. Changes in transplanted kidney volume measured by ultrasound. Br J Radiol. 1987;60(714): 525-529. 52. American College of Radiology (ACR), Society for Pediatric Radiology (SPR), Society of Radiologists in Ultrasound (SRU), American Institute of Ultrasound in Medicine (AIUM). AIUM practice guideline for the performance of an ultrasound examination of solid-organ transplants. J Ultrasound Med. 2014;33(7):1309-1320. 53. Tublin ME, Bude RO, Platt JF. Review. The resistive index in renal Doppler sonography: where do we stand? AJR Am J Roentgenol. 2003;180(4): 885-892. 54. Weber TM, Lockhart ME. Renal transplant complications. Abdom Imaging. 2013;38(5):1144-1154. 55. Rigg KM. Renal transplantation: current status, complications and prevention. J Antimicrob Chemother. 1995;36(Suppl. B):51-57. 56. Pirsch JD, Ploeg RJ, Gange S, et al. Determinants of graft survival after renal transplantation. Transplantation. 1996;61(11):1581-1586. 57. Akbar SA, Jafri SZ, Amendola MA, et al. Complications of renal transplantation. Radiographics. 2005;25(5):1335-1356. 58. Dodd GD 3rd, Tublin ME, Shah A, Zajko AB. Imaging of vascular complications associated with renal transplants. AJR Am J Roentgenol. 1991;157(3): 449-459. 59. Jordan ML, Cook GT, Cardella CJ. Ten years of experience with vascular complications in renal transplantation. J Urol. 1982;128(4):689-692. 60. Hanto DW, Simmons RL. Renal transplantation: clinical considerations. Radiol Clin North Am. 1987;25(2):239-248. 61. Baxter GM, Ireland H, Moss JG, et al. Colour Doppler ultrasound in renal transplant artery stenosis: which Doppler index? Clin Radiol. 1995;50(9): 618-622. 62. de Morais RH, Muglia VF, Mamere AE, et al. Duplex Doppler sonography of transplant renal artery stenosis. J Clin Ultrasound. 2003;31(3): 135-141. 63. Tublin ME, Dodd GD 3rd. Sonography of renal transplantation. Radiol Clin North Am. 1995;33(3):447-459. 64. Penny MJ, Nankivell BJ, Disney AP, et al. Renal graft thrombosis. A survey of 134 consecutive cases. Transplantation. 1994;58(5):565-569. 65. Baxter GM, Morley P, Dall B. Acute renal vein thrombosis in renal allografts: new Doppler ultrasonic findings. Clin Radiol. 1991;43(2): 125-127. 66. Reuther G, Wanjura D, Bauer H. Acute renal vein thrombosis in renal allografts: detection with duplex Doppler US. Radiology. 1989;170(2): 557-558.

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67. Lockhart ME, Wells CG, Morgan DE, et al. Reversed diastolic flow in the renal transplant: perioperative implications versus transplants older than 1 month. AJR Am J Roentgenol. 2008;190(3):650-655. 68. Pozniak MA, Dodd GD 3rd, Kelcz F. Ultrasonographic evaluation of renal transplantation. Radiol Clin North Am. 1992;30(5):1053-1066. 69. Middleton WD, Kellman GM, Melson GL, Madrazo BL. Postbiopsy renal transplant arteriovenous fistulas: color Doppler US characteristics. Radiology. 1989;171(1):253-257. 70. Huang MW, Muradali D, Thurston WA, et al. Uterine arteriovenous malformations: gray-scale and Doppler US features with MR imaging correlation. Radiology. 1998;206(1):115-123. 71. Rahmouni A, Bargoin R, Herment A, et al. Color Doppler twinkling artifact in hyperechoic regions. Radiology. 1996;199(1):269-271. 72. Letourneau JG, Day DL, Ascher NL, Castaneda-Zuniga WR. Imaging of renal transplants. AJR Am J Roentgenol. 1988;150(4):833-838. 73. Silver TM, Campbell D, Wicks JD, et al. Peritransplant fluid collections. Ultrasound evaluation and clinical significance. Radiology. 1981;138(1): 145-151. 74. Data from the Organ Procurement and Transplantation Network and the U.S. Scientific Registry of Transplant Recipients. In United Network for Organ Sharing and Scientific Registry Data, 2008. Available from: https:// optn.transplant.hrsa.gov/data/view-data-reports/national-data/#. 75. White SA, Shaw JA, Sutherland DE. Pancreas transplantation. Lancet. 2009;373(9677):1808-1817. 76. Hariharan S, Pirsch JD, Lu CY, et al. Pancreas after kidney transplantation. J Am Soc Nephrol. 2002;13(4):1109-1118. 77. Pozniak MA, Propeck PA, Kelcz F, Sollinger H. Imaging of pancreas transplants. Radiol Clin North Am. 1995;33(3):581-594. 78. Freund MC, Steurer W, Gassner EM, et al. Spectrum of imaging findings after pancreas transplantation with enteric exocrine drainage: Part 1, posttransplantation anatomy. AJR Am J Roentgenol. 2004;182(4):911-917. 79. Kersting S, Ludwig S, Ehehalt F, et al. Contrast-enhanced ultrasonography in pancreas transplantation. Transplantation. 2013;95(1):209-214. 80. Krebs TL, Daly B, Wong JJ, et al. Vascular complications of pancreatic transplantation: MR evaluation. Radiology. 1995;196(3):793-798. 81. Foshager MC, Hedlund LJ, Troppmann C, et al. Venous thrombosis of pancreatic transplants: diagnosis by duplex sonography. AJR Am J Roentgenol. 1997;169(5):1269-1273. 82. Vandermeer FQ, Manning MA, Frazier AA, Wong-You-Cheong JJ. Imaging of whole-organ pancreas transplants. Radiographics. 2012;32(2): 411-435. 83. Stockland AH, Willingham DL, Paz-Fumagalli R, et al. Pancreas transplant venous thrombosis: role of endovascular interventions for graft salvage. Cardiovasc Intervent Radiol. 2009;32(2):279-283. 84. Barth MM, Khwaja K, Faintuch S, Rabkin D. Transarterial and transvenous embolotherapy of arteriovenous fistulas in the transplanted pancreas. J Vasc Interv Radiol. 2008;19(8):1231-1235. 85. Hagspiel KD, Nandalur K, Burkholder B, et al. Contrast-enhanced MR angiography after pancreas transplantation: normal appearance and vascular complications. AJR Am J Roentgenol. 2005;184(2):465-473. 86. Drachenberg CB, Papadimitriou JC. Spectrum of histopathological changes in pancreas allograft biopsies and relationship to graft loss. Transplant Proc. 2007;39(7):2326-2328. 87. Patel B, Markivee CR, Mahanta B, et al. Pancreatic transplantation: scintigraphy, US, and CT. Radiology. 1988;167(3):685-687. 88. Yuh WT, Wiese JA, Abu-Yousef MM, et al. Pancreatic transplant imaging. Radiology. 1988;167(3):679-683. 89. Wong JJ, Krebs TL, Klassen DK, et al. Sonographic evaluation of acute pancreatic transplant rejection: morphology—Doppler analysis versus guided percutaneous biopsy. AJR Am J Roentgenol. 1996;166(4):803-807. 90. Aideyan OA, Foshager MC, Benedetti E, et al. Correlation of the arterial resistive index in pancreas transplants of patients with transplant rejection. AJR Am J Roentgenol. 1997;168(6):1445-1447. 91. Heyneman LE, Keogan MT, Tuttle-Newhall JE, et al. Pancreatic transplantation using portal venous and enteric drainage: the postoperative appearance of a new surgical procedure. J Comput Assist Tomogr. 1999;23:283290.

92. Patel BK, Garvin PJ, Aridge DL, et al. Fluid collections developing after pancreatic transplantation: radiologic evaluation and intervention. Radiology. 1991;181(1):215-220. 93. Howard RJ, Patton PR, Reed AI, et al. The changing causes of graft loss and death after kidney transplantation. Transplantation. 2002;73(12): 1923-1928. 94. Briggs JD. Causes of death after renal transplantation. Nephrol Dial Transplant. 2001;16(8):1545-1549. 95. Apel H, Walschburger-Zorn K, Haberle L, et al. De novo malignancies in renal transplant recipients: experience at a single center with 1882 transplant patients over 39 yr. Clin Transplant. 2013;27(1):E30-E36. 96. Penn I. Post-transplant malignancy: the role of immunosuppression. Drug Saf. 2000;23(2):101-113. 97. Parker A, Bowles K, Bradley JA, et al. Diagnosis of post-transplant lymphoproliferative disorder in solid organ transplant recipients—BCSH and BTS guidelines. Br J Haematol. 2010;149(5):675-692. 98. Haque T, Crawford DH. Role of donor versus recipient type Epstein-Barr virus in post-transplant lymphoproliferative disorders. Springer Semin Immunopathol. 1998;20(3-4):375-387. 99. Babcock GJ, Decker LL, Freeman RB, Thorley-Lawson DA. Epstein-Barr virus–infected resting memory B cells, not proliferating lymphoblasts, accumulate in the peripheral blood of immunosuppressed patients. J Exp Med. 1999;190(4):567-576. 100. Opelz G, Daniel V, Naujokat C, et al. Effect of cytomegalovirus prophylaxis with immunoglobulin or with antiviral drugs on post-transplant non-Hodgkin lymphoma: a multicentre retrospective analysis. Lancet Oncol. 2007;8(3): 212-218. 101. Nalesnik MA, Makowka L, Starzl TE. The diagnosis and treatment of posttransplant lymphoproliferative disorders. Curr Probl Surg. 1988;25(6): 367-472. 102. Vrachliotis TG, Vaswani KK, Davies EA, et al. CT findings in posttransplantation lymphoproliferative disorder of renal transplants. AJR Am J Roentgenol. 2000;175(1):183-188. 103. Tsao L, Hsi ED. The clinicopathologic spectrum of posttransplantation lymphoproliferative disorders. Arch Pathol Lab Med. 2007;131(8): 1209-1218. 104. Opelz G, Dohler B. Lymphomas after solid organ transplantation: a collaborative transplant study report. Am J Transplant. 2004;4(2):222-230. 105. Vegso G, Hajdu M, Sebestyen A. Lymphoproliferative disorders after solid organ transplantation—classification, incidence, risk factors, early detection and treatment options. Pathol Oncol Res. 2011;17(3):443-454. 106. Dotti G, Fiocchi R, Motta T, et al. Epstein-Barr virus–negative lymphoproliferate disorders in long-term survivors after heart, kidney, and liver transplant. Transplantation. 2000;69(5):827-833. 107. Donnelly LF, Frush DP, Marshall KW, White KS. Lymphoproliferative disorders: CT findings in immunocompromised children. AJR Am J Roentgenol. 1998;171(3):725-731. 108. Penn I. Cancers complicating organ transplantation. N Engl J Med. 1990;323(25):1767-1769. 109. Pickhardt PJ, Siegel MJ. Abdominal manifestations of posttransplantation lymphoproliferative disorder. AJR Am J Roentgenol. 1998;171(4): 1007-1013. 110. Kaushik S, Fulcher AS, Frable WJ, May DA. Posttransplantation lymphoproliferative disorder: osseous and hepatic involvement. AJR Am J Roentgenol. 2001;177(5):1057-1059. 111. Meador TL, Krebs TL, Cheong JJ, et al. Imaging features of posttransplantation lymphoproliferative disorder in pancreas transplant recipients. AJR Am J Roentgenol. 2000;174(1):121-124. 112. Pickhardt PJ, Siegel MJ. Posttransplantation lymphoproliferative disorder of the abdomen: CT evaluation in 51 patients. Radiology. 1999;213(1): 73-78. 113. Allen U, Hebert D, Moore D, et al. Epstein-Barr virus–related post-transplant lymphoproliferative disease in solid organ transplant recipients, 1988-97: a Canadian multi-centre experience. Pediatr Transplant. 2001;5(3): 198-203. 114. Swinnen LJ. Diagnosis and treatment of transplant-related lymphoma. Ann Oncol. 2000;11(Suppl. 1):45-48.

PART THREE: Small Parts, Carotid Artery, and Peripheral Vessel Sonography CHAPTER

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The Thyroid Gland Luigi Solbiati, J. William Charboneau, Vito Cantisani, Carl Reading, and Giovanni Mauri

SUMMARY OF KEY POINTS • Ultrasound is the best imaging modality to study the thyroid gland for both diffuse and nodular disease. • The overwhelming majority of thyroid nodules are benign. Thyroid cancer is rare and accounts for less than 1% of all malignant neoplasms. • Approximately 80% of nodular thyroid disease is caused by hyperplasia. When hyperplasia leads to an overall increase in size or volume of the gland, the term “goiter” is used. • Most hyperplastic or adenomatous nodules are isoechoic compared with normal thyroid tissue, but may become hyperechoic because of the numerous interfaces between cells and colloid substance. • Hyperfunctioning (autonomous) nodules often exhibit an abundant perinodular and intranodular vascularity. • Purely anechoic areas are caused by serous or colloid fluid. • Adenomas represent only 5% to 10% of all nodular disease of the thyroid and are seven times more common in women than men. In general, the cytologic features of follicular adenomas are indistinguishable from those of follicular carcinoma.

• Solid consistency, hypoechogenicity, microcalcifications, taller-than-wide appearance, hypervascularity, irregular margins, invasion of adjacent structures, and presence of cervical lymph node metastases are suspicious signs of thyroid malignancy. • Ultrasound-guided fine-needle aspiration is the most effective method for diagnosing malignancy in a thyroid nodule. • After partial or near-total thyroidectomy for carcinoma, sonography is the preferred method for follow-up, by detecting residual, recurrent, or metastatic disease in the neck. • The Thyroid Imaging Reporting and Data System (TIRADS) can be used to stratify the risk of malignancy of a thyroid nodule according to its ultrasonographic characteristics. • Ultrasound-guided ablation with chemical agents (ethanol) or thermal energy (radiofrequency and laser ablation) can be used to treat thyroid adenoma, benign cold nodules, and even nodal metastases of thyroid cancers.

CHAPTER OUTLINE INSTRUMENTATION AND TECHNIQUE ANATOMY CONGENITAL THYROID ABNORMALITIES NODULAR THYROID DISEASE Pathologic Features and Sonographic Correlates Hyperplasia and Goiter Adenoma

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Carcinoma Lymphoma Thyroid Metastases Fine-Needle Aspiration Biopsy Sonographic Applications Detection of Thyroid Masses Differentiation of Benign and Malignant Nodules Thyroid Imaging Reporting and Data System

ecause of the superficial location of the thyroid gland, highresolution real-time gray-scale and color Doppler sonography can demonstrate normal thyroid anatomy and pathologic conditions with remarkable clarity. As a result, ultrasound plays an increasingly important role in the diagnostic evaluation of thyroid disease, although it is only one of several diagnostic methods currently available. To use ultrasound effectively and economically, it is important to understand its current capabilities and limitations.

Contrast-Enhanced Ultrasound and Elastography Guidance for Needle Biopsy Guidance for Percutaneous Treatment The Incidentally Detected Nodule DIFFUSE THYROID DISEASE Acknowledgment

INSTRUMENTATION AND TECHNIQUE High-frequency transducers (7.5-15.0 MHz) currently provide both deep ultrasound penetration—up to 5 cm—and highdefinition images, with a resolution of 0.5 to 1.0 mm. No other clinically used imaging method can achieve this degree of spatial resolution. Linear array transducers with either rectangular or trapezoidal scan format are preferred to sector transducers because of the wider near field of view and the capability to combine

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Submandibular gland Internal jugular vein

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FIG. 19.1  Cervical “Map.”  Such diagrams help communicate relationships of pathology to clinicians and serve as a reference for follow-up examinations.

VII Cervical vertebrae Common carotid artery Esophagus

high-frequency gray-scale and color Doppler images. The thyroid gland is one of the most vascular organs of the body. As a result, Doppler examination may provide useful diagnostic information in some thyroid diseases. Two newer techniques used for the sonographic study of the thyroid gland are contrast-enhanced sonography and elastography. Contrast-enhanced sonography using second-generation contrast agents and very low mechanical index can provide useful information for the diagnosis of select cases of nodular disease and for ultrasound-guided therapeutic procedures. Elastography is based on the principle that when body tissues are compressed, the softer parts deform more easily than the harder parts. The amount of displacement at various depths is determined by the ultrasound signals reflected by tissues before and after they are compressed, and the corresponding strains are calculated from these displacements and displayed visually. The patient is typically examined in the supine position, with the neck extended. A small pad may be placed under the shoulders to provide better exposure of the neck, particularly in patients with a short, stocky habitus. The thyroid gland must be examined thoroughly in both transverse and longitudinal planes. Imaging of the lower poles can be enhanced by asking the patient to swallow, which momentarily raises the thyroid gland in the neck. The entire gland, including the isthmus, must be examined. The examination must also be extended laterally to include the region of the carotid artery and jugular vein to identify enlarged jugular chain lymph nodes, superiorly to visualize submandibular adenopathy, and inferiorly to define any pathologic supraclavicular lymph nodes. In addition to the images recorded during the examination, some operators include in the permanent record a diagrammatic representation of the neck showing the location(s) of any abnormal findings (Fig. 19.1). This cervical “map” helps to communicate the anatomic relationships of the pathology more clearly to the referring clinician and the patient. It also serves as a useful reference for the radiologist and sonographer for follow-up examinations.

FIG. 19.2  Normal Thyroid Gland.  (A) Transverse sonogram made with 7.5-MHz linear array transducer. (B) Corresponding anatomic drawing. C, Common carotid artery; J, jugular vein; Tr, tracheal air shadow.

Longus colli muscle

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ANATOMY The thyroid gland is located in the anteroinferior part of the neck (infrahyoid compartment) in a space outlined by muscle, trachea, esophagus, carotid arteries, and jugular veins (Fig. 19.2). The thyroid gland is made up of two lobes located along either side of the trachea and connected across the midline by the isthmus, a thin structure draping over the anterior tracheal wall at the level of the junction of the middle and lower thirds of the thyroid gland. From 10% to 40% of normal patients have a small thyroid (pyramidal) lobe arising superiorly from the isthmus and lying in front of the thyroid cartilage.1 It can be regularly visualized in younger patients, but it undergoes progressive atrophy in adulthood and becomes invisible. The size and shape of the thyroid lobes vary widely in normal patients. In tall individuals the lateral lobes have a longitudinally elongated shape on the sagittal scans, whereas in shorter individuals the gland is more oval. In the newborn the thyroid gland is 18 to 20 mm long, with an anteroposterior (AP) diameter of 8 to 9 mm. By 1 year of age, the mean length is 25 mm and AP diameter is 12 to 15 mm.2 In adults the mean length is approximately 40 to 60 mm, with mean AP diameter of 13 to 18 mm. The mean thickness of the isthmus is 4 to 6 mm.3 Sonography is an accurate method for calculating thyroid volume. In about one-third of cases, the sonographic measurement of volume differs from the estimated physical size on examination.4 Thyroid volume measurements may be useful for goiter size determination to assess the need for surgery, permit calculation of the dose of iodine-131 (131I) needed for treating thyrotoxicosis, and evaluate response to suppression treatments.5 Thyroid volume can be calculated with linear parameters or more precisely with mathematical formulas. Among the linear

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FIG. 19.3  Volume Measurement of Thyroid Gland.  (A) Transverse and (B) longitudinal images show calipers at the boundaries of thyroid gland. C, Carotid artery; Tr, trachea air shadow. The calculated thyroid volume is based on the ellipsoid formula with a correction factor (length × width × thickness × 0.52 for each lobe). In this case, the volume is 10 mL (or grams), which is within normal limits for this female patient. (C) Images from real-time three-dimensional study of normal thyroid lobe, visualized simultaneously in axial (top left), longitudinal (top right), and coronal (bottom left) planes. (D) Volumetric reconstruction of gland.

parameters, the AP diameter is the most precise because it is relatively independent of possible dimensional asymmetry between the two lobes. When the AP diameter is more than 2 cm, the thyroid gland may be considered “enlarged.” The most common mathematical method to calculate thyroid volume is based on the ellipsoid formula with a correction factor (length × width × thickness × 0.529 for each lobe)6 (Fig. 19.3A-B). With use of this method, the mean estimated error is approximately 15%. The most precise mathematical method is the integration of the cross-sectional areas of the thyroid gland, achieved through evenly spaced sonographic scans.7 With this method the mean estimated error is 5% to 10%.8 Modern threedimensional (3-D) ultrasound technology allows one to simultaneously obtain the three orthogonal planes of thyroid lobes and then to calculate the volume either automatically or manually9 (Fig. 19.3C-D). In neonates, thyroid volume ranges from 0.40 to 1.40 mL, increasing by 1.0 to 1.3 mL for each 10 kg of body weight, up to a normal volume in adults of 10 to 11 ± 3 mL.7 In general, thyroid volume is larger in patients living in regions with iodine deficiency and in patients who have acute hepatitis or chronic

renal failure. Volume is smaller in patients who have chronic hepatitis or have been treated with thyroxine or radioactive iodine.5,7 Normal thyroid parenchyma has a homogeneous, medium- to high-level echogenicity that makes detection of focal cystic or hypoechoic thyroid lesions relatively easy in most cases. The thin, hyperechoic line around the thyroid lobes is the capsule, which is often identifiable on ultrasound. It may become calcified in patients who have uremia or disorders of calcium metabolism. With currently available high-sensitivity Doppler instruments, the rich vascularity of the gland can be seen homogeneously distributed throughout the entire parenchyma (Fig. 19.4). The superior thyroid artery and vein are found at the upper pole of each lobe. The inferior thyroid vein is found at the lower pole (Fig. 19.5), and the inferior thyroid artery is located posterior to the lower third of each lobe. The mean diameter of the arteries is 1 to 2 mm; the lower veins can be up to 8 mm in diameter. Normally, peak systolic velocities reach 20 to 40 cm/ sec in the major thyroid arteries and 15 to 30 cm/sec in intraparenchymal arteries. These are the highest velocities found in blood vessels supplying superficial organs.

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The sternohyoid and omohyoid muscles (strap muscles) are seen as thin, hypoechoic bands anterior to the thyroid gland (see Fig. 19.2). The sternocleidomastoid muscle is seen as a larger oval band that lies lateral to the thyroid gland. An important anatomic landmark is the longus colli muscle, located posterior to each thyroid lobe, in close contact with the prevertebral space.

The recurrent laryngeal nerve and the inferior thyroid artery pass in the angle among the trachea, esophagus, and thyroid lobe. On longitudinal scans, the recurrent laryngeal nerve and inferior thyroid artery may be seen between the thyroid lobe and esophagus on the left and between the thyroid lobe and longus colli muscle on the right. The esophagus, primarily a midline structure, may be found laterally and is usually on the left side. It is clearly identified by the target appearance of bowel in the transverse plane and by its peristaltic movements when the patient swallows.

CONGENITAL THYROID ABNORMALITIES FIG. 19.4  Normal Thyroid Vascularity on Power Doppler Ultrasound.

Congenital conditions of the thyroid gland include aplasia of one lobe or the whole gland, varying degrees of hypoplasia, and ectopia (Fig. 19.6). Sonography can be used to help establish the diagnosis of hypoplasia by demonstrating a diminutive gland. High-frequency ultrasound can also be used in the study of congenital hypothyroidism (CH), a relatively common disorder occurring in about 1 in 3000 to 4000 live births. Determining the cause of CH (dysgenesis, dyshormonogenesis, or pituitary or hypothalamic hypothyroidism) is clinically important because prognosis and therapy differ. Early initiation of therapy can prevent mental retardation and delayed bone development.10,11 Measurement of thyroid lobes can be used to differentiate aplasia (absent gland) from goitrous hypothyroidism (gland enlargement). Radionuclide scans are more often used to detect ectopic thyroid tissue (e.g., in a lingual or suprahyoid position).

NODULAR THYROID DISEASE FIG. 19.5  Normal Inferior Thyroid Vein.  Longitudinal power Doppler image shows a large inferior thyroid vein with associated normal venous spectral waveform.

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Many thyroid diseases can manifest clinically with one or more thyroid nodules. Such nodules represent common and controversial clinical problems. Epidemiologic studies estimate that

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FIG. 19.6  Congenital Thyroid Abnormalities.  (A) Hypoplasia of right thyroid lobe. C, Carotid artery; Tr, tracheal air shadow. (B) Ectopic (sublingual) thyroid gland. Transverse ultrasound image inferior to the base of the tongue shows a U-shaped parenchymal structure.

CHAPTER 19  The Thyroid Gland 4% to 7% of adults in the United States have palpable thyroid nodules, with women affected more frequently than men.12,13 Exposure to ionizing radiation increases the incidence of benign and malignant nodules, with 20% to 30% of a radiation-exposed population having palpable thyroid disease.14,15 Although nodular thyroid disease is relatively common, thyroid cancer is rare and accounts for less than 1% of all malignant neoplasms.16 The overwhelming majority of thyroid nodules are benign. The clinical challenge is to distinguish the few clinically significant malignant nodules from the many benign nodules and thus identify patients who need surgical excision. This task is complicated because nodular disease of the thyroid gland often is clinically occult ( 1.5 cm

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Mortality

1973 1976 1979 1982 1985 1988 1991 1994 1997 2000 Year FIG. 19.43  Thyroid Cancer: Incidence Versus Mortality.  Although the rate of occurrence of thyroid cancer has more than doubled in the last 30 years, the mortality rate is unchanged over that period. (Adapted from Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA. 2006;295[18]:2164-2167.138)

surgery for nodule excision based on positive, suspicious, or nondiagnostic results, and most of these nodules are benign.101,142,143 Of these surgical patients, only 15% to 32% have cancer.101,142 Therefore the majority of patients who undergo surgery for thyroid nodule excision will have had an operation for clinically insignificant, benign nodular disease. The potential cost of the FNA biopsy workup of these nodules must be considered. For discussion purposes, assume that 1 million of the estimated 300 million people in the United States undergo a high-frequency ultrasound thyroid examination, and that one or more thyroid nodules are detected in approximately 40%. Therefore 400,000 people will have one or more thyroid nodules detected by ultrasound imaging. Assuming a cost of approximately $1500 for an ultrasound-guided FNA and cytologic analysis, $600 million could theoretically be spent to exclude or detect thyroid cancer in this group. If 18% of these FNA biopsies result in suspicious or nondiagnostic results, 72,000 procedures could occur at a cost of almost $20,000 each, for an additional cost of $1.44 billion. Finally, approximately 5%, or almost 3600 patients, could experience significant postsurgical morbidity, including hoarseness, hypoparathyroidism, and long-lasting pain.144 Clearly, this type of aggressive management of thyroid nodules would entail massive health care expenditures and could have an extremely negative clinical impact.145 4. Which incidentally discovered nodules should be pursued? Because of the many nodules detected on ultrasound, the therapeutic approach should allow most patients with clinically significant cancers to go on to further investigations. More important, it should allow most patients with benign lesions to avoid further costly, potentially harmful workup. With this goal in mind, many practices, including ours, have found that it is both impractical and imprudent to pursue the diagnosis for most of the small nodules detected incidentally on ultrasound. If technically possible, we usually obtain FNA biopsy of lesions that exhibit sonographic features strongly associated with malignancy, such as marked hypoechogenicity, taller-than-wide shape, and thick irregular margins, as well as lesions containing microcalcifications.

Nodules that have malignant features (marked hypoechogenicity, taller-than-wide shape, thick irregular margins, and/or calcifications or microcalcifications)

DIFFUSE THYROID DISEASE Several thyroid diseases are characterized by diffuse rather than focal involvement. This usually results in generalized enlargement of the gland (goiter) and no palpable nodules. Specific conditions that produce such diffuse enlargement include chronic autoimmune lymphocytic thyroiditis (Hashimoto thyroiditis), colloid or adenomatous goiter, and Graves disease. These conditions are usually diagnosed on the basis of clinical and laboratory findings and occasionally FNA biopsy. Sonography is seldom indicated. However, high-resolution sonography can be helpful when the underlying diffuse disease causes asymmetrical thyroid enlargement, which suggests a mass in the larger lobe. The sonographic finding of generalized parenchymal abnormality may alert the clinician to consider diffuse thyroid disease as the underlying cause. FNA, with sonographic guidance if necessary, can be performed if a nodule is detected. Recognition of diffuse thyroid enlargement on sonography can often be facilitated by noting the thickness of the isthmus, normally a thin bridge of tissue measuring only a few millimeters in AP dimension. With diffuse thyroid enlargement, the isthmus may be up to 1 cm or more in thickness.

Diffuse Thyroid Diseases Acute suppurative thyroiditis Subacute granulomatous thyroiditis Hashimoto thyroiditis (chronic lymphocytic thyroiditis) Adenomatous or colloid goiter Painless (silent) thyroiditis

Each type of thyroiditis, including acute suppurative thyroiditis, subacute granulomatous thyroiditis (de Quervain disease), and chronic lymphocytic thyroiditis (Hashimoto disease) has distinctive clinical and laboratory features.146 Acute suppurative thyroiditis is a rare inflammatory disease usually caused by bacterial

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infection and affecting children. Sonography can be useful in select patients to detect the development of a frank thyroid abscess. The infection usually begins in the perithyroidal soft tissues. On ultrasound images, an abscess is seen as a poorly defined, hypoechoic heterogeneous mass with internal debris, with or without septa and gas. Adjacent inflammatory nodes are often present. Subacute granulomatous thyroiditis or De Quervain disease is a spontaneously remitting inflammatory disease probably caused by viral infection. The clinical findings include fever, enlargement of the gland, and pain on palpation. Sonographically, the gland may appear enlarged and hypoechoic, with normal or decreased vascularity caused by diffuse edema of the gland, or the process may appear as focal hypoechoic regions147,148 (Fig. 19.44). Although usually not necessary, sonography can be used to assess evolution of de Quervain disease after medical therapy. The most common type of thyroiditis is chronic autoimmune lymphocytic thyroiditis, or Hashimoto thyroiditis. It typically occurs as a painless, diffuse enlargement of the thyroid gland in a young or middle-aged woman, often associated with hypothyroidism. It is the most common cause of hypothyroidism in North America. Patients with this autoimmune disease develop antibodies to their own thyroglobulin as well as to the major

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FIG. 19.44  Focal Areas of Subacute Thyroiditis.  (A) Longitudinal power Doppler image of the thyroid gland shows two poorly defined hypoechoic areas (arrows) caused by subacute thyroiditis at fine-needle aspiration. (B) Longitudinal image of a different patient shows poorly defined hypoechoic area (arrows). (C) This area has returned to normal on follow-up examination 4 weeks later after medical therapy.

enzyme of thyroid hormonogenesis, thyroid peroxidase. The typical sonographic appearance of Hashimoto thyroiditis is diffuse, coarsened, parenchymal echotexture, generally more hypoechoic than a normal thyroid144 (Fig. 19.45). In most cases the gland is enlarged. Multiple, discrete hypoechoic micronodules from 1 to 6 mm in diameter are strongly suggestive of chronic thyroiditis; this appearance has been called micronodulation (see Fig. 19.45, Video 19.7). Micronodulation is a highly sensitive sign of chronic thyroiditis, with a positive predictive value of 94.7%.149 Histologically, micronodules represent lobules of thyroid parenchyma that have been infiltrated by lymphocytes and plasma cells. These lobules are surrounded by multiple linear echogenic fibrous septations (Fig. 19.46). These fibrotic septations may give the parenchyma a “pseudolobulated” appearance. Both benign and malignant thyroid nodules may coexist with chronic lymphocytic thyroiditis, and FNA is often necessary to establish the final diagnosis150 (Figs. 19.47 to 19.49). As with other autoimmune disorders, there is an increased risk of malignancy, with a B-cell malignant lymphoma most often arising within the gland. The vascularity on color Doppler imaging is normal or decreased in most patients with the diagnosis of Hashimoto thyroiditis (see Fig. 19.45). Occasionally, hypervascularity similar to the “thyroid inferno” of Graves disease occurs. One study

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FIG. 19.45  Hashimoto Thyroiditis: Micronodularity.  (A) Transverse and (B) longitudinal images of the left lobe demonstrate multiple small hypoechoic nodules that are lymphocyte infiltration of the parenchyma. (C) and (D) Longitudinal images of another patient show multiple tiny hypoechoic nodules and increased flow on power Doppler. This increased flow may indicate an acute phase of the thyroiditis. (E) and (F) Longitudinal images of a different patient show multiple tiny hypoechoic nodules and decreased flow on color Doppler scan. The blood flow is normal or diminished in most cases of Hashimoto thyroiditis.

suggested that hypervascularity occurs when hypothyroidism develops, perhaps related to stimulation from the associated high serum levels of thyrotropin (TSH).151 Often, cervical lymphadenopathy is present, most evident near the lower pole of the thyroid gland (Fig. 19.50). The end stage of chronic thyroiditis is atrophy, when the thyroid gland is small, with poorly defined margins and heterogeneous texture caused by progressive fibrosis. Blood

flow signals are absent. Occasionally, discrete nodules occur, and FNA biopsy is needed to establish the diagnosis.150 Painless (silent) thyroiditis has the typical histologic and sonographic pattern of chronic autoimmune thyroiditis (hypoechogenicity, micronodulation, and fibrosis), but clinical findings resemble classic subacute thyroiditis, with the exception of node tenderness. Moderate hyperthyroidism with thyroid

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FIG. 19.46  Hashimoto Thyroiditis: Coarse Septations.  (A) Transverse dual image of the thyroid shows marked diffuse enlargement of both lobes and the isthmus. Multiple linear bright echoes throughout the hypoechoic parenchyma are caused by lymphocytic infiltration of the gland with coarse septations from fibrous bands. Tr, Tracheal air shadow. (B) Transverse and (C) longitudinal images of another patient demonstrate linear echogenic septations throughout the gland. (D) Longitudinal image of another patient shows thicker echogenic linear areas that separate hypoechoic regions.

FIG. 19.47  Hashimoto Thyroiditis: Nodule.  Longitudinal image shows a discrete hypoechoic nodule (arrows) that proved to be Hashimoto thyroiditis at fine-needle aspiration biopsy.

FIG. 19.48  Hashimoto Thyroiditis With Papillary Thyroid Cancer.  Longitudinal image shows classic Hashimoto thyroiditis (micronodularity) and a hypoechoic dominant nodule (arrow) in the upper pole caused by papillary thyroid carcinoma. A dominant nodule in Hashimoto thyroiditis should be considered “indeterminate” and fineneedle aspiration performed.

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A

FIG. 19.49  Lymphoma in Hashimoto Thyroiditis.  Transverse image of the left lobe shows diffuse hypoechoic enlargement caused by lymphoma in a gland with Hashimoto thyroiditis. Tr, Tracheal air shadow.

B FIG. 19.51  Hyperthyroidism: Graves Disease.  (A) Transverse dual image of the thyroid gland shows marked diffuse enlargement of both thyroid lobes and the isthmus. The gland is diffusely hypoechoic. (B) Transverse color Doppler image of the left lobe shows increased vascularity, indicating an acute stage of the Graves disease process. Tr, Trachea.

FIG. 19.50  Hashimoto Thyroiditis With Hyperplastic Enlarged Lymph Nodes.  Longitudinal image shows micronodularity of Hashimoto thyroiditis and an enlarged lymph node (arrow) inferior to the lower pole.

enlargement usually occurs in the early phase, in some cases followed by hypothyroidism of variable degree. In postpartum thyroiditis the progression to hypothyroidism is more common. In most cases the disease spontaneously remits within 3 to 6 months, and the gland may return to a normal appearance. Although the appearance of diffuse parenchymal inhomogeneity and micronodularity is typical of Hashimoto thyroiditis, other diffuse thyroid diseases, most frequently multinodular or adenomatous goiter, may have a similar sonographic appearance. Most patients with adenomatous goiter have multiple discrete nodules separated by otherwise normal-appearing thyroid parenchyma (see Fig. 19.29); others have enlargement with rounding of the poles of the gland, diffuse parenchymal inhomogeneity, and no recognizable normal tissue. Adenomatous goiter affects women three times more often than men.

Graves disease is a common diffuse abnormality of the thyroid gland and is usually biochemically characterized by hyperfunction (thyrotoxicosis). The echotexture may be more inhomogeneous than in diffuse goiter, mainly because of numerous large, intraparenchymal vessels. Furthermore, especially in young patients, the parenchyma may be diffusely hypoechoic because of the extensive lymphocytic infiltration or the predominantly cellular content of the parenchyma, which becomes almost devoid of colloid substance. Color Doppler sonography often demonstrates a hypervascular pattern referred to as the thyroid inferno (Fig. 19.51). Spectral Doppler will often demonstrate peak systolic velocities exceeding 70 cm/sec, which is the highest velocity found in thyroid disease. There is no correlation between the degree of thyroid hyperfunction assessed by laboratory studies and the extent of hypervascularity or blood flow velocities. Previous studies have shown that Doppler analysis can be used to monitor therapeutic response in patients with Graves disease.152 A significant decrease in flow velocities in the superior and inferior thyroid arteries after medical treatment has been reported. The rarest type of inflammatory thyroid disease is invasive fibrous thyroiditis, also called Riedel struma.146 This disease primarily affects women and often progresses to complete destruction of the gland. Some cases may be associated with

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A

B

C FIG. 19.52  Riedel Struma (Invasive Fibrous Thyroiditis).  (A) Transverse dual-color Doppler ultrasound image of the thyroid shows a diffuse hypoechoic process in the right lobe extending around the common carotid artery (arrows). Tr, Trachea. (B) Longitudinal power Doppler image of the right common carotid artery shows a hypoechoic soft tissue mass (arrows) encasing the vessel. (C) Contrast-enhanced CT scan shows mild enlargement of the right thyroid lobe and soft tissue thickening (arrows) around the right common carotid artery. Incidentally noted is dilation of the air-filled esophagus (E).

mediastinal or retroperitoneal fibrosis or sclerosing cholangitis. In the few cases of invasive fibrous thyroiditis examined sonographically, the gland was diffusely enlarged and had an inhomogeneous parenchymal echotexture. The primary reason for sonography is to check for extrathyroid extension of the inflammatory process, with encasement of the adjacent vessels (Fig. 19.52). Such information can be particularly useful in surgical planning. Open biopsy is generally required to distinguish this condition from anaplastic thyroid carcinoma. The sonographic findings in these two diseases may be identical.

Acknowledgment The authors would like to acknowledge the aid of Maija Radzina, MD, PhD, Institute of Diagnostic Radiology, Paula Stradins Clinical University Hospital, Riga, Latvia.

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137. Harach HR, Franssila KO, Wasenius VM. Occult papillary carcinoma of the thyroid. A “normal” finding in Finland. A systematic autopsy study. Cancer. 1985;56(3):531-538. 138. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA. 2006;295(18):2164-2167. 139. Ross DS. Editorial: predicting thyroid malignancy. J Clin Endocrinol Metab. 2006;91(11):4253-4255. 140. Burch HB. Evaluation and management of the solid thyroid nodule. Endocrinol Metab Clin North Am. 1995;24(4):663-710. 141. Goellner J. Fine-needle aspiration of the thyroid gland. In: Erosan YS, Bonfiglio TA, editors. Fine-needle aspiration of subcutaneous organs and masses. Philadelphia: Lippincott-Raven; 1996. p. 81-98. 142. Haas S, Trujillo A, Kunstle J. Fine needle aspiration of thyroid nodules in a rural setting. Am J Med. 1993;94(4):357-361. 143. Spiliotis J, Scopa CD, Gatopoulou C, et al. Diagnosis of thyroid cancer in southwestern Greece. Bull Cancer. 1991;78(10):953-959. 144. Songun I, Kievit J, Wobbes T, et al. Extent of thyroidectomy in nodular thyroid disease. Eur J Surg. 1999;165(9):839-842. 145. Reading CC, Charboneau JW, Hay ID, Sebo TJ. Sonography of thyroid nodules: a “classic pattern” diagnostic approach. Ultrasound Q. 2005;21(3): 157-165. 146. Hay ID. Thyroiditis: a clinical update. Mayo Clin Proc. 1985;60(12): 836-843. 147. Adams H, Jones MC. Ultrasound appearances of de Quervain’s thyroiditis. Clin Radiol. 1990;42(3):217-218. 148. Birchall IW, Chow CC, Metreweli C. Ultrasound appearances of de Quervain’s thyroiditis. Clin Radiol. 1990;41(1):57-59. 149. Yeh HC, Futterweit W, Gilbert P. Micronodulation: ultrasonographic sign of Hashimoto thyroiditis. J Ultrasound Med. 1996;15(12):813819. 150. Takashima S, Matsuzuka F, Nagareda T, et al. Thyroid nodules associated with Hashimoto thyroiditis: assessment with US. Radiology. 1992;185(1): 125-130. 151. Lagalla R, Caruso G, Benza I, et al. [Echo-color Doppler in the study of hypothyroidism in the adult]. Radiol Med. 1993;86(3):281-283. 152. Castagnone D, Rivolta R, Rescalli S, et al. Color Doppler sonography in Graves’ disease: value in assessing activity of disease and predicting outcome. AJR Am J Roentgenol. 1996;166(1):203-207.

CHAPTER

20

 

The Parathyroid Glands Bonnie J. Huppert and Carl Reading

SUMMARY OF KEY POINTS • In the vast majority of cases, primary hyperparathyroidism is caused by hyperfunction of a single parathyroid gland due to adenoma, much less commonly due to multiple gland involvement. • Surgical removal of the abnormal gland is the only definitive treatment for primary hyperparathyroidism, and selective, minimally invasive surgical techniques are most commonly used for first-time surgery. • The role of parathyroid imaging is not in the diagnosis of primary hyperparathyroidism but rather to provide accurate adenoma localization to successfully direct selective surgical parathyroid resection. • When used by an experienced examiner, parathyroid sonography can provide high-resolution anatomic imaging

with good sensitivity and accuracy which is noninvasive, lacks radiation exposure, is relatively low cost, and has the added ability to assess for concomitant thyroid disease prior to surgery. • In persistent or recurrent hyperparathyroidism, liberal use of multimodality preoperative imaging is particularly beneficial prior to reoperation. • In selected cases, ultrasound can also be used to guide biopsy of suspected parathyroid adenomas to provide preoperative confirmation and to guide ablation of abnormal parathyroid glands in patients who are not surgical candidates.

CHAPTER OUTLINE EMBRYOLOGY AND ANATOMY PRIMARY HYPERPARATHYROIDISM Prevalence Diagnosis Pathology Treatment SONOGRAPHIC APPEARANCE Shape Echogenicity and Internal Architecture Vascularity Size Multiple Gland Disease Carcinoma

H

ADENOMA LOCALIZATION Sonographic Examination and Typical Locations Ectopic Locations Retrotracheal/Retroesophageal Adenoma Mediastinal Adenoma Intrathyroid Adenoma Carotid Sheath/Undescended Adenoma PERSISTENT OR RECURRENT HYPERPARATHYROIDISM SECONDARY HYPERPARATHYROIDISM

igh-frequency sonography is a well-established, noninvasive imaging method used in the evaluation and treatment of patients with parathyroid disease. Sonography is often used for the preoperative localization of enlarged parathyroid glands or adenomas in patients with hyperparathyroidism. Ultrasound is also used to guide the percutaneous biopsy of suspected parathyroid adenomas or enlarged glands, particularly in patients with persistent or recurrent hyperparathyroidism, as well as in some patients with suspected ectopic glands. In select patients, sonography can be used to guide the percutaneous ethanol

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PITFALLS IN INTERPRETATION False-Positive Examination False-Negative Examination ACCURACY IN IMAGING Ultrasound Other Modalities Importance of Imaging in Primary Hyperparathyroidism INTRAOPERATIVE SONOGRAPHY PERCUTANEOUS BIOPSY ETHANOL ABLATION

ablation of parathyroid adenomas as an alternative to surgical treatment.

EMBRYOLOGY AND ANATOMY The paired superior and inferior parathyroid glands have different embryologic origins, and knowledge of their development aids in understanding their ultimate anatomic locations.1-3 The superior parathyroid glands arise from the paired fourth branchial pouches (clefts), along with the lateral lobes of the

CHAPTER 20  The Parathyroid Glands thyroid gland. Minimal migration occurs during fetal development, and the superior parathyroids usually remain associated with the posterior aspect of the middle to upper portion of the thyroid gland. The majority of superior parathyroid glands (>80%) are found at autopsy within a 2-cm area located just superior to the crossing of the recurrent laryngeal nerve and the inferior thyroid artery.4 The inferior parathyroid glands arise from the paired third branchial pouches, along with the thymus.2 During fetal development, these “parathymus glands” migrate caudally along with the thymus in a more anterior plane than their superior counterparts, bypassing the superior glands to become the inferior parathyroid glands.3 Because of their greater caudal migration, the inferior parathyroid glands are more variable in location than the superior glands and can be found anywhere from the angle of the mandible to the pericardium. The majority of inferior parathyroid glands (>60%) come to rest at or just inferior to the posterior aspect of the lower pole of the thyroid4 (Fig. 20.1). A significant percentage of parathyroid glands lie in relatively or frankly ectopic locations in the neck or mediastinum. Symmetry to fixed landmarks occurs in 70% to 80%, so side-to-side comparisons can often be made.3,4 The ectopic superior parathyroid gland usually lies posterior to the esophagus or in the

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tracheoesophageal groove, in the retropharyngeal space, or has continued its descent from the posterior neck into the posterosuperior mediastinum.5,6 Superior glands are less often found higher in the neck, near the superior extent of the thyroid, or, in rare cases, surrounded by thyroid tissue within the thyroid capsule.4 The inferior parathyroid gland is more frequently ectopic than its superior counterpart.4,6 About 25% of the inferior glands fail to completely dissociate from the thymus and continue to migrate in an anterocaudal direction and are found in the low neck along the thyrothymic ligament or embedded within or adjacent to the thymus in the low neck and anterosuperior mediastinum. Less common ectopic positions of the inferior parathyroid glands include an undescended position high in the neck anterior to the carotid bifurcation associated with a remnant of thymus, and lower in the neck along or within the carotid sheath.7 In other rare cases, ectopic glands have also been reported in the mediastinum posterior to the esophagus or carina, in the aortopulmonic window, within the pericardium, or even far laterally within the posterior triangle of the neck. Most adults have four parathyroid glands, two superior and two inferior, each measuring about 5 × 3 × 1 mm and weighing on average 35 to 40 mg (range, 10-78 mg).3,8 Supernumerary glands (>4) may be present and result from the separation of parathyroid anlage when the glands pull away from the pouch structures during the embryologic branchial complex phase.9,10 These supernumerary glands are often associated with the thymus in the anterior mediastinum, suggesting a relationship in their development with the inferior parathyroid glands.11 Supernumerary glands have been reported in 13% of the population at autopsy studies3,4; however, many of these are small, rudimentary or split glands. “Proper” supernumerary glands (>5 mg and located well away from the other four glands) are found in 5% of cases. The presence of fewer than four parathyroid glands is rare clinically but has been reported in 3% at autopsy. Normal parathyroid glands vary from a yellow to a red-brown color, depending on the degree of vascularity and the relative content of yellow parenchymal fat and chief cells.8 The chief cells are the primary source for the production of parathyroid hormone (PTH, parathormone). The percentage of glandular fat typically increases with age or with disuse atrophy. Hyperfunctioning glands resulting from adenomas or hyperplasia contain relatively little fat and are vascular, thus more reddish. The glands are generally oval or bean shaped but may be spherical, lobular, elongated, or flattened. Although normal parathyroid glands are occasionally seen with high-frequency ultrasound,12,13 typically they are not visualized, likely because of their small size, deep location, and poor conspicuity related to increased glandular fat. Eutopic parathyroid glands typically derive their major blood supply from branches of the inferior thyroid artery, with a lesser and variable contribution to the superior glands from the superior thyroid artery.3,7

PRIMARY HYPERPARATHYROIDISM FIG. 20.1  Location of Parathyroid Glands.  Frequency of the location of normal superior and inferior parathyroid glands. Anatomic drawing from 527 autopsies. T, Thymus. (Modified from Gilmour JR. The gross anatomy of the parathyroid glands. J Pathol 1938;46:133-148.1)

Prevalence Primary hyperparathyroidism is a common endocrine disease, with prevalence in the United States of 1 to 2 per 1000

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population.14 Women are affected two to three times more frequently than men, particularly after menopause. More than half of patients with primary hyperparathyroidism are older than 50 years, and cases are rare in those younger than age 20.

Diagnosis Primary hyperparathyroidism is usually suspected because an increased serum calcium level is detected on routine biochemical screening. Elevated ionized serum calcium level, hypophosphatasia, and hypercalciuria may be further biochemical clues to the disease. A serum PTH level that is “inappropriately high” for the corresponding serum calcium level confirms the diagnosis. Even when the PTH level is within the upper limits of the normal range in a hypercalcemic patient, the diagnosis of primary hyperparathyroidism should still be suspected, since hypercalcemia from other nonparathyroid causes (including malignancy) should suppress the glandular function and decrease the serum PTH level. Because of earlier detection by increasingly routine laboratory tests, the later “classic” signs of hyperparathyroidism, such as “painful bones, renal stones, abdominal groans, and psychic moans,” are often not present. Many patients are diagnosed before severe manifestations of hyperparathyroidism, such as nephrolithiasis, osteopenia, subperiosteal resorption, and osteitis fibrosis cystica. In general, patients rarely have obvious symptoms unless their serum calcium level exceeds 12 mg/dL. However, subtle nonspecific symptoms, such as muscle weakness, malaise, constipation, dyspepsia, polydipsia, and polyuria, may be elicited from these otherwise asymptomatic patients by more specific questioning.

Pathology Primary hyperparathyroidism is caused by a single adenoma in 80% to 90% of cases, by multiple gland enlargement in 10% to 20%, and by carcinoma in less than 1%.6,15,16 A solitary adenoma may involve any one of the four glands. Multigland enlargement most often results from primary parathyroid hyperplasia and less often from multiple adenomas. Hyperplasia usually involves all four glands asymmetrically, whereas multiple adenomas may involve two or possibly three glands. An adenoma and hyperplasia cannot always be reliably distinguished histologically, and the sample may be referred to as “hypercellular parathyroid” tissue. Because of this inconsistent pattern of gland involvement, and because distinguishing hyperplasia from multiple adenomas is difficult pathologically, these two entities are often histologically considered together as “multiple gland disease.”17

Causes of Primary Hyperparathyroidism Type of Disease

Percentage

Single adenoma Multiple gland disease Carcinoma

80%-90% 10%-20% 14 mg/dL). The diagnosis is often made at operation when the surgeon discovers an enlarged, firm gland that is adherent to the surrounding tissues due to local invasion. A thick, fibrotic capsule is often present. Treatment consists of en bloc resection without entering the capsule, to prevent tumor seeding. In many cases, cure may not be possible because of the invasive and metastatic nature of the disease. Generally, death occurs not from tumor spread but from complications associated with unrelenting hyperparathyroidism.

Treatment No effective definitive medical therapies are available for the treatment of primary hyperparathyroidism. Medications utilized include short-term hypocalcemic agents such as calcitonin and calcimimetics (calcium-sensing receptor agonists) such as cinacalcet. The bisphosphonates aid in preventing bone mass loss. Synthetic vitamin D analogs such as paricalcitol are mainly used in the treatment of secondary hyperparathyroidism. Surgery is the only definitive treatment for primary hyperparathyroidism. Studies demonstrate that surgical cure rates by an experienced surgeon are greater than 95%, and the morbidity and mortality rates are extremely low.24,25 Therefore in symptomatic patients with primary hyperparathyroidism, the treatment of choice is surgical excision of the involved parathyroid gland or glands.

CHAPTER 20  The Parathyroid Glands

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FIG. 20.2  Typical Parathyroid Adenoma.  (A) Transverse and (B) longitudinal sonograms of a typical adenoma (arrows) located adjacent to the posterior aspect of the thyroid (T). C, Common carotid artery; J, internal jugular vein; Tr, trachea.

However, since in current practice, most cases of primary hyperparathyroidism are discovered in the early stages of the disease, some controversy exists as to whether asymptomatic patients with minimal hypercalcemia should be treated surgically, or followed medically with frequent measurements of bone density, serum calcium levels, and urinary calcium excretion and monitoring for nephrolithiasis.26 Recommendations for the management of asymptomatic primary hyperparathyroidism have been outlined in various articles, many of which are based on International Workshop and National Institutes of Health (NIH) Consensus Conference statements and subsequent updates. This area continues to evolve, and approaches to treatment may differ slightly among clinical practices.24-31

SONOGRAPHIC APPEARANCE Shape Parathyroid adenomas are typically oval or bean shaped (Fig. 20.2). As parathyroid glands enlarge, they dissect between longitudinally oriented tissue planes in the neck and acquire a characteristic oblong shape. If this process is exaggerated, they can become tubular or flattened. There is often asymmetry in the enlargement, and the cephalic and/or caudal end can be more bulbous, producing a triangular, tapering, teardrop or bilobed shape.19,32-34

Echogenicity and Internal Architecture The echogenicity of most parathyroid adenomas is substantially less than that of normal thyroid tissue (Fig. 20.3). The characteristic hypoechoic appearance of parathyroid adenomas is caused by the uniform hypercellularity of the gland with little fat content, which leaves few interfaces for reflecting sound. Occasionally, adenomas have a heterogeneous appearance, with areas of increased and decreased echogenicity. The rare, functioning parathyroid lipoadenomas are more echogenic than the adjacent thyroid gland because of their high fat content35 (Fig. 20.3G). A great majority of parathyroid adenomas are homogeneously solid. About 2% have internal cystic components resulting from cystic degeneration (most often) or true simple cysts (less often)36-38 (Fig. 20.3E and F, Video 20.1). Adenomas may rarely contain internal calcification (Fig. 20.3H and I).

Vascularity Color flow, spectral, and power Doppler sonography of an enlarged parathyroid gland may demonstrate a hypervascular pattern with prominent diastolic flow (Fig. 20.4). An enlarged extrathyroidal artery, often originating from branches of the inferior thyroidal artery, may be visualized supplying the adenoma with its insertion along the long-axis pole.39-44 A finding described in parathyroid adenomas is a vascular arc, which envelops 90 to 270 degrees of the mass. This vascular flow pattern may increase the sensitivity of initial detection of parathyroid adenomas and aid in confirming the diagnosis by allowing for differentiation from lymph nodes, which have a central hilar flow pattern. Asymmetric increased vascular flow may also be present in the thyroid gland adjacent to a parathyroid adenoma.

Size Most parathyroid adenomas are 0.8 to 1.5 cm long and weigh 500 to 1000 mg. The smallest adenomas can be minimally enlarged glands that appear virtually normal during surgery but are found to be hypercellular on pathologic examination (Fig. 20.5, Video 20.2). Large adenomas can be 5 cm or more in length and weigh more than 10 g. Preoperative serum calcium levels are usually higher in patients with larger adenomas.32

Multiple Gland Disease Multiple gland disease may be caused by diffuse hyperplasia or multiple adenomas. Individually, these enlarged glands may have the same sonographic and gross appearance as other parathyroid adenomas (Fig. 20.6, Videos 20.3 and 20.4). However, the glands may be inconsistently and asymmetrically enlarged, and the diagnosis of multigland disease can be difficult to make sonographically. For example, if one gland is much larger than the others, the appearance may be misinterpreted as solitary adenomatous disease. Alternatively, if multiple glands are only minimally enlarged, the diagnosis may be missed altogether.

Carcinoma Carcinomas are usually larger than adenomas.45-47 Carcinomas often measure more than 2 cm compared with about 1 cm for adenomas (Fig. 20.7). On ultrasound, carcinomas also frequently have a lobular contour, heterogeneous internal architecture, and internal cystic components. However, large adenomas may also

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FIG. 20.3  Spectrum of Echogenicity and Internal Architecture of Parathyroid Adenomas and Enlarged Hyperplastic Glands.  Longitudinal sonograms. (A) Typical homogeneous hypoechoic appearance of a parathyroid adenoma (arrows) with respect to the overlying thyroid tissue. (B) Highly hypoechoic solid adenoma. (C) Mixed-geographic echogenicity. The adenoma is hyperechoic in its cranial portion and hypoechoic in its caudal portion. (D) An adenoma with diffusely heterogeneous echogenicity. (E) Partial cystic change. An ectopic adenoma posterior to the jugular vein (J) has both solid and cystic components. (F) Completely cystic 2-cm adenoma (calipers) near the lower pole of the thyroid (T). See also Video 20.1. (G) A lipoadenoma is more echogenic than the adjacent lower pole thyroid tissue. (H) Enlarged parathyroid gland with small, nonshadowing calcifications in the setting of secondary hyperparathyroidism related to chronic renal failure. (I) Enlarged parathyroid gland with densely shadowing peripheral calcifications in the setting of secondary hyperparathyroidism.

have these features. In many cases, carcinomas are indistinguishable sonographically from large, benign adenomas.45 Some authors report that a depth-to-width ratio of 1 or greater is a sonographic feature more associated with carcinoma than with adenoma, with sensitivity and specificity of 94% and 95%, respectively.47 Gross evidence of invasion of adjacent structures, such as vessels or muscles, is a reliable preoperative sonographic criterion for the diagnosis of malignancy, but this is an uncommon finding.

ADENOMA LOCALIZATION Sonographic Examination and Typical Locations The sonographic examination of the neck for parathyroid adenoma localization is performed with the patient supine. The patient’s neck is hyperextended by a pad centered under the scapulae, and the examiner usually sits at the patient’s head. High-frequency

CHAPTER 20  The Parathyroid Glands

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FIG. 20.4  Typical Hypervascularity of Parathyroid Adenoma.  (A) Transverse gray-scale and (B) transverse and (C) longitudinal power Doppler ultrasound images show hypervascularity of a parathyroid adenoma with polar feeding vessel and prominent peripheral vascular arcs.

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FIG. 20.5  Spectrum of Size of Parathyroid Adenomas.  Longitudinal sonograms. (A) Minimally enlarged, 0.5 × 0.2–cm parathyroid adenoma (calipers). See also Video 20.2. (B) Typical midsized, 1.5 × 0.6–cm, 400-mg adenoma (arrow). (C) Large, 3.5 × 2–cm, >4000-mg adenoma (calipers).

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FIG. 20.6  Multiple Gland Disease.  (A) Longitudinal sonogram of the right neck shows superior and inferior parathyroid gland enlargement (arrows) in the setting of secondary hyperparathyroidism, which can be difficult to distinguish from multiple adenomas. T, Thyroid. (B) Transverse sonogram in another patient shows enlargement of bilateral superior parathyroid glands in the setting of secondary hyperparathyroidism. C, Common carotid artery; Tr, trachea. See also Videos 20.3 and 20.4.

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FIG. 20.7  Parathyroid Carcinoma.  (A) Longitudinal sonogram shows heterogeneous 4-cm parathyroid carcinoma (arrow) located near tip of lower pole of the left thyroid lobe (T). (B) Transverse sonogram with color Doppler flow imaging shows prominent internal vascularity of the carcinoma. C, Common carotid artery. (C) Longitudinal sonogram in another patient shows lobulated, solid and cystic, 4-cm parathyroid carcinoma (arrows) adjacent to the lower pole of the thyroid. (D) Longitudinal sonogram in another patient shows a 3-cm heterogeneous solid low-grade parathyroid carcinoma (calipers) with irregular lobulated margins (arrows) posterior to the thyroid.

transducers (6-15 MHz and 8-18 MHz) are used to provide optimal spatial resolution and visualization in most patients; the highest frequency possible should be used that still allows for tissue penetration to visualize the deeper structures, such as the longus colli muscles. In obese patients with thick necks or with large multinodular thyroid glands, use of a 5- to 8-MHz transducer may be necessary to obtain adequate depth of penetration.

The pattern of the sonographic survey of the neck for adenoma localization can be considered in terms of the pattern of dissection and visualization that the surgeon uses in a thorough neck exploration. The typical superior parathyroid adenoma is usually adjacent to the posterior aspect of the midportion of the thyroid (Fig. 20.8, Videos 20.5 and 20.6). The location of the typical inferior parathyroid adenoma is more variable but usually lies

CHAPTER 20  The Parathyroid Glands

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FIG. 20.8  Superior Parathyroid Adenoma.  (A) Longitudinal and (B) transverse sonograms show an adenoma (arrows) adjacent to the posterior aspect of the midportion of the left lobe of the thyroid (T). C, Common carotid artery; E, esophagus; Tr, trachea. See also Videos 20.5 and 20.6.

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FIG. 20.9  Inferior Parathyroid Adenoma.  (A) Longitudinal and (B) transverse sonograms show an adenoma (arrows) adjacent to lower pole of right lobe of the thyroid (T). C, Common carotid artery; Tr, trachea. See also Videos 20.7 and 20.8.

close to the lower pole of the thyroid (Fig. 20.9, Videos 20.7 and 20.8). Most of these inferior adenomas are adjacent to the posterior aspect of the lower pole of the thyroid, and the rest are in the soft tissues 1 to 2 cm inferior to the thyroid. Therefore the examination is initiated on one side of the neck, centered in the region of the thyroid gland, with the focal zone placed deep to the thyroid. High-resolution gray-scale images are obtained in the transverse (axial) and longitudinal (sagittal) planes. Any potential parathyroid adenomas detected in the transverse scan plane must be confirmed by longitudinal imaging to prevent mistaking other structures for an adenoma. Some authors recommend the use of compression of the superficial soft tissues to aid in adenoma detection.12,43,48 This has been described as “graded” compression with the transducer to effect minimal deformity of the overlying subcutaneous tissues and strap muscles and increase the conspicuity of deeper, smaller adenomas (2-10% >10%-≤50% >50%-2-3 mm and increasing in size with Valsalva maneuver or standing) of the pampiniform plexus located posterior to the testis.

CHAPTER OUTLINE SONOGRAPHIC TECHNIQUE NORMAL ANATOMY INTRATESTICULAR SCROTAL MASSES Malignant Tumors Germ Cell Tumors Non–Germ Cell Tumors Testicular Metastases Lymphoma and Leukemia Extramedullary Myeloma Metastatic Disease Benign Intratesticular Lesions Cysts Tubular Ectasia of Rete Testis Cystic Dysplasia Epidermoid Cysts

D

Abscess Segmental Infarction Adrenal Rests Splenogonadal Fusion Calcifications EXTRATESTICULAR PATHOLOGIC LESIONS Tunica Vaginalis Hydrocele, Hematocele, and Pyocele Paratesticular Masses Hernia Calculi Varicocele Fibrous Pseudotumor Polyorchidism

iagnostic ultrasound is the most common imaging technique used to supplement the physical examination of the scrotum and is an accurate means of evaluating many scrotal processes. Technical advancements in high-resolution real-time sonography and the ability of color and power Doppler sonography to evaluate testicular perfusion have improved and expanded the clinical applications of scrotal sonography to include (among other indications) assessment of scrotal masses, evaluation of acute scrotal pain, evaluation of scrotal trauma, assessment of varicoceles in the infertility workup, assessment for tumors and metastatic disease, and evaluation of an undescended testis.

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Epididymal Lesions Cystic Lesions Tumors Sperm Granuloma Postvasectomy Changes in the Epididymis Chronic Epididymitis Sarcoidosis ACUTE SCROTAL PAIN Torsion Epididymitis and Epididymo-orchitis Fournier Gangrene TRAUMA CRYPTORCHIDISM

SONOGRAPHIC TECHNIQUE Scrotal ultrasound examination is performed with the patient in the supine position. The scrotum is elevated on top of a towel draped over the thighs, and the penis is placed on the patient’s abdomen and covered with a towel. Optimal results are typically obtained with a high-frequency (14-18 MHz) linear array transducer. If greater penetration is needed because of scrotal swelling, a lower-frequency transducer may be used. A directcontact scan is performed using acoustic coupling gel. Images of both testes are obtained in transverse and sagittal planes. The

CHAPTER 22  The Scrotum Scrotal Sonography: Current Uses Evaluation of location and characteristics of scrotal masses Evaluation of acute scrotal pain Evaluation of scrotal trauma, including surgical or iatrogenic injury Evaluation for varicoceles in infertile men Evaluation of testicular ischemia with color and power Doppler sonography Follow-up of patients with previous testicular neoplasms, lymphoma, or leukemia Detection of occult primary tumor in patients with known metastatic disease Localization of the undescended testis

Spermatic cord

Testicular artery Pampiniform plexus Head of epididymis Efferent ductules

Septa Seminiferous tubules

size and appearance of each testis and epididymis should be noted and compared to the contralateral structures. Color and pulsed Doppler parameters should be optimized to evaluate for low flow velocities and to demonstrate blood flow in the testes and surrounding structures. Transverse images including portions of both testes should be acquired in gray-scale and color Doppler modes to demonstrate symmetry. Scrotal structures should be examined thoroughly to evaluate for extratesticular masses or processes. Additional techniques, such as upright positioning of the patient or performing the Valsalva maneuver, may be used to evaluate venous vascularity for varicocele or for inguinal hernia assessment.

NORMAL ANATOMY The normal scrotal wall consists of the epidermis, superficial dartos muscle, dartos fascia, external spermatic fascia, cremasteric muscle and fascia, and internal spermatic fascia. The scrotum is a fibromuscular sac that is divided by the midline raphe, forming a right and left hemiscrotum. Each hemiscrotum contains a testis, epididymis, spermatic cord, and vascular and lymphatic networks (Fig. 22.1). The two layers of the tunica vaginalis separate the testis from much of the scrotal wall and form an isolated mesothelial lined sac.1,2 During embryologic development, the tunica vaginalis arises from the processus vaginalis, an outpouching of fetal peritoneum that accompanies the testis in its descent into the scrotum. The upper portion of the processus vaginalis, extending from the internal inguinal ring to the upper pole of the testis, is normally obliterated. The lower portion, the tunica vaginalis, remains as a closed pouch within each hemiscrotum, partially folded around the testis. Only the posterior aspect of the testis, the site of attachment of the testis and epididymis, is not in continuity with the tunica vaginalis. The inner or visceral layer of the tunica vaginalis covers the testis, epididymis, and lower portion of the spermatic cord. The outer or parietal layer of the tunica vaginalis lines the walls of the scrotal pouch and is attached to the fascial coverings of the testis. A small amount of fluid is normally present between these two layers.3

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Tunica albuginea

Cremasteric artery Vas deferens Deferential artery Rete testes

Body of epididymis

Tunica vaginalis Tail of epididymis FIG. 22.1  Normal Intrascrotal Anatomy.  (With permission from Sudakoff GS, Quiroz F, Karcaaltincaba M, Foley WD. Scrotal ultrasonography with emphasis on the extratesticular space: anatomy, embryology, and pathology. Ultrasound Q. 2002;18[4]:255-273.78)

The fibrous tunica albuginea covers and protects the testis. Posteromedially, the tunica albuginea projects inward into the testis to form the mediastinum. Numerous fibrous septations project inward from the mediastinum, dividing the testis into 250 to 400 lobules. Each lobule consists of one to three seminiferous tubules supporting the Sertoli cells and spermatocytes. The Leydig cells are adjacent to the tubules, within the loose interstitial tissue, and are responsible for testosterone secretion. The adult testes are ovoid glands measuring 3 to 5 cm in length, 2 to 4 cm in width, and 3 cm in anteroposterior dimension. Testicular size and weight decrease with age.3,4 Sonographically, the normal testis has relatively homogeneous, medium-level, granular echotexture (Fig. 22.2A). Prepubertal testes are typically less echogenic than postpubertal testes secondary to incomplete maturation of the germ cell elements and tubules.5 The tunica (tunica vaginalis and tunica albuginea) can often be seen as an echogenic outline of the testes. Where the tunica invaginates to form the mediastinum testis, the mediastinum testis is sometimes seen as a linear echogenic band extending craniocaudally within the testis (Fig. 22.2C). Its appearance varies according to the amount of fibrous and fatty tissue present. The fibrous septum, or septula testis, may be seen as a linear echogenic or hypoechoic structure (Fig. 22.2B). The seminiferous tubules converge to form larger tubuli recti, which open into the dilated spaces of the rete testis. The normal rete testis can be identified in 20% of patients as a hypoechoic region near the mediastinum.6 The rete testis drains into the epididymal head via 15 to 20 efferent ductules. The epididymis is a curved structure measuring 6 to 7 cm in length and lying posterolateral to the testis. It is composed

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FIG. 22.2  Normal Intrascrotal Anatomy.  Longitudinal scans show (A) normal homogeneous echotexture of the testis; (B) striated appearance of the septula testis; (C) mediastinum testis (arrow) as a linear echogenic band of fibrofatty tissue; (D) head (white arrow) and body (black arrow) of epididymis; (E) hydrocele (H) and appendix testis (arrow); and (F) appendages of epididymis (arrows). (G) Color Doppler scan shows normal testicular arteries. (H) Transverse scan shows hypoechoic band of transmediastinal artery (arrow). (I) Color Doppler scan shows transmediastinal artery.

of a head, a body, and a tail. The pyramid-shaped epididymal head, or globus major, is located at the superoposterior aspect of the testis, measuring 5 to 12 mm in diameter (Fig. 22.2D). It is formed by the efferent ductules from the rete testis, which join together to form a single convoluted duct, the ductus epididymis. This duct forms the body and the majority of the tail of the epididymis, measures approximately 6 m in length and follows a convoluted course from the head to the tail of the epididymis. The body (corpus) of the epididymis lies adjacent to the posterolateral margin of the testis. The tail (globus minor) is loosely attached to the lower pole of the testis by areolar tissue. The ductus epididymis forms an acute angle at the inferior aspect of the globus minor and courses cephalad as the vas deferens to the spermatic cord. Sonographically, the epididymal head is normally isoechogenic or slightly more echogenic than the testis,

and its echotexture may be coarser. The body tends to be isoechoic or slightly less echogenic than the globus major and testis. The normal body measures less than 4 mm in diameter, averaging 1 to 2 mm. The appendix testis, a remnant of the upper end of the paramesonephric (Müllerian) duct, is a small ovoid structure usually located on the superior pole of the testis or in the groove between the testis and the head of the epididymis. The appendix testis is identified sonographically in 80% of testes and is more readily visible when a hydrocele is present7 (Fig. 22.2E). The appendix testis may appear stalklike and pedunculated, cystic, or even calcified.8 The appendices of the epididymis are blindending tubules (vasa aberrantia) derived from the mesonephric (Wolffian) duct; they form small stalks, which may be duplicated, and project from the epididymis9 (Fig. 22.2F). In rare cases,

CHAPTER 22  The Scrotum

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FIG. 22.3  Spectral Doppler of Normal Intratesticular and Extratesticular Arterial Flow.  (A) Intratesticular artery has a low-impedance waveform with large amount of end diastolic flow. (B) Extratesticular scrotal arterial supply (cremasteric and deferential arteries) has high-impedance waveform with reversed flow in diastole.

other appendages, such as the paradidymis (organ of Giraldés) and the superior and inferior vas aberrans of Haller, may be seen.10 The appendages of the epididymis are most often identified sonographically as separate structures when a hydrocele is present. Knowledge of the arterial supply of the testis is important for interpretation of color flow Doppler sonography of the testis. Testicular blood flow is supplied primarily by the testicular, deferential, and cremasteric (external spermatic) arteries. The testicular arteries arise from the anterior aspect of the aorta immediately below the origin of the renal arteries. They course through the inguinal canal with the spermatic cord to the posterosuperior aspect of the testis. On reaching the testis, the testicular artery divides into branches that pierce the tunica albuginea where the capsular arteries form and arborize over the surface of the testis in a layer known as the tunica vasculosa, deep to the tunica albuginea. Centripetal branches arise from these capsular arteries; these branches course along the septa to converge on the mediastinum. From the mediastinum, these branches form recurrent rami that course into the testicular parenchyma, where they branch into arterioles and capillaries11 (Fig. 22.2G). In about 50% of normal testes a transmediastinal artery supplies the testis, entering through the mediastinum and coursing toward the periphery of the gland to supply the capsular arteries, and is accompanied by a large vein, frequently seen as a hypoechoic band in the midtestis11,12 (Fig. 22.2H and I). The transmediastinal artery may be associated with acoustic shadowing obscuring the distal aspect of the testis and giving

rise to the “two-tone” testis appearance.13 The deferential artery originates from the superior vesical artery and courses to the tail of the epididymis, where it divides and forms a capillary network. The cremasteric artery arises from the inferior epigastric artery. It courses with the remainder of the structures of the spermatic cord through the inguinal ring, continuing to the surface of the tunica vaginalis, where it anastomoses with capillaries of the testicular and deferential arteries. The velocity waveforms of the normal capsular and intratesticular arteries show high levels of antegrade diastolic flow throughout the cardiac cycle, reflecting the low vascular resistance of the testis (Fig. 22.3A). Supratesticular arterial waveforms vary in appearance. Two main types of waveforms exist: a low-resistance waveform similar to that seen in the capsular and intratesticular arteries, reflecting the testicular artery; and a high-resistance waveform with sharp, narrow systolic peaks and little or no diastolic flow14 (Fig. 22.3B). This high-resistance waveform is believed to reflect the high vascular resistance of the extratesticular tissues. The deferential and cremasteric arteries within the spermatic cord primarily supply the epididymis and extratesticular tissues, but they also supply the testis through anastomoses with the testicular artery. The spermatic cord consists of the vas deferens; the testicular, cremasteric, and deferential arteries; a pampiniform plexus of veins; the lymphatics; and the nerves of the testis. It courses superiorly toward the superficial and deep (also called “internal”) inguinal rings. Sonographically, the normal spermatic cord lies just beneath the skin and may be difficult to distinguish from

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the adjacent soft tissues of the inguinal canal.15 Distally, it may be visualized within the scrotum when a hydrocele is present or with the use of color flow Doppler sonography.

Pathologic Classification of Testicular Tumors32 GERM CELL TUMORS Seminoma Classic Spermatocytic Nonseminomatous germ cell tumors Mixed malignant germ cell Embryonal cell carcinoma Yolk sac tumor (endodermal sinus tumor) Teratoma Choriocarcinoma Placental site trophoblastic tumor Trophoblastic tumor, unspecified Regressed tumor

INTRATESTICULAR SCROTAL MASSES When a scrotal mass is palpated, the concern is for the presence of a testicular neoplasm. With sonographic examination, intrascrotal masses can be detected with a sensitivity of nearly 100%.16 Delineation between intratesticular and extratesticular processes is 98% to 100% accurate.16-19 In general, intratesticular masses should be considered malignant.19,20 If the mass is extratesticular and cystic, then this process is almost certainly benign, with the general accepted prevalence of malignancy of extratesticular lesions being 3% to 6%.19,21-24 Testicular neoplasms account for 1% to 2% of all malignant neoplasms in men and represent the most common nonhematologic malignancy in men in the 15- to 49-year-old age group.25-27 Most (65%-94%) patients with testicular neoplasms present with painless unilateral testicular masses or diffuse testicular enlargement, and 4% to 14% present with symptoms of metastatic disease.3,28,29 Approximately 10% to 15% of patients will present with pain and initially may be misdiagnosed as having epididymo-orchitis.30 Testicular tumors are subdivided into two major categories: germ cell and stromal tumors, with germ cell tumors accounting for 90% to 95% of all testicular tumors. Germ cell tumors arise from primitive germ cells and are further divided into seminoma and nonseminomatous germ cell tumors (NSGCTs). These tumors are uniformly malignant. Non–germ cell (sex cord– stromal) primary tumors of the testis derive from the sex cords (Sertoli cells) and the stroma (Leydig cells) and are malignant in approximately 10% of cases.3,29 Nonprimary tumors include lymphoma, leukemia, and metastases and can present as intratesticular masses. Color Doppler imaging has limited ability to distinguish between malignant and benign solid intratesticular masses.31

Malignant Tumors Germ Cell Tumors Intratubular germ cell neoplasia is believed to be the precursor of most germ cell tumors and is the equivalent of carcinoma in situ. It is thought that these abnormal cells develop along a unipotential line and form seminoma, or develop along a totipotential line and form nonseminomatous tumors.33,34 Seminomas are radiosensitive tumors, whereas NSGCTs respond better to surgery and chemotherapy.27 Approximately 95% of primary testicular neoplasms larger than 1.6 cm in diameter show increased vascularity on color flow Doppler examination. However, color Doppler findings do not appear to be important in the evaluation of adult testicular tumors.35 Color flow may help to identify tumors that are relatively isoechoic with testicular parenchyma,36 but focal or diffuse inflammatory lesions cannot be distinguished from neoplasms on the basis of color flow Doppler or spectral Doppler findings. Nonpalpable testicular tumors have also been detected with

STROMAL TUMORS Leydig cell (interstitial) Sertoli cell Granulosa cell Mixed undifferentiated sex cord MIXED GERM CELL–STROMAL TUMORS Gonadoblastoma Germ cell–stromal–sex cord, unclassified METASTATIC NEOPLASMS Lymphoma Leukemia Myeloma Carcinoma OTHERa Adrenal rests Epidermoid cyst Malacoplakia Carcinoid tumor Mesenchymal tumor Granulomatous disease a

Rare tumors and nonneoplastic tumorous conditions. Modified from Moch H, Cubilla AL, Humphrey PA, et al. The 2016 WHO classification of tumours of the urinary system and male genital organs-Part A: renal, penile, and testicular tumors. Eur Urol. 2016:70(10):93-105.32

sonography in patients presenting for scrotal discomfort or infertility.37-40 Incidentally discovered nonpalpable lesions are often benign, but 20% to 30% are malignant.38,39,41 Tumor markers have a role in diagnosis, staging, prognosis, and follow-up of a number of germ cell tumors, with three markers having clinical use: α-fetoprotein, human chorionic gonadotropin, and, less so, lactate dehydrogenase. α-Fetoprotein is produced by the fetal liver, gastrointestinal tract, and yolk sac and is elevated in yolk sac tumors or mixed germ cell tumors containing yolk sac elements. Human chorionic gonadotropin is a glycoprotein produced by syncytiotrophoblasts of the developing placenta. It is elevated in tumors containing syncytiotrophoblasts, including choriocarcinoma and seminoma. Lactate dehydrogenase, although not specific, correlates with bulk of disease and is used in staging.20

CHAPTER 22  The Scrotum

FIG. 22.4  Mixed Tumor.  Transverse scan of coexistent solid masses— a mixed germ cell tumor (M) and a seminoma (S).

Seminoma.  Seminoma is the most common pure, or single cell–type, germ cell tumor in adults, accounting for 35% to 50% of all germ cell neoplasms.20,30 It is also a common component of mixed germ cell tumors, occurring in 30% of these tumors. Seminomas tend to occur in slightly older patients than do other testicular neoplasms, with a peak incidence in the fourth and fifth decades, and they rarely occur before puberty.3,42,43 They are typically confined within the tunica albuginea at presentation, with approximately 25% of patients having metastases at diagnosis. As a result of the radiosensitivity and chemosensitivity of the primary tumor and its metastases, seminomas have the most favorable prognosis of the malignant testicular tumors. A second primary synchronous or metachronous germ cell tumor occurs in 1% to 2.5% of patients with seminomas (Fig. 22.4). Seminoma is the most common tumor type in cryptorchid testes. Between 8% and 30% of patients with seminoma have a history of undescended testes.29,43 The risk of a seminoma developing is substantially increased in an undescended testis, even after orchiopexy. Patients with a normally located but atrophic testis have an increased risk of seminoma (Video 22.1). There is also an increased risk of malignancy developing in the contralateral, normally located testis. Therefore sonography is often used to screen for an occult tumor in both testes after orchiopexy. Seminomas range from a small, well-circumscribed lesion to large masses replacing the testis. Macroscopically, cellular morphology resembles that of primitive germ cells, which are relatively uniform.25 The sonographic features of pure seminoma parallel this homogeneous macroscopic appearance. Pure seminomas usually have predominantly uniform, low-level echoes without calcification, and they appear hypoechoic compared with normally echogenic testicular parenchyma (Fig. 22.5).44 Larger tumors may have a more heterogeneous appearance. In rare cases, seminomas become necrotic and appear partly cystic on sonography (Fig. 22.5I).

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Nonseminomatous Germ Cell Tumors.  NSGCTs include embryonal carcinomas, teratomas, yolk sac (endodermal sinus) tumors, choriocarcinomas, and mixed germ cell tumors. These tumors occur more often in younger patients than do seminomas, with a peak incidence during the latter part of the second decade and the third decade. They are uncommon before puberty and after age 50. Approximately 70% of NSGCTs produce hormonal markers.45 Up to 60% of germ cell tumors are mixed germ cell tumors, composed of at least two different cell types.20,46 Pure NSGCTs are rare and occur more often in the pediatric population.20 The sonographic appearance of NSGCTs reflects the histologic features and relative proportions of each component, although as a group these tumors are more heterogeneous than seminoma, demonstrating irregular margins, echogenic foci, and solid and cystic components (Fig. 22.6). These malignancies are more aggressive than seminomas, frequently invading the tunica albuginea and resulting in distortion of the testicular contour (see Fig. 22.6). Approximately 60% of NSGCTs have metastatic involvement at presentation.46 Mixed germ cell tumors are the most common germ cell tumors, constituting up to 60% of all germ cell tumors. They contain nonseminomatous germ cell elements in various combinations. Seminomatous elements may also be present but do not influence prognosis or treatment.47 Embryonal carcinoma is the most common component, although any combination of cell types may occur. Imaging features are variable, reflecting the diversity of this group of tumors. Nonseminomatous tumors are not as radiosensitive as seminomas. Embryonal carcinoma is composed of primitive anaplastic cells that resemble early embryonic cells. It is present in 87% of mixed germ cell tumors, but in its pure form it is rare, accounting for only 2% to 3% of testicular germ cell neoplasms (Fig. 22.6C).48 As with other NSGCTs, embryonal cell tumors occur in younger patients than seminomas do, with a peak incidence during the latter part of the second and third decades. The sonographic features of pure embryonal cell carcinoma are nonspecific, especially in children, in whom the only finding may be testicular enlargement without a defined mass.36,49 Totipotent germ cells that differentiate toward extraembryonic fetal membranes give rise to yolk sac tumors, or endodermal sinus tumors. Yolk sac tumors are the most common germ cell tumor in infants younger than 2 years, accounting for 80% of childhood testicular neoplasms.49 Yolk sac tumor is rare in its pure form in adults, although it is present in 44% of adult cases of mixed germ cell tumor (Fig. 22.6D).20 Yolk sac tumor is associated with elevated levels of α-fetoprotein in greater than 90% of infants. Teratomas constitute 5% to 10% of primary testicular neoplasms. They are defined according to the World Health Organization (WHO) classification on the basis of the presence of derivatives of the different germinal layers (endoderm, mesoderm, and ectoderm). Histologically, teratomas can be divided into mature and immature. The peak incidence is in infancy and early childhood, with another peak in the third decade of life. In infants and young children, teratomas are the second most common testicular tumor after yolk sac tumor and are considered benign, even when they are histologically immature.43,50,51 Postpubertal testicular teratomas are malignant and

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FIG. 22.5  Seminoma: Spectrum of Appearances.  Longitudinal scans. (A) and (B) Subtle hypoechoic seminoma (arrows) with increased flow. (C) Typical homogeneous hypoechoic seminoma. (D) Two small foci of seminoma. (E) Slightly heterogeneous seminoma. (F) Seminoma associated with microlithiasis and coarser calcifications. (G) Seminoma occupying most of testis. Typical homogeneous hypoechoic sonographic appearance. (H) Gross specimen of seminoma in G. (I) Necrotic seminoma replacing testicle. See also Video 22.1.

have a higher metastatic rate, approximately 20%, than their ovarian counterpart.52 Teratomas in their pure form are rare in adults, although teratomatous elements occur in approximately half of all adult cases of mixed germ cell tumor (Fig. 22.6B). Both mature and immature teratomas are generally associated with normal tumor markers, although elevated levels of α-fetoprotein or human chorionic gonadotropin may be found.47 Sonographically, the teratoma is usually a well-defined, markedly heterogeneous mass containing cystic and solid areas of various sizes and appears similar to other NSGCTs. Dense echogenic foci causing acoustic shadowing are common, resulting from focal calcification, cartilage, immature bone, fibrosis, and noncalcific scarring (Fig. 22.6E).44 Choriocarcinoma accounts for less than 1% of malignant primary testicular tumors in its pure form but occurs in 8% of mixed germ cell tumors.20,43,48,50 The peak incidence is in the second and third decades. These tumors are highly malignant and metastasize early by hematogenous and lymphatic routes. The primary tumor and metastases are often hemorrhagic, and patients may have symptoms resulting from hemorrhagic

metastases, including hemoptysis, hematemesis, and central nervous system–related symptoms. Focal necrosis of the primary tumor secondary to hemorrhage is an almost invariable feature, and calcification may be present, giving a sonographic appearance similar to the other NSGCTs (Fig. 22.6F). The levels of human chorionic gonadotropin are elevated and cause gynecomastia in 10% of cases.20,53 Choriocarcinoma has the worst prognosis of any of the germ cell tumors.50 Regressed Germ Cell Tumor.  Sonography is an important diagnostic tool for patients who present with widespread metastatic testicular carcinoma (Fig. 22.7) even though the primary tumor has involuted (Fig. 22.8); ultrasound is an important component in the search for a primary testicular neoplasm. Mediastinal and central nervous system extragonadal tumors can often present as primary lesions, although retroperitoneal germ cell tumors are more likely to have a testicular origin.54,55 The primary testicular tumor may regress, despite widespread advancing metastatic disease, resulting in an echogenic fibrous and possibly calcific scar. Regression may be caused by the high metabolic rate of the tumor and vascular compromise from the

CHAPTER 22  The Scrotum

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FIG. 22.6  Nonseminomatous Germ Cell Tumor: Spectrum of Appearances.  (A) and (B) Mixed germ cell tumor. (A) Longitudinal scan shows a large tumor with cystic changes occupying most of the testis and invading the tunica (arrow). (B) Transverse scan shows a heterogeneous, mixed germ cell tumor that has 85% teratoma elements. (C) Embryonal carcinoma. Longitudinal scan shows relatively homogeneous tumor (arrow). (D) Yolk sac, or Endodermal sinus tumor. Longitudinal scan shows a mildly heterogenous tumor extending to the mediastinum (arrow). (E) Teratoma. Longitudinal scans shows a large heterogeneous mass with cystic foci and scattered calcifications. (F) Choriocarcinoma. Longitudinal scan shows a relatively homogeneous tumor (arrows).

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FIG. 22.7  Occult Testicular Seminoma With Retroperitoneal Metastases.  (A) Contrast-enhanced CT scan shows extensive retroperitoneal adenopathy from seminoma. (B) Longitudinal sonographic scan shows occult homogeneous hypoechoic seminoma. The physical examination of the testis was negative.

tumor outgrowing its blood supply. Tumors are typically clinically occult with the affected testis normal or small on palpation. Histologic analysis may reveal no residual tumor, although intratubular malignant germ cells may be present.25,28,54 These lesions, also known as “Azzopardi tumors,” have a variable sonographic appearance; they can be hypoechoic or hyperechoic or seen as focal calcifications. Although sonographic appearance is not specific for a “burned-out” or regressed tumor, findings

are suggestive in the context of histologically proven testicular metastases.56

Non–Germ Cell Tumors Sex Cord–Stromal Tumors. Sex cord–stromal tumors account for 3% to 6% of all testicular neoplasms. The prevalence is greater in the pediatric population where non–germ cell tumors account for 10% to 30% of all testicular neoplasms. The term

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FIG. 22.8  Regressed, or “Burned-Out,” Germ Cell Tumor.  (A) Longitudinal scan shows a partly calcified nonviable germ cell tumor in a patient with retroperitoneal metastases. Notice the hypoechoic mass around the focus of calcification. (B) Contrast-enhanced CT scan in the same patient shows heterogeneous left retroperitoneal adenopathy (arrow) from regressed primary testicular teratoma.

sex cord–stromal tumor refers to a neoplasm containing Leydig, Sertoli, thecal, granulosa, or lutein cells and fibroblasts in various degrees of differentiation. These tumors may contain single or multiple cell types because of the totipotentiality of the gonadal stroma.29 The most common type of sex cord–stromal tumor is a Leydig cell tumor, accounting for 1% to 3% of all testicular neoplasms; these can occur in any age group, although predominantly in patients aged 20 to 50 years.42,43,53 Patients most often present with painless testicular enlargement or a palpable mass. Approximately 30% of patients present with an endocrinopathy secondary to secretions of androgens or estrogens by the tumor, which may manifest as precocious virilization, impotence, or loss of libido. The tumor is bilateral in 3% of cases. From 10% to 15% of the tumors are malignant, having invaded the tunica at diagnosis. These gonadal tumors are usually small, solid, homogeneous hypoechoic masses on sonography and may show mainly peripheral flow on color Doppler imaging (Fig. 22.9A and B).57 Foci of hemorrhage and necrosis are present in 25% of tumors,42,53 and thus cystic spaces due to hemorrhage and/or necrosis are occasionally seen in larger lesions. Sertoli cell tumors are rare and account for less than 1% of all testicular tumors; they occur with equal frequency in all age groups.58 They can be of one of three histologic types: Sertoli cell tumor not otherwise specified, sclerosing Sertoli cell tumor, or large cell calcifying Sertoli cell tumor. The most common presentation is with a painless intratesticular mass. These tumors are less likely than Leydig cell tumors to be hormonally active, although gynecomastia may occur. Sertoli cell tumors may occur in undescended testes, in patients with testicular feminization, Klinefelter syndrome, and Peutz-Jeghers syndrome.59 Sertoli cell tumors are typically well-circumscribed, unilateral, rounded to lobulated masses. Occasionally, hemorrhage or necrosis may occur, giving a more heterogeneous appearance on sonography. The large-cell calcifying Sertoli cell tumor is a subtype with distinctive clinical, histologic, and sonographic features.59 These tumors are often bilateral and multifocal and may be almost completely calcified. Carney complex, a very rare autosomal

dominant multiple endocrine neoplasia syndrome, is often associated with Sertoli cell tumors (Fig. 22.9C). Additional, less common tumors in this category include granulosa cell tumors, fibroma-thecomas, and mixed sex cord–stromal tumors (Fig. 22.9D). Gonadal stromal tumors in conjunction with germ cell tumors are called gonadoblastomas. The majority of gonadoblastomas occur in the setting of gonadal dysgenesis and intersex syndromes.43,60

Testicular Metastases Lymphoma and Leukemia Lymphoma accounts for 5% of all testicular tumors and is the most common testicular tumor in men older than 60 years, where it can account for up to 50% of intratesticular masses. However, testicular involvement occurs in only 1% to 3% of patients with lymphoma.29,61 The peak age at diagnosis of lymphoma is 60 to 70 years; 80% of the patients are older than 50 years at diagnosis. Malignant lymphoma is the most common bilateral testicular tumor, occurring bilaterally either in a synchronous or, more often, in a metachronous manner in up to 38% of cases.60 One-half of bilateral testicular neoplasms are lymphoma.29,42 Most lymphomas of the testis are B-cell lymphomas, with diffuse large cell lymphoma being the most common. Hodgkin lymphoma of the testis is extremely rare. Testicular Metastases LYMPHOMA Mostly non-Hodgkin lymphoma LEUKEMIA Second most common Acute leukemia: 40%-65% “Sanctuary” site NONLYMPHOMA METASTASES Lung and prostate most common Kidney, stomach, colon, pancreas, melanoma

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FIG. 22.9  Stromal Tumors: Spectrum of Appearances.  (A) and (B) Leydig cell tumor. (A) Transverse scan shows several small, hypoechoic solid masses in the midtestis consistent with Leydig cell hyperplasia. (B) Longitudinal scan shows a hypoechoic solid mass in the midtestis. The patient had bilateral Leydig cell tumors. (C) Longitudinal scan of multifocal large-cell calcifying Sertoli cell tumor. (D) Stromal tumor. Transverse scan demonstrates a large, heterogeneous tumor (which was a stromal tumor, not otherwise specified) replacing the testis. (C courtesy of Theodora Potretzke, MD, Mayo Clinic.)

Testicular lymphoma most frequently occurs in association with disseminated disease, as the initial manifestation of occult nodal disease, or as a site of recurrent disease.29 True primary lymphoma of the testis has not been conclusively documented.47 Although most patients with lymphoma of the testis present with a painless intratesticular mass or diffuse testicular enlargement, approximately 25% of the patients have constitutional symptoms, such as fever, weakness, anorexia, or weight loss. Lymphoma of the testis is often large at diagnosis. The tunica vaginalis is usually intact, but unlike germ cell tumors, extension into the epididymis and spermatic cord is common, occurring in up to 50% of cases.62 The scrotal skin is rarely involved. Grossly, the tumor is not encapsulated but compresses the parenchyma to the periphery. The sonographic appearance of lymphoma is nonspecific, although generally appears as homogeneous, hypoechoic lesions which may diffusely infiltrate the testis29; however, focal hypoechoic lesions can occur (Fig. 22.10). Hemorrhage and necrosis are rare. Color flow Doppler imaging shows increased vascularity in testicular lymphoma, regardless of lesion size, and the appearance may resemble diffuse inflammation63 (Fig. 22.10C). Unlike inflammation, lymphoma is usually painless, and the testes are not tender to palpation.

Leukemia is the second most common metastatic testicular neoplasm. Primary testicular leukemia is rare, but leukemic infiltration of the testis during bone marrow remission is common in children.29,64 The testis appears to act as a “sanctuary” site for leukemic cells during chemotherapy because of the blood-testis barrier, which inhibits concentration of chemotherapeutic agents.64 The highest frequency of testicular involvement is found at autopsy in patients with acute leukemia (40%-65%). Approximately 20% to 35% of patients with chronic leukemia have testicular involvement.65 Most cases of testicular involvement occur within 1 year of the discontinuation of long-term remission maintenance chemotherapy. The sonographic appearance of leukemia is nonspecific and similar to lymphoma. Patients most frequently present with diffuse infiltration, which produces diffusely enlarged, hypoechoic testes (Fig. 22.10E).63 The differential diagnosis includes inflammation.

Extramedullary Myeloma Involvement of the testis is usually a manifestation of diffuse myeloma, although rarely the testis may be the site of primary focal myeloma (plasmacytoma).66 The testis may have single or multiple nodules that appear hypoechoic and homogeneous

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FIG. 22.10  Lymphoma, Leukemia, and Metastases. (A)-(D) Lymphoma. (A) Longitudinal scan shows two subtle hypoechoic foci of lymphoma. In another patient, sagittal gray-scale (B) and power Doppler (C) images show diffuse, homogeneous hypoechoic hypervascular mass. (D) Heterogeneous involvement of the testes in patient with lymphoma. (E) Leukemia. Longitudinal scan shows diffuse hypoechoic involvement. (F) Melanoma metastasis. Longitudinal scan shows a hypoechoic lobulated mass in the upper pole of the testis and epididymis.

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located within the parenchyma. Cystic testicular lesions are not always benign; testicular tumors (especially NSGCTs) can undergo cystic degeneration from hemorrhage or necrosis. The distinction between a benign cyst and a cystic neoplasm is of utmost clinical importance (Fig. 22.12). Simple intratesticular cysts can be managed conservatively without the need for surgical intervention.73 Of the 34 cystic testicular masses discovered with sonography by Hamm et al.,72 16 were neoplastic, and all of these had sonographic features of complicated cysts. NCGCTs, especially those with teratoma elements, are the most common tumors to contain both cystic and solid components. FIG. 22.11  Multiple Testicular Hamartomas in Cowden Disease. Dual transverse image shows multiple bilateral small echogenic hamartomas. The patient had Cowden disease, an inherited autosomal dominant disorder, which causes multiple hamartomas in the gastrointestinal tract.

on sonographic examination with marked hypervascularity.67,68 Bilateral involvement occurs in approximately 20% of cases.47

Metastatic Disease Nonlymphomatous metastases to the testes are uncommon, representing 0.02% to 5% of all testicular neoplasms.69 The most frequent primary sites are the lung and prostate gland.42 Other frequent primary sites for metastatic neoplasms include melanoma, kidney, colon, stomach, and pancreas.70 Most metastases are clinically silent, being discovered incidentally at autopsy. Testicular metastases are most common in patients during the sixth and seventh decades.3 They are usually multiple and are bilateral in 15% of cases.42 Because primary germ cell tumors may also be multicentric and bilateral, these features are not helpful in distinguishing primary from metastatic testicular neoplasms. Widespread systemic metastases are usually present in patients with testicular metastases. Possible routes of metastases to the testis include retrograde venous, hematogenous, retrograde lymphatic, and direct tumor invasion. Metastases from sites remote from the testis, such as the lung and skin, most likely spread hematogenously. Retrograde venous extension through the testicular vein occurs in renal cell carcinoma and may also occur in urinary bladder and prostate tumors.71 Neoplasms with metastases to the periaortic lymph nodes may involve the testis through retrograde lymphatic extension. Sonographic features of nonlymphomatous testicular metastases vary. The appearance is often hypoechoic but may be echogenic or complex3 (Fig. 22.10F). Other rare tumors of the testis include hamartoma (Fig. 22.11), dermoid tumor, hemangioma, intratesticular adenomatoid tumor, carcinoid tumor, carcinoma of the mediastinum testis, neuroectodermal tumor, leiomyoma, Brenner tumor, fibroma, fibrosarcoma, osteosarcoma, chondrosarcoma, and undifferentiated sarcoma, among others.

Benign Intratesticular Lesions Cysts Intratesticular cystic lesions are discovered incidentally on sonography in 8% to 10% of men.72 Benign testicular cysts may be associated with the tunica albuginea, tunica vaginalis, or

Testicular Cystic Lesions BENIGN Tunica albuginea cysts Tunica vaginalis cysts Intratesticular cysts Tubular ectasia of rete testis Cystic dysplasia Epidermoid cysts Abscess MALIGNANT Nonseminomatous germ cell tumor Necrosis or hemorrhage in tumor Tubular obstruction by tumor

Cysts of the tunica albuginea are located within the tunica, which surrounds the testis. They vary in size from 2 to 30 mm and are well defined. They are usually solitary and unilocular but may be multiple or multilocular72,74 (Fig. 22.12A). The mean age at presentation is 40 years, but cysts also occur in the fifth and sixth decades.75 The cysts may be asymptomatic, but patients frequently present with cysts that are clinically palpable, firm scrotal nodules. Histologically, they are simple cysts lined with cuboid or low columnar cells and filled with serous fluid.76 Careful scanning in multiple planes allows delineation of the cyst as arising from the tunica albuginea and clarifies its benign nature. Complex tunica albuginea cysts may simulate a testicular neoplasm.77 Cysts of the tunica vaginalis are rare and arise from the visceral or parietal layer of the tunica vaginalis. They may be single or multiple. Sonographically, they usually appear anechoic but may have septations or may contain echoes caused by hemorrhage.78 Intratesticular cysts are simple cysts filled with clear serous fluid; they vary in size from 2 to 18 mm.79 Sonographically, they are well-defined, anechoic cysts with thin, smooth walls and posterior acoustic enhancement. Hamm et al.72 reported that in all 13 of their cases, the cysts were located near the mediastinum testis, supporting the theory that they originate from the rete testis, possibly secondary to posttraumatic or postinflammatory stricture formation (Fig. 22.12B).

Tubular Ectasia of Rete Testis Tubular ectasia of the rete testis is a benign, normal variant that may be mistaken for a testicular neoplasm.80-83 Dilatation of the

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FIG. 22.12  Intratesticular Cystic Lesions.  (A) Tunica albuginea cyst. Longitudinal scan shows a cyst arising from the tunica albuginea. These cysts are usually palpable. (B) Intratesticular cyst. Transverse scan shows bilateral benign intratesticular cysts. (C) Cystic dilatation in rete testis. Transverse scan shows dilated tubules of the rete testis in both testes. (D)-(F) Epidermoid cyst (benign). See also Video 12.2. (D) Typical whorled appearance; (E) heterogeneous hypoechoic lesion (arrows); (F) typical peripheral calcifications. (G) Transverse scan shows an intratesticular cystic lesion with minimal mural nodularity (arrow). (H) Transverse scan at 6-month interval follow-up shows interval development of an isoechoic, solid mass (arrow) partially filling the cystic lesion, surgically proven to represent teratoma. (G and H courtesy of Shane Macauley, MD.)

rete testis is thought to result from obstruction in the efferent tubules or epididymis, with epididymal obstruction caused by inflammation, trauma, or surgery. Sonographic appearance is of multiple fluid-filled tubular structures in or adjacent to the mediastinum testis with no associated soft tissue abnormality and no flow on color flow Doppler imaging (Fig. 22.12C). Rete testis dilatation is often bilateral, asymmetric, and is frequently associated with a spermatocele. The characteristic sonographic appearance and location should allow recognition as a benign condition, thus preventing an orchiectomy. Characteristic findings of the dilated rete testis on magnetic resonance imaging (MRI) include intratesticular signal intensity similar to that of fluid in the region of the mediastinum testis.80 This appearance is in contrast to the MRI appearance of testicular tumors, which typically have low signal intensity on T2-weighted imaging.

Cystic Dysplasia Cystic dysplasia is a rare congenital malformation, usually occurring in infants and young children, although one case was reported in a 30-year-old man.84,85 This lesion is thought to result from an embryologic defect that prevents connection of the tubules of the rete testis and the efferent ductules. Pathologically, the lesion consists of multiple, interconnecting cysts of various sizes and shapes, separated by fibrous septa. This lesion originates in the rete testis and extends into the adjacent parenchyma, resulting in pressure atrophy of the adjacent testicular parenchyma. The cysts are lined by a single layer of flat or cuboidal epithelium. Sonographically, the appearance is similar to acquired cystic dilatation of the rete testis. Renal agenesis or dysplasia frequently coexists with testicular cystic dysplasia.85

CHAPTER 22  The Scrotum Epidermoid Cysts An epidermoid cyst is an uncommon, benign, generally well-circumscribed tumor of germ cell origin, representing approximately 1% of all testicular tumors. These tumors occur at any age but are most common during the second to fourth decades.42 Usually, patients present with a painless testicular nodule; one-third of the tumors are discovered incidentally on physical examination. Diffuse, painless testicular enlargement occurs in 10% of patients. Pathologically, epidermoid cysts are composed of keratinizing, stratified, squamous epithelium with a well-defined, fibrotic wall. Although the histogenesis of epidermoid cysts is controversial, the current prevailing theory is that these entities represent teratomas that have undergone monodermal differentiation. However, a complete absence of mesodermal or ectodermal components and absence of intraepithelial neoplasia, a histologic precursor of germ cell tumors, brings this theory into question. Additionally, unlike germ cell tumors, epidermoid cysts have an invariably benign course without recurrence or metastatic disease following resection.86 Squamous metaplasia of seminiferous epithelium or rete testis is an alternative diagnosis.87 These benign lesions can be differentiated from premalignant teratomas only through histologic examination. Sonographically, epidermoid cysts are generally well-defined, round to ovoid, avascular masses and may be multiple or bilateral.86 A characteristic whorled or laminated appearance, like the layers of an onion skin, corresponds to the alternating layers of compacted keratin and desquamated squamous cells seen histologically88-90 (Fig. 22.12D, Video 22.2). This appearance, however, may not be pathognomonic because it is rarely seen with teratoma.91 Another typical appearance of an epidermoid cyst is a well-defined hypoechoic mass with an echogenic capsule

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that may be calcified (Fig. 22.12F). There may be central calcification, giving a “bull’s eye” or target appearance.86 Epidermoid cysts may also have the nonspecific appearance of a hypoechoic mass with or without calcifications and may resemble germ cell tumors (Fig. 22.12E). Avascularity is a clue to the diagnosis.89 Although the sonographic appearance is characteristic, it is not pathognomonic, and histologic confirmation should be obtained by a conservative testis-sparing approach with local excision (enucleation).92 MRI has been used to support the sonographic diagnosis of epidermoid cysts as they have a target appearance with low signal capsule. The layers of keratinizing material are rich in water and lipid and can appear as areas of high signal intensity on both T1- and T2-weighted imaging.93,94

Abscess Testicular abscesses are usually a complication of epididymoorchitis, although they may also result from an undiagnosed testicular torsion, testicular infarct, trauma, a gangrenous or infected tumor, or a primary pyogenic orchitis. Infectious causes of abscess formation are mumps, smallpox, scarlet fever, influenza, typhoid, sinusitis, osteomyelitis, and appendicitis.95 A testicular abscess may cross the mesothelial lining of the tunica vaginalis, resulting in formation of a pyocele or a fistula to the scrotal skin. Most often, sonography demonstrates an irregularly marginated, hypoechoic or mixed echogenic intratesticular mass (Fig. 22.13). Testicular abscesses have no diagnostic sonographic features but can often be distinguished from tumors on the basis of clinical symptoms and short-term interval change. In patients with acquired immunodeficiency syndrome (AIDS), distinguishing an abscess from a neoplastic process may be difficult on sonographic examination. Clinical findings may

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FIG. 22.13  Testicular Abscesses.  (A) Transverse gray-scale image shows typical hypoechoic intratesticular abscesses, which may be indistinguishable from a tumor. However, heterogeneity of the parenchyma, skin thickening, and developing pyocele suggest that these masses represent abscesses. (B) Transverse color Doppler image shows echogenic and hypoechoic areas in the intratesticular abscesses with increased vascularity around the abscesses.

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be helpful; however, orchiectomy is frequently necessary to obtain a histologic diagnosis.96,97

Segmental Infarction Segmental testicular infarction may occur after torsion, trauma, surgery, bacterial endocarditis, vasculitis, leukemia, or hypercoagulable states.98 Spontaneous infarction of the testis is rare. The sonographic appearance depends on the age of the infarction. Initially, a typical segmental infarct is seen as a focal, wedgeshaped or round hypoechoic mass, with approximately 80% occurring in the upper pole, likely secondary to vascular supply between the upper and lower poles.99 The focal hypoechoic mass may not be distinguishable from a neoplasm on the basis of its gray-scale sonographic appearance.100,101 These lesions should have reduced or absent blood flow, depending on the age of the infarction.99 If a well-circumscribed, nonpalpable, relatively peripheral, hypoechoic mass shows a complete lack of vascularity on power Doppler imaging or after the administration of sonographic contrast agent, it may be possible to distinguish such

benign infarctions from neoplasm102,103 (Fig. 22.14). With time, the hypoechoic mass or the entire testis often decreases in size and develops areas of increased echogenicity because of fibrosis or dystrophic calcification.104 The early sonographic appearance may be difficult to distinguish from a testicular neoplasm, but infarcts decrease substantially in size, whereas tumors characteristically enlarge with time.3,101,105

Adrenal Rests Adrenal rests are a rare cause of intertesticular masses and can be seen in the setting of congenital adrenal hyperplasia (CAH), and rarely in the setting of Cushing syndrome. CAH is an autosomal recessive disease involving an adrenocortical enzyme defect. This disease typically becomes clinically obvious early in life or in early adulthood. Patients often present with a testicular mass or enlargement, precocious puberty, and with or without salt-depletion syndrome. Adrenal rests arise from aberrant adrenocortical cells that migrate with gonadal tissues in the fetus. They can form tumorlike masses in response to elevated levels

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FIG. 22.14  Testicular Infarcts: Spectrum of Appearances.  (A) and (B) Acute infarct. (A) Longitudinal power Doppler scan shows an avascular area at the upper pole from partial torsion. (B) Longitudinal color Doppler scan shows an avascular area in the midtestis caused by vasculitis. (C) and (D) Chronic infarct. (C) Longitudinal scan shows a peripheral wedge-shaped hypoechoic area caused by prior mumps orchitis. (D) Longitudinal power Doppler scan shows lack of vascularity in the lower pole.

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FIG. 22.15  Adrenal Rests in Patient With Congenital Adrenal Hyperplasia.  (A) Longitudinal scan shows multifocal hypoechoic masses (arrows) within the testis that cannot be distinguished from tumor. (B) CT in same patient shows bilateral adrenal hyperplasia (arrows).

of circulating adrenocorticotropic hormone in CAH and Cushing syndrome. These lesions are typically multifocal, bilateral, and eccentrically located. Sonographically, they are variable in appearance, typically presenting as hypoechoic masses, although they may be heterogeneous, hyperechoic masses with posterior acoustic shadowing (Fig. 22.15). Adrenal rests can demonstrate spokelike vascularity with multiple peripheral vessels radiating toward a central point within the mass. Usually, if the patient has the appropriate hormonal abnormalities associated with CAH and if sonography shows the appropriate findings, no further workup is necessary.106,107 If confirmation of the diagnosis is required, a biopsy under ultrasound guidance may be obtained intraoperatively when the testis is exposed. Additionally, testicular vein sampling will show elevated cortisol levels compared with peripheral blood levels.108 Treatment with glucocorticoid replacement therapy results in stabilization or regression of the masses.109

Splenogonadal Fusion Splenogonadal fusion is a rare congenital anomaly in which there is fusion of the spleen and gonad. It typically occurs on the left side and is most often associated with cryptorchidism.110 There are two types of splenogonadal fusion: continuous and discontinuous. In the more common continuous form, the gonad is linked to the spleen by a fibrous cord of splenic tissue. In the discontinuous form, ectopic splenic tissue is attached to the testis. Rarely, ectopic splenic tissue may occur on the epididymis or spermatic cord. Splenogonadal fusion may mimic testicular malignancy. The diagnosis may be established by documenting uptake on a technetium-99m sulfur colloid scan. Calcifications Scrotal calcifications may be seen within the parenchyma of the testis or epididymis, attached to the tunica, or freely located in the fluid between the layers of the tunica vaginalis. Large, smooth, curvilinear intratesticular calcifications without an associated soft tissue mass are characteristic of a large-cell calcifying Sertoli cell tumor111 (see Fig. 22.9C). Scattered calcifications may be found in tuberculosis, filariasis, and scarring from regressed germ cell tumor or trauma.

Scrotal Calcifications TESTICULAR Solitary, postinflammatory granulomatous, vascular Microlithiasis Regressed, or “burned-out,” germ cell tumor Large-cell calcifying Sertoli cell tumor Teratoma Mixed germ cell tumor Sarcoid Tuberculosis Chronic infarct Posttraumatic EXTRATESTICULAR Tunica vaginalis, “scrotal pearls” Torsed appendages Chronic epididymitis Schistosomiasis

Testicular microlithiasis is a condition in which calcifications are present within the seminiferous tubules of the testis either unilaterally or bilaterally. It is postulated that microlithiasis is caused by defective Sertoli cell phagocytosis of degenerating tubular cells, which then calcify within the seminiferous tubules.112,113 Microlithiasis has been classified as diffuse and limited.114 In the diffuse form, innumerable small, hyperechoic foci are diffusely scattered throughout the testicular parenchyma. These tiny (1-3 mm) foci rarely shadow and occasionally demonstrate a comet-tail appearance (Fig. 22.16). In the limited form, less than five hyperechoic foci are seen per image of the testis (Fig. 22.16B). Microlithiasis is seen in 1% to 2% of patients referred for testicular sonography and has a reported prevalence in the general population of 0.6% to 0.9%.115 Microlithiasis has been associated with cryptorchidism, Klinefelter syndrome, Down syndrome, pulmonary alveolar microlithiasis, AIDS, neurofibromatosis, previous radiotherapy, and subfertility.112,115-117 Microlithiasis is typically an incidental finding on scrotal ultrasound, and if

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FIG. 22.16  Microlithiasis and Associated Testicular Tumors: Spectrum of Appearances.  (A) Light microscopy examination shows multiple intratubular calcifications (dark areas) characteristic of microlithiasis. (B) Longitudinal scan shows a few tiny calcifications of limited microlithiasis. (C) and (D) Diffuse microlithiasis. (E) Transverse scan of testis shows microlithiasis and partially cystic mass caused by mixed germ cell tumor. (F) Limited microlithiasis with seminoma. Longitudinal scan shows a few tiny calcifications and a homogeneous hypoechoic mass. (G) Longitudinal scan shows microlithiasis and two hypoechoic homogeneous masses (arrows) due to seminoma. (H) Longitudinal scan shows large hypoechoic mass with multiple small and coarser calcifications. (I) Dual transverse image shows large hypoechoic left testicular mass and microcalcifications in the right testis.

associated with a mass, management is dictated by the intratesticular mass itself. It has been correlated with testicular carcinoma, although the extent of the risk for subsequent development of neoplasm and the recommended surveillance in the setting of microlithiasis remain controversial.114,115,118 Annual physical examination and periodic self-examination have been suggested for those who have no additional risk factors.114,115,119,120 Recent literature suggests that there is no causal link and that sonographic follow-up of microlithiasis should be determined by any additional risk factors and not the microlithiasis itself.121

EXTRATESTICULAR PATHOLOGIC LESIONS Tunica Vaginalis Hydrocele, Hematocele, and Pyocele The normal scrotum contains a few milliliters of serous fluid between the layers of the tunica vaginalis, and this is usually

visible on sonographic examination. Larger volumes of serous fluid, and blood, pus, or urine may also accumulate in the space between the parietal and visceral layers of the tunica vaginalis lining the scrotum. These fluid collections should be confined to the anterolateral portions of the scrotum because of the attachment of the testis to the epididymis and scrotal wall posteriorly (the bare area)9 (Fig. 22.17). Hydrocele is an abnormal accumulation of serous fluid between the layers of the tunica vaginalis. Hydrocele is the most common cause of painless scrotal swelling14 and may be congenital or acquired. The congenital type results from incomplete closure of the processus vaginalis, with persistent open communication between the scrotal sac and the peritoneum, usually resolving by 18 months of age (Fig. 22.17D). Acquired hydroceles may be idiopathic or caused by epididymitis, epididymo-orchitis, torsion, or, in rare cases, tumors. Hydroceles associated with testicular tumors are usually small.3,122,123 Sonography is useful in detecting a potential cause of the hydrocele by allowing evaluation of the testis when a

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FIG. 22.17  Scrotal Fluid Collections: Spectrum of Appearances.  (A) Hydrocele. Transverse scan shows a large hydrocele anterolaterally with testis partially enveloped by tunica vaginalis posteriorly. (B) Encysted hydrocele. Longitudinal scan along the spermatic cord shows a fluid collection present in the inguinal canal. (C) Encysted hydrocele. Coronal CT image of patient in B demonstrates a well circumscribed fluid collection (arrow) corresponding to sonographic examination. (D) Patent processus vaginalis. Longitudinal scan of inguinal region shows an elongated fluid collection (arrows) above the level of the testis and epididymis (E) in patient with chronic hydrocele. (E) Hematocele. Transverse scan shows loculated fluid with internal echoes and mass affect on the testis (T). (F) Pyocele. Longitudinal scan shows an irregular, centrally hypodense, extratesticular (T, testis) collection (arrow) adjacent to the epididymis (E) in the setting of epididymo-orchitis.

large hydrocele hampers palpation. Hydroceles are characteristically anechoic collections with good sound transmission surrounding the anterolateral aspects of the testis. Low-level to medium-level echoes from fibrin bodies or cholesterol crystals may occasionally be visualized moving freely within a

hydrocele.124 Rarely, a large hydrocele may impede testicular venous drainage and cause absence of antegrade arterial diastolic flow.122 Uncommonly, a hydrocele may be loculated around the spermatic cord above the testis and epididymis, representing a noncommunicating, encysted hydrocele; or the

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collection communicates with the peritoneum but not the scrotum, a funicular hydrocele125 (Fig. 22.17B and C). Hematoceles and pyoceles are less common than simple hydroceles. Hematoceles (accumulation of blood within the tunica vaginalis) result from trauma, surgery, neoplasms, or torsion.126 Pyoceles result from untreated epididymo-orchitis or rupture of an intratesticular abscess into the space between the layers of the tunica vaginalis. Both hematoceles and pyoceles appear as complex fluid collections with internal septations and loculations (Fig. 22.17). Thickening of the scrotal skin and calcifications may be seen in chronic cases.

Paratesticular Masses Most extratesticular neoplasms in adults are benign, but extratesticular neoplasms in children are frequently malignant.127

Extratesticular Tumors/Masses BENIGN Hernia Adenomatoid tumor Fibroma/fibrous pseudotumor Lipoma Hemangioma Leiomyoma Neurofibroma Cholesterol granuloma Polyorchidism Papillary cystadenoma Adrenal rest MALIGNANT Fibrosarcoma Liposarcoma Rhabdosarcoma Histiocytoma Lymphoma Metastases

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Hernia An inguinal hernia is a common paratesticular mass.128 Although scrotal hernias are usually diagnosed on the basis of clinical history and physical examination, sonography is useful in the evaluation of atypical cases. Hernias are classified as either direct or indirect. An indirect hernia exits the abdominal cavity through the internal inguinal ring, can traverse the inguinal canal, and extend into the scrotum. Indirect hernias are associated with a patent processus vaginalis. A direct hernia represents a protrusion through the abdominal wall at Hesselbach triangle, an area of weakness bordered by the lateral border of the rectus sheath medially, the inferior epigastric artery laterally, and the inguinal ligament inferiorly. Sonographic appearance of an inguinal hernia depends on its contents. Bowel will often be fluid filled with multiple internal bright echoes. Bowel gas may cause shadowing, a finding also seen with abscesses and thus potentially confusing. The presence of bowel loops within the hernia may be confirmed by the visualization of valvulae conniventes or haustrations and detection of peristalsis on real-time examination (Fig. 22.18A). The presence of highly echogenic material within the scrotum may result from a hernia containing omentum or other fatty masses such as lipomas, although lipomas are typically well defined and herniated omentum can typically be traced back to the inguinal canal (Fig. 22.18B). Sonographic examination of the inguinal canal into the scrotum is necessary to make the diagnosis.129 Additional discussion of hernias can be found in Chapter 13. Calculi Extratesticular scrotal calculi are calcifications within the tunica vaginalis (Fig. 22.19). These fibrinoid loose bodies have been called scrotoliths, or “scrotal pearls” because of their macroscopic appearance, which is usually rounded, pearly white, and rubbery. Histologically, they consist of fibrinoid material deposited around a central nucleus of hydroxyapatite.130 They may result from inflammatory deposits that form and then ultimately separate

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FIG. 22.18  Indirect Inguinal Hernias: Spectrum of Appearances.  (A) Herniated small bowel. Oblique scan shows herniated small bowel (arrow) superior to and abutting the testis (T). (B) Herniated mesenteric fat. Longitudinal scan shows herniated fat (H) above testis (T) and epididymis (E).

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FIG. 22.19  Benign Intrascrotal Calcification.  (A) Calcified tunica plaque (arrow) on the tunica vaginalis. (B)-(D) Scrotal pearls. (B) Mobile scrotal calcification in a small hydrocele. (C) Longitudinal scan shows a mostly calcified scrotal pearl (arrow) in a hydrocele. T, Testis. (D) Bilateral scrotal pearls.

from the tunica vaginalis, or from torsion of the appendix testis or appendix epididymis. Sonographically, they appear as free floating, echogenic calculi with posterior acoustic shadowing; can be multiple; and range in size from a few millimeters to larger than a centimeter. Hydroceles facilitate the sonographic diagnosis of scrotal calculi.

Varicocele A varicocele is an abnormal dilatation of the veins of the pampiniform plexus located posterior to the testis, adjacent to the epididymis, and accompanying the vas deferens within the spermatic cord14 (Fig. 22.20). A varicocele is the most frequently encountered mass of the spermatic cord. The veins of the pampiniform plexus normally range from 0.5 to 1.5 mm in diameter, with a main draining vein up to 2 mm in diameter.

The size for normal varies, with some diagnosticians using greater than 2 mm as a guideline for the diagnosis of a varicocele and others using 3 mm.131 There are two types of varicoceles: primary (idiopathic) and secondary. The idiopathic varicocele is caused by incompetent valves in the internal spermatic vein, which results in impaired drainage of blood from the spermatic vein and pampiniform plexus with the patient in an upright position. Varicoceles affect approximately 15% of men but occur in up to 40% of men attending infertility clinics.132,133 Varicocele is the most common correctable cause of male infertility.134 Idiopathic varicoceles occur much more commonly on the left side and are most common in men aged 15 to 25 years. The left-sided predominance probably occurs because the left testicular vein is longer, with venous drainage into the left renal vein entering the renal vein

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FIG. 22.20  Varicocele.  (A) Longitudinal and (B) color Doppler images show serpentine, hypoechoic, dilated veins posterior to the testis. The blood flow in a varicocele is slow and may be detected only with low-flow Doppler settings or the Valsalva maneuver. See also Video 22.3.

at a right angle, as opposed to the right spermatic vein, which drains directly into the vena cava. Idiopathic varices normally distend when the patient is upright or performs the Valsalva maneuver and decompress when the patient is supine. Primary varicoceles are bilateral in up to 50% of cases.135 Secondary varicoceles result from increased pressure on the spermatic vein or its tributaries by marked hydronephrosis, an enlarged liver, abdominal neoplasms, or venous compression by a retroperitoneal mass.43 Secondary varicoceles may also occur in nutcracker syndrome (nutcracker phenomenon), in which the superior mesenteric artery compresses the left renal vein.136 A search for neoplastic obstruction of gonadal venous return must be undertaken in cases of a right-sided, nondecompressible, or newly discovered varicocele in a patient older than 40 years14 (Fig. 22.21). The appearance of secondary varicoceles is not affected by patient position. In infertile men, sonography aids in the diagnosis of clinically palpable and subclinical varicoceles. Sonography is also of value in assessing testicular size before and after treatment, because varicocele may be associated with a decreased testicular volume.133 There is poor correlation between the size of the varicocele and the degree of testicular tissue damage leading to infertility, and surgical repair of subclinical varicoceles for infertility has been controversial.137 Sonographically, a varicocele consists of multiple, serpentine, anechoic structures more than 2 mm in diameter, creating a tortuous, multicystic collection located adjacent or proximal to the upper pole of the testis and head of the epididymis. A highfrequency transducer in conjunction with low-flow Doppler settings should be used to optimize slow-flow detection within varices. Slowly moving red blood cells may be visualized with

high-frequency transducers, even when flow is too slow to be detected by Doppler imaging. Venous flow can be augmented with the patient in the upright position or during Valsalva maneuver (Video 22.3). Varicoceles follow the course of the spermatic cord into the inguinal canal and are easily compressed by the transducer.3 Rarely, varicoceles may be intratesticular, either in a subcapsular location or around the mediastinum testis138,139 (Fig. 22.22).

Fibrous Pseudotumor Fibrous pseudotumor is a rare, nonneoplastic mass of reactive fibrous tissue that most commonly involves the tunica vaginalis. These masses are known by a number of names, including fibroma, paratesticular fibrosis, or inflammatory pseudotumor, and can become quite large and mimic neoplasms. Most patients present with a painless scrotal mass, possibly with a prior history of infection or trauma. Histologically, masses are composed of hyalinized collagen and granulation tissue and may be partially calcified. On sonography, fibrous pseudotumors may appear as one or more solid masses attached to or closely associated with the capsule of the testis. There may be an associated hydrocele. Echogenicity is variable and they may be seen as a hypoechoic, hyperechoic, or heterogeneous paratesticular mass with posterior acoustic shadowing depending on extent of calicfications140-142 (Fig. 22.23A and B). Polyorchidism Polyorchidism, or supernumerary testes, is a rare entity thought to result from abnormal division of the genital ridge embryologically. The supernumery testes are intrascrotal in location in approximately 75% of cases and present as a painless scrotal

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FIG. 22.21  Varicocele Caused by Retroperitoneal Paraganglioneuroma.  (A) Longitudinal scan shows extremely dilated veins of large, right varicocele. (B) Transverse abdominal sonogram shows paraganglioneuroma (arrow) adjacent to the inferior vena cava (I). A, Aorta; GB, gallbladder. (C) Axial CT scan shows the vascular mass (arrows) adjacent to inferior vena cava.

Epididymal Lesions

FIG. 22.22  Intratesticular Varicocele.  Longitudinal scan shows the dilated intratesticular veins.

mass (Fig. 22.24). Twenty percent of supernumery testes are inguinal with the remaining retroperitoneal in location.60 These supernumery testes have similar imaging characteristics to normal testes, but they are more mobile and therefore at increased risk of torsion. There has also been an increased risk of carcinoma reported.131,135,137,143

Cystic Lesions The most common epididymal mass is a cyst, which includes epididymal cysts and spermatoceles. Both were seen in 20% to 40% of all asymptomatic patients studied by Leung et al.,144 and were multiple in 30% of cases. Both epididymal cysts and spermatoceles are thought to result from dilatation of the epididymal ductules, but the contents of these masses differ.14 Epididymal cysts contain clear serous fluid, whereas spermatoceles are filled with spermatozoa and sediment containing lymphocytes, fat globules, and cellular debris, giving the fluid a thick, milky appearance.3 Both lesions may result from prior episodes of epididymitis or trauma. Spermatoceles and epididymal cysts appear identical on sonography: anechoic, circumscribed masses with no or few internal echoes. Loculations and septations are often seen (Fig. 22.25). In rare cases, a spermatocele may be hyperechoic.9 Differentiation between a spermatocele and an epididymal cyst is rarely important clinically. Spermatoceles almost always occur in the head of the epididymis and represent cystic dilatation of efferent ductules, whereas epididymal cysts arise throughout the length of the epididymis.

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FIG. 22.23  Extratesticular Scrotal Solid Masses: Spectrum of Appearances.  (A) Fibrous pseudotumor. Transverse scan shows a mass of mixed echogenicity lateral to and separate from the testis. (B) Fibrous pseudotumor. Longitudinal scan shows a lamellated extratesticular mass (arrow) with a central echogenic focus adjacent to the tunica of the testis (T). (C) Benign adenomatoid tumor of epididymis. Longitudinal scan shows a hypoechoic mass (arrow) in the epididymal tail separate from the testis (T). (D) Spermatic cord lipoma. Longitudinal scan shows an echogenic mass superior to the epididymis and testis, along the spermatic cord. (E) Liposarcoma. Transverse scan shows a large heterogeneous mass (arrow) deep to the testis (T) in the scrotal wall or spermatic cord. (F) Liposarcoma. Contrast-enhanced axial CT image shows a heterogeneous mass containing fat and solid components (arrow) associated with the spermatic cord in patient E, consistent with a liposarcoma. (G) Leiomyoma of cord. Longitudinal scan shows a solid mass superior to the testis. (H) Rhabdomyosarcoma. Longitudinal extended–field of view scan in a 12-year-old shows a large, paratesticular mass inferior to the testis. (I) Metastasis from lung carcinoma. Longitudinal scan shows a heterogenous mass with calcifications in the tail of the epididymis.

Tumors The most common epididymal neoplasm is the benign adenomatoid tumor, which accounts for approximately 30% of all paratesticular neoplasms, second only to lipoma.28 Although most frequently located in the tail (see Fig. 22.23C), adenomatoid tumors may occur anywhere in the epididymis and have also been reported in the spermatic cord, as well as the tunica albuginea, where they may grow intratesticularly. Adenomatoid tumor may occur at any age but most often affects patients aged 20 to 50 years.3,145 Adenomatoid tumors are generally unilateral, solitary, well defined, and round or oval, rarely measuring more than 5 cm in diameter. Occasionally, they may appear plaquelike and poorly defined. Sonography usually shows a solid,

well-circumscribed mass with echogenicity that is at least as great as the testis,3 although they may also be hypoechoic. Other benign extratesticular tumors are rare and include lipomas (see Fig. 22.23D), leiomyomas (see Fig. 22.23G), fibromas, hemangiomas, neurofibromas, and cholesterol granulomas. Adrenal rests may also be encountered in the spermatic cord, testis, epididymis, rete testis, and tunica albuginea, typically in the setting of CAH. Papillary cystadenoma of the epididymis is a rare tumor with a strong association with von Hippel–Lindau disease. Up to 40% of cystadenomas are bilateral, a finding that is virtually pathognomic for von Hippel–Lindau disease. These tumors are benign epithelial tumors of the epididymis, occurring in the

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dilated vas deferens may be seen in addition to the enlarged epididymis. An unusual appearance described as “dancing megasperm” is occasionally seen in patients with vasectomy (Video 22.5). High reflective echoes within the dilated epididymis appear to move independently, shown histologically to be aggregations of spermatozoa and macrophages.152

FIG. 22.24  Polyorchidism.  Transverse extended field of view image of the right hemiscrotum shows a right testis (R) and two additional intrascrotal masses with similar imaging characteristics to the right testis (*) consistent with supernumery testes in an asymptomatic patient with a palpable mass.

efferent ductules of the epididymal head. They generally present as a hard, palpable mass, and at ultrasound appear as an echogenic, solid mass with distinct, small cystic spaces. The majority of solid epididymal masses are benign. However, primary extratesticular scrotal malignant neoplasms do occur, including adenocarcinoma, fibrosarcoma, liposarcoma (see Fig. 22.23E and F), histiocytoma, and lymphoma in adults and rhabdomyosarcoma in children (see Fig. 22.23H). Metastatic tumors to the epididymis are also rare. The most common primary sites include the testis, stomach, kidney, prostate, colon, and, less often, the pancreas146,147 (see Fig. 22.23I). Size of the lesion and the presence of color flow may be helpful in the diagnosis of extratesticular scrotal masses.23,148 Larger masses (>1.5 cm) with prominent color flow that present without cl inical symptoms of inflammation are more likely to be malignant.23,148

Sperm Granuloma Sperm granulomas are thought to arise from extravasation of spermatozoa into the soft tissues surrounding the epididymis, producing a necrotizing granulomatous response.3 These lesions may be painful or asymptomatic, and they are most often found in patients after vasectomy. It is assumed that vasectomy produces increased pressure in the epididymal ductules, causing rupture with subsequent formation of sperm granulomas. Sperm granulomas may also be associated with prior epididymal infection or trauma. The typical sonographic appearance is that of a solid, hypoechoic or heterogeneous mass, usually located in or adjacent to the epididymis, although it may simulate an intratesticular lesion (Fig. 22.26A). Chronic sperm granulomas may contain calcification.149 Postvasectomy Changes in the Epididymis Sonographic changes in the epididymis are very common in patients after vasectomy.150,151 In addition to the formation of sperm granulomas, these findings include epididymal enlargement with ductular ectasia involving the epididymis (Fig. 22.26B) and rete testis, as well as the development of cysts (Video 22.4). A

Chronic Epididymitis Chronic epididymitis is more commonly seen with conditions associated with granulomatous reactions, including tuberculosis, brucellosis, syphilis, and parasitic and fungal infections.60 Tuberculosis epididymal infections are the most common of these and are believed to result from renal disease seeding the lower genitourinary tract, with 25% of patients having bilateral involvement.153 Patients with chronic granulomatous epididymitis caused by spread of tuberculosis from the genitourinary tract complain of a hard, nontender scrotal mass.14 Sonography most often shows a thickened tunica albuginea and a thickened, irregular epididymis with variable appearance (Fig. 22.27). Calcification may be identified within the tunica albuginea or epididymis.3 Associated findings include hydroceles, scrotal wall thickening, and fistulas.153 Untreated granulomatous epididymitis can spread to the testes, causing an epididymo-orchitis, although this is less common than isolated epididymal disease. Focal testicular involvement may demonstrate a variable sonographic appearance and may simulate the appearance of a testicular neoplasm on sonography. Patients may also develop chronic epididymitis after episodes of acute bacterial epididymitis that do not subside. Sarcoidosis Sarcoidosis is a noninfectious, chronic, granulomatous disease that may involve the genital tract.154-156 In an autopsy series, approximately 5% of cases had genital tract involvement, with the epididymis most frequently involved.60 The clinical presentation is acute or recurrent epididymitis or painless enlargement of the testis or epididymis. Sonographically, sarcoid lesions are irregular, hypoechoic solid masses in the testis or epididymis (Fig. 22.28). Occasionally, hyperechoic, calcific foci with acoustic shadowing may be seen. Distinguishing sarcoidosis from an inflammatory process or a neoplasm is difficult on sonography alone. Resection or orchiectomy may be necessary for definitive diagnosis. As noted previously, tuberculosis can also cause a chronic granulomatous reaction of the genital tract, typically a granulomatous epididymitis.

ACUTE SCROTAL PAIN Acute scrotal pain may have numerous causes. More common causes include torsion of the spermatic cord and testis, epididymitis or orchitis, torsion of a testicular appendage, acute hydrocele, strangulated hernia, idiopathic scrotal edema, Henoch-Schönlein purpura, abscess, traumatic hemorrhage, hemorrhage into a testicular neoplasm, and scrotal fat necrosis. Torsion of the spermatic cord and acute epididymitis or epididymo-orchitis are the most common causes of acute scrotal pain. These entities cannot be distinguished by

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FIG. 22.25  Extratesticular Scrotal Cysts: Spectrum of Appearances.  (A) Spermatocele. Longitudinal scan shows an anechoic cyst in head of the epididymis. (B) Spermatocele. Longitudinal scan shows a large cyst containing internal echoes in head of the epididymis. (C) Septate spermatocele. Longitudinal scan shows a septate cyst in head of the epididymis. (D) Epididymal cyst. Longitudinal scan shows a cyst in body of the epididymis. (E) Cyst of vas deferens remnant. Longitudinal scan shows a cyst with internal echoes inferior to the testis (surgically proven). (F) Epidermoid inclusion cyst of epididymis. Longitudinal color Doppler scan shows bilobed cystic mass in head of the epididymis surrounded by vessels.

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FIG. 22.26  Postvasectomy Changes.  (A) Sperm granuloma. Transverse scan shows a heterogeneous mass (arrow) along the vas deferens and separate from the epididymis (E) in a postvasectomy patient. (B) Postvasectomy changes in epididymis. Longitudinal image of the scrotum shows ectasia of the ductules of the epididymis (arrows) in a patient who had a vasectomy. See also Videos 22.4 and 22.5.

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FIG. 22.27  Tuberculous Epididymo-orchitis.  (A) Longitudinal scan shows a heterogeneous mass with calcification involving the head and body of the epididymis and the adjacent testis (T). (B) Longitudinal color Doppler image shows increased vascularity in the epididymis and adjacent testis.

rate from torsion but also an increase in unnecessary surgical procedures. Real-time sonography, Doppler sonography, testicular radionuclide scintigraphy, and MRI have been used to increase the accuracy of distinguishing between infection and torsion.158 Currently, sonography using color flow or power Doppler is the imaging study of choice to diagnose the cause of acute scrotal pain.

FIG. 22.28  Testicular Sarcoid.  Longitudinal scan of the testis shows multiple, small, hypoechoic, solid masses resulting from sarcoid.

routine physical examination or laboratory tests in up to 50% of patients.157 In the past, immediate surgical exploration was been advised in boys and young men with acute scrotal pain, unless a definitive diagnosis of epididymitis or orchitis was made. This aggressive approach resulted in an increased testicular salvage

Causes of Acute Scrotal Pain Torsion of the testis Epididymo-orchitis Testicular or epididymal appendage torsion Strangulated hernia Trauma Idiopathic scrotal edema Henoch-Schönlein purpura

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Torsion Torsion is more common in adolescent boys and represents approximately 20% of the acute scrotal pathologic phenomena in postpubertal males.3 Prompt diagnosis is necessary because torsion requires immediate surgery to preserve the testis. The testicular salvage rate is over 80% if surgery is performed within 5 or 6 hours of the onset of pain, 70% if surgery is performed within 6 to 12 hours, and only 20% if surgery is delayed for more than 12 hours.159 Two types of testicular torsion have been described: intravaginal and extravaginal. Extravaginal torsion occurs prenatally and in newborns up to 30 days after delivery. Torsion occurs outside of the tunica vaginalis when the testis, gubernaculum, and tunica vaginalis are not fixed to the scrotal wall, allowing rotation of these structures as a unit and causing torsion of the cord at the level of the external ring. If this occurs prenatally, the affected neonate presents with a firm, painless mass in the scrotum, and swelling and discoloration of the affected side. The testis is typically infarcted and necrotic at birth. Postnatal testicular torsion is detected as a change in the testicular examination.160,161 Intravaginal torsion is the more common type, arising within the tunica vaginalis and occurring most frequently at puberty. It results from anomalous suspension of the testis by a long stalk of spermatic cord mesentery, resulting in complete investment of the distal cord, testis, and epididymis by the tunica vaginalis. This allows the testis to swing and rotate within the tunica vaginalis like a clapper inside a bell, the so-called bell-clapper deformity (Fig. 22.29). Anomalous testicular suspension is bilateral in 50% to 80% of patients; hence the contralateral testis is usually fixed at the time of surgery as well. Sonography is considered the first step in evaluation of the acute scrotum, and its role is well established.162-164 Sonographic findings vary with duration and degree of rotation. Gray-scale sonographic changes are nonspecific in the acute phase of torsion.157,161,165 A torsed testis with normal, homogeneous echogenicity on gray-scale imaging has a high chance of successful salvage at surgery.166 Testicular enlargement and decreased echogenicity are the most common findings 4 to 6 hours after the onset of torsion. With continued torsion, at 24 hours the testis can develop heterogeneous echotexture secondary to vascular congestion, hemorrhage, and infarction167-169 (Fig. 22.30). A hypoechoic or heterogeneous echogenicity may indicate nonviability, although this is not specific.166 Torsion may change the position of the long axis of the testis. Extratesticular sonographic findings typically occur in torsion and are important to recognize. The spermatic cord immediately cranial to the testis and epididymis is twisted, causing a characteristic torsion knot or “whirlpool pattern” of concentric layers seen on sonography or MRI161,170,171 (Fig. 22.30G and H). The epididymis may be enlarged and heterogeneous because of hemorrhage or ischemia, and may be difficult to separate from the torsion knot of the spermatic cord. This spherical epididymiscord complex can be mistaken for epididymitis.161 A reactive hydrocele and scrotal skin thickening are often seen with torsion. Large, echogenic, or complex extratesticular masses caused by hemorrhage in the tunica vaginalis or epididymis may be seen

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FIG. 22.29  “Bell-Clapper” Anomaly, Intravaginal Torsion, and Extravaginal Torsion.  (A) Normal anatomy. The tunica vaginalis (arrows) does not completely surround the testis and epididymis, which are attached to the posterior scrotal wall (short arrow). (B) Bell-clapper anomaly. The tunica vaginalis (arrows) completely surrounds the testis, epididymis, and part of the spermatic cord, predisposing to torsion. (C) Intravaginal torsion. Bell-clapper anomaly with complete torsion of the spermatic cord, compromising the blood supply to the testis. (D) Extravaginal torsion in a neonate. Tunica vaginalis (arrows) is in normal position, but abnormal motility allows rotation of the testis, epididymis, and spermatic cord.

in patients with undiagnosed torsion.172 The gray-scale findings of acute and subacute torsion are not specific and may be seen in testicular infarction caused by epididymitis, epididymo-orchitis, and traumatic testicular rupture or infarction. Doppler sonography is the most useful and most rapid technique to establish the diagnosis of testicular ischemia and to help distinguish torsion from epididymo-orchitis.157,162,167 The absence of intratesticular blood flow at color and power Doppler ultrasound is considered diagnostic of ischemia (color and power techniques appear to have equivalent sensitivity in the diagnosis of torsion).173-178 Meticulous scanning of the testicular parenchyma with the use of low-flow detection Doppler settings (low pulse repetition frequency, low wall filter, high Doppler gain, small color sampling box, lowest possible threshold setting) is important because intratesticular vessels are small and have low flow velocities, especially in prepubertal boys. Color flow Doppler sonography is more sensitive for showing decreased testicular flow in incomplete torsion than is nuclear scintigraphy, which is rarely

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FIG. 22.30  Torsion of Spermatic Cord and Testis: Spectrum of Appearances.  (A)-(D) Acute torsion. Longitudinal power Doppler scans show (A) no flow in the testis and (B) abnormal, transverse, and vertical orientation of the testis with no flow. (C) After manual detorsion of case in B, longitudinal color Doppler scan shows the normal orientation of the testis with blood flow present. The testis has a striated appearance caused by the previous ischemia. (D) Dual transverse gray-scale scan shows enlarged hypoechoic right testis resulting from torsion and skin thickening in the right hemiscrotum. (E) Partial torsion. Longitudinal scan with spectral Doppler shows a high-resistance testicular arterial waveform with little diastolic flow because of venous occlusion; a small, reactive hydrocele was found. (F) After spontaneous detorsion of case in E, longitudinal scan with spectral Doppler shows return of diastolic flow. (G) Torsion knot. Longitudinal scan with acute spermatic cord torsion shows the “torsion knot” complex of epididymis and spermatic cord. (H) Acute torsion. Intraoperative photograph shows the twisted spermatic cord that gives the torsion knot appearance on sonograph. (I) Subacute torsion (3 days of pain). Transverse power Doppler scan shows absent flow within the testis with surrounding hyperemia. (H with permission from Winter TC. Ultrasonography of the scrotum. Appl Radiol 2002;31[3]:9-18.169)

used anymore to diagnose torsion.179 In testicular torsion, color Doppler sonography has a sensitivity of 80% to 98%, specificity of 97% to 100%, and accuracy of 97%.161,162,180 The use of intravascular contrast agents in sonography can improve the sensitivity and specificity of detecting blood flow in the scrotum.175,181 In pediatric patients, it may be difficult to document flow in a normal testis.182 In practice, many surgeons elect to explore the testis

surgically if clinical symptoms and signs are suggestive and results of the sonographic examination are equivocal. Torsion is not an all or none phenomenon. Potential pitfalls in using sonography in the diagnosis of torsion are partial torsion, torsion/detorsion, and ischemia from orchitis. Torsion of at least 540 degrees is necessary for complete arterial occlusion.162,183 With partial torsion of 360 degrees or less, arterial flow may still

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occur, but venous outflow is often obstructed, causing diminished diastolic arterial flow on spectral Doppler examination184,185 (Fig. 22.30E). If spontaneous detorsion occurs, flow within the affected testis may be normal, or it may be increased and mimic orchitis.186 Spontaneous detorsion can occur with sequelae including a segmental testicular infarction.102,103 Segmental testicular infarction may also occur with Henoch-Schönlein purpura or with orchitis (see Fig. 22.14). Orchitis may also cause global ischemia of the testis and mimic torsion.186 In subacute or chronic torsion, Doppler sonography demonstrates no flow in the testis and increased flow in the paratesticular tissues, including the epididymis-cord complex and dartos fascia (Fig. 22.30I). Torsion of the appendix testis or appendix epididymis can present with acute scrotal pain, potentially mimicking testicular torsion clinically, although there are no other clinical symptoms and the cremasteric reflex can still be elicited. Patients are rarely referred for imaging because the pain is usually not severe, and the twisted appendage may be evident on physical examination as a small firm nodule palpable at the superior aspect of the testis, with a bluish discoloration, or the “blue dot” sign.187 Up to 95% of twisted appendages involve the appendix testis and occur most often in boys aged 7 to 14 years.65 The sonographic appearance of the twisted testicular appendage has been described as an avascular hyperechoic mass with a central hypoechoic focus adjacent to the head of a normally perfused testis and surrounded by an area of increased color Doppler perfusion.162,188 These cases are managed conservatively with pain typically resolving in 2 to 3 days with interval atrophy of the torsed appendage. The role of sonography is to exclude testicular torsion or epididymoorchitis. Idiopathic scrotal edema typically affects prepubertal boys, with acute onset of relatively painless scrotal erythema and subcutaneous edema. Idiopathic scrotal edema typically resolves spontaneously in 1 to 3 days without sequelae.

Epididymitis and Epididymo-orchitis Epididymitis is the most common cause of acute scrotal pain in postpubertal men. It may be acute or chronic, depending on the inciting organism and the duration of the process. Acute epididymitis usually results from a lower urinary tract infection and is less often hematogenous or traumatic in origin. The common causative organisms are Escherichia coli, Pseudomonas, and Klebsiella. Sexually transmitted organisms causing urethritis, such as Neisseria gonorrhoeae and Chlamydia trachomatis, are common causes of epididymitis in younger men. Less frequently, epididymitis may be caused by tuberculosis, mumps, or syphilitic orchitis.153,189 The age of peak incidence is 40 to 50 years. Typically, patients present with the insidious onset of pain which increases over 1 or 2 days. Fever, dysuria, and urethral discharge may also be present. In acute epididymitis, sonography characteristically shows enlargement of the epididymis, involving the tail initially and frequently spreading to the entire epididymis190 (Fig. 22.31A and B). The echogenicity of the epididymis is usually decreased and its echotexture is often coarse and heterogeneous, likely secondary to edema, hemorrhage, or both. Color flow Doppler sonography usually shows increased blood flow in the epididymis or testis,

or both, compared with the asymptomatic side.191 Reactive hydrocele formation is common, and associated scrotal wall thickening may be seen. Direct extension of epididymal inflammation to the testis, called epididymo-orchitis, occurs in up to 20% of patients with acute epididymitis. Isolated orchitis may also occur. In such cases, increased blood flow is localized to the testis (Fig. 22.31D and E, Video 22.6). Testicular involvement may be focal or diffuse. Characteristically, focal orchitis produces a hypoechoic area adjacent to an enlarged portion of the epididymis. Color Doppler shows increased flow in the hypoechoic area of the testis; increased flow in the tunica vasculosa may also be visible as lines of color signal radiating from the mediastinum testis.192 These lines of color correspond to septal accentuation visible as hypoechoic bands on gray-scale sonography (Fig. 22.31H and I). Spectral Doppler shows increased diastolic flow in uncomplicated orchitis (Fig. 22.32A). If left untreated, the entire testis may become involved, appearing hypoechoic and enlarged. As pressure in the testis increases from edema, venous infarction with hemorrhage may occur, appearing hyperechoic initially and hypoechoic later.192 Ischemia and subsequent infarction may also occur when the vascularity of the testis is compromised by venous occlusion or venous thrombosis.193 When vascular disruption is severe, resulting in complete testicular infarction, the changes are indistinguishable from those seen in testicular torsion. Color Doppler sonography may show focal areas of reactive hyperemia and increased blood flow associated with relatively avascular areas of infarction in both the testis and the epididymis in patients with severe epididymo-orchitis. Diastolic flow reversal in the arterial waveforms of the testis is an ominous finding, associated with testicular infarction in severe epididymo-orchitis194 (Fig. 22.32B). In addition to infarction, other complications of acute epididymo-orchitis include intratesticular abscess formation and development of a pyocele (see Figs. 22.13 and 22.17F). Chronic changes may be seen in the epididymis or testis from clinically resolved epididymo-orchitis. Swelling of the epididymis may persist and appear as a heterogeneous mass on sonography. The testis may have a persistent, striated appearance of septal accentuation from fibrosis (Figs. 22.33 and 22.34). This striated appearance of the testis is nonspecific and may also be seen after ischemia from torsion or during a hernia repair.192,195 A similar heterogeneous appearance in the testis may be seen in older patients because of seminiferous tubule atrophy and sclerosis.196 Focal areas of infarction in the testis may persist as wedge-shaped or cone-shaped hypoechoic areas or may appear as hyperechoic scars.192 If complete infarction of the testis has occurred because of epididymo-orchitis, the testis may become small, with a hypoechoic or heterogeneous echotexture.

Fournier Gangrene Fournier gangrene is a necrotizing fasciitis of the perineum, external genitalia, and perianal area occurring most frequently in men aged 50 to 70 years. The origin is usually a disease process from the overlying skin, urinary tract, or colorectal area, frequently due to a synergistic polymicrobial infection.197 Predisposing factors include systemic immunosuppression, diabetes mellitus,

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C E FIG. 22.31  Epididymo-orchitis, Epididymitis, and Orchitis: Spectrum of Appearances.  (A) and (B) Acute epididymitis. Longitudinal gray-scale and color Doppler images show enlargement and a heterogeneous echotexture of tail of the epididymis, with greatly increased flow in tail of the epididymis and minimally increased flow in the adjacent testis. (C) Acute epididymo-orchitis. Longitudinal color Doppler scan shows increased flow in the epididymis and testis. (D) and (E) Acute orchitis. Longitudinal dual-image gray-scale and color Doppler images show that right testis is hypoechoic and has greatly increased flow.

chronic alcoholism, and steroid therapy.152 Multiple organisms are usually involved, including Klebsiella, Streptococcus, Proteus, and Staphylococcus. Surgical debridement of devitalized tissue is usually required, and morbidity and mortality are high without prompt treatment. Ultrasound is helpful in diagnosis by demonstrating scrotal wall thickening containing gas with accompanying shadowing.

TRAUMA When evaluating testicular integrity in the setting of acute trauma, the primary role of sonography is to assess for the continuity of the tunica albuginea: this determines clinical management. Disruption of the tunica albuginea indicates testicular rupture. Prompt diagnosis of a ruptured testis is crucial because of the

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FIG. 22.31, cont’d. (F) Longitudinal gray-scale scan with 3 weeks of epididymo-orchitis unresolved with antibiotic therapy shows hypoechoic areas in the testis and an enlarged heterogeneous tail of the epididymis. (G) Color Doppler image shows increased flow in the testis and epididymis with an area of decreased flow due to ischemia (arrow). (H) and (I) Acute orchitis. Longitudinal gray-scale and color Doppler images show hypoechoic bands caused by septal accentuation from edema and increased vascularity of the testis. See also Video 22.6.

direct relationship between early surgical intervention and testicular salvageability. Approximately 90% of ruptured testes can be saved if surgery is performed within the first 72 hours, whereas only 45% may be salvaged after 72 hours.198 Sonographic features of testicular rupture include focal areas of altered testicular echogenicity, corresponding to areas of hemorrhage or infarction, and hematocele formation in 33% of patients. A discrete fracture plane may not be identified. Tunical disruption associated with extrusion of the seminiferous tubules is specific for rupture (Fig. 22.35E, Video 22.7). However, the sensitivity of the diagnosis of rupture based on tunical disruption alone is only 50%. Heterogeneity of the testis with associated testicular contour irregularity may be helpful in making the diagnosis of rupture.110,199,200 Color Doppler imaging can be helpful because rupture of the tunica albuginea is almost always associated

with disruption of the tunica vasculosa and loss of blood supply to part or all of the testis.110 Although not specific for a ruptured testicle, these features may suggest the diagnosis in the appropriate clinical setting, prompting immediate surgical exploration. Clinical diagnosis is often impossible because of marked scrotal pain and swelling; thus sonography can be invaluable in the assessment of tunica albuginea integrity and the extent of testicular hematoma.110,198-200 A visibly intact tunica albuginea should exclude rupture, but a complex intrascrotal hematoma may be difficult to distinguish from testicular rupture and may obscure the tunica110,201 (Fig. 22.35A). Patients with large intrascrotal hematomas or hematoceles will often undergo surgical exploration because it is difficult to exclude rupture sonographically in the presence of surrounding complex fluid.110 If a patient with a presumed intratesticular hematoma is not surgically explored,

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FIG. 22.32  Spectral Doppler Changes in Orchitis.  (A) Uncomplicated orchitis. Longitudinal scan with spectral Doppler tracing shows increased diastolic flow in the testis. (B) Orchitis with venous compromise. Longitudinal scan with spectral Doppler tracing in more severe orchitis shows reversal of flow in diastole caused by edema impeding venous flow.

FIG. 22.33  Heterogeneous “Striped” Testis.  Transverse dual image shows heterogeneity in the right testis with marked septal accentuation from previous orchitis. This appearance may also be seen after ischemia.

FIG. 22.34  Fibrosis of Testis After Orchitis.  Pathologic specimen of testis shows linear bands of fibrosis (white areas) caused by previous severe orchitis. A similar “end-stage” testis could have this appearance due to ischemia.

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FIG. 22.35  Testicular Trauma: Spectrum of Appearances.  (A) Hematoma. Longitudinal image shows hematoma (arrows) on the anterior surface of the testis. Tunica intact at surgery. (B) Fracture of testis. Transverse scan shows a heterogeneous testicle with a linear band (arrows) indicating a fracture. H, Testicular hematoma. (C) Tunical tear. Longitudinal color Doppler image shows contour irregularity of the testis with disruption of the tunica (arrow). Extruded testis parenchyma shows no color flow. (D) Same case as C. Photograph during surgery shows tunical tear in the exposed right testis. (E) Rupture of testis. Longitudinal image shows rupture of the testis with extrusion of seminiferous tubules (arrow). (F) In same case as E, photograph during surgery shows a tear in the tunica inferiorly with extrusion of seminiferous tubules. (G) and (H) Fracture of testis. Longitudinal and transverse color Doppler images of the left testis show an irregular linear, hypoechoic, avascular band representing a testicular fracture following acute blunt trauma. The tunica albuginea was intact. See also Video 22.7.

it is incumbent upon the clinician to follow the intratesticular abnormality to resolution because a testicular tumor can mimic an intratesticular hematoma and also predispose to rupture following relatively minor trauma. Testicular fracture refers to discontinuity of normal testicular parenchyma, which may be present in the absence of disruption of the tunica albuginea. An associated intratesticular hematoma or hematocele may be present. Sonographically, the fracture appears as a linear, hypoechoic, avascular band extending across the testicular parenchyma (Fig. 22.35).

Sonography can also be used to discern the severity of scrotal trauma resulting from penetrating scrotal injury. Gunshot injury is the most common cause; other causes include stabbing, self mutilation, human and animal bites, and projectile injuries. Bilateral injuries are more common in the setting of penetrating trauma.202 Penetrating trauma can disrupt the tunica albuginea, as well as penetrate the parenchyma, causing a fracturelike injury. Ultrasound can assess the degree of injury and evaluate for the presence of foreign bodies and for the presence of air, which may denote the path of the penetrating injury.203 Doppler

CHAPTER 22  The Scrotum sonography can assess for viability of the testis in the setting of penetrating trauma. A careful gray-scale and color flow Doppler evaluation of the epididymis should be performed in all examinations of blunt trauma. Traumatic epididymitis may be an isolated finding that should not be confused with an infectious process.204

CRYPTORCHIDISM The testes remain near the deep inguinal ring until the seventh month of gestation when they normally begin their descent through the inguinal canal into the twin scrotal sacs.1,2 The gubernaculum testis is a fibromuscular structure that extends from the inferior pole of the testis to the scrotum and guides the testis in its descent, a process normally completed before birth. Undescended testis is one of the most common genitourinary anomalies in male infants. At birth, 3.5% of male infants weighing more than 2500 g have an undescended testis; 10% to 25% of these cases are bilateral. This figure decreases to 0.8% by age 1 year because the testes descend spontaneously in most infants. The incidence of undescended testes increases to 30% in premature infants, approaching 100% in neonates who weigh less than 1000 g at birth. Complete descent is necessary for full testicular maturation.205,206 Malpositioned testes may be located anywhere along the pathway of descent from the retroperitoneum to the scrotum. Most (80%) undescended testes are palpable, lying distal to the external inguinal ring. Anorchia occurs in 4% of the remaining patients with impalpable testes.206 Localization of the undescended testis is important for the prevention of two potential complications of cryptorchidism: infertility and cancer. The undescended testis is more likely to undergo malignant change than is the normally descended testis.3 The most common malignancy is seminoma. The risk of malignancy is increased in both the undescended testis after orchiopexy and the normally descended testis. Therefore careful serial examinations of both testes are essential. Sonographically, the undescended testis is often smaller and slightly less echogenic than the contralateral, normally descended testis (Fig. 22.36). The pars infravaginalis gubernaculi, which is the distal bulbous segment of the gubernaculum testis, can be

FIG. 22.36  Testis in Inguinal Canal.  Longitudinal scan shows an elongated, ovoid, undescended testis.

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mistaken for the testis. After completion of testicular descent, the pars infravaginalis gubernaculi and the gubernaculum normally atrophy. If the testis remains undescended, both structures persist. The pars infravaginalis gubernaculi is located distal to the undescended testis, usually in the scrotum, but it may be found in the inguinal canal. Sonographically, the pars infravaginalis gubernaculi is a hypoechoic, cordlike structure of echogenicity similar to the testis, with the gubernaculum leading to it.207 Sonography is often used in the initial evaluation of cryptorchidism, although the value of this has been questioned because it is insensitive in detecting high intraabdominal testes.208 MRI has also been used in cryptorchidism because it is more sensitive than ultrasound in detecting undescended testes in the retroperitoneum.209,210 Nonvisualization of an undescended testis on sonography or MRI does not exclude its presence, and therefore laparoscopy or surgical exploration should be performed if clinically indicated. REFERENCES 1. Larsen WJ. Human embryology. New York: Churchill Livingstone; 1993. p. 235-280. 2. Moore KL, Persaud TVN. The developing human: clinically oriented embryology. 5th ed. Philadelphia: Saunders; 1993. 3. Krone KD, Carroll BA. Scrotal ultrasound. Radiol Clin North Am. 1985;23(1): 121-139. 4. Trainer TD. Histology of the normal testis. Am J Surg Pathol. 1987;11(10): 797-809. 5. Siegel MJ. The acute scrotum. Radiol Clin North Am. 1997;35(4): 959-976. 6. Thomas RD, Dewbury KC. Ultrasound appearances of the rete testis. Clin Radiol. 1993;47(2):121-124. 7. Johnson KA, Dewbury KC. Ultrasound imaging of the appendix testis and appendix epididymis. Clin Radiol. 1996;51(5):335-337. 8. Sellars ME, Sidhu PS. Ultrasound appearances of the testicular appendages: pictorial review. Eur Radiol. 2003;13(1):127-135. 9. Black JA, Patel A. Sonography of the normal extratesticular space. AJR Am J Roentgenol. 1996;167(2):503-506. 10. Allen TD. Disorders of the male external genitalia. In: Kelalis PP, King LR, editors. Clinical pediatric urology. Philadelphia: Saunders; 1976. p. 636-668. 11. Middleton WD, Bell MW. Analysis of intratesticular arterial anatomy with emphasis on transmediastinal arteries. Radiology. 1993;189(1):157-160. 12. Fakhry J, Khoury A, Barakat K. The hypoechoic band: a normal finding on testicular sonography. AJR Am J Roentgenol. 1989;153(2):321-323. 13. Bushby LH, Sellars ME, Sidhu PS. The “two-tone” testis: spectrum of ultrasound appearances. Clin Radiol. 2007;62(11):1119-1123. 14. Middleton WD, Thorne DA, Melson GL. Color Doppler ultrasound of the normal testis. AJR Am J Roentgenol. 1989;152(2):293-297. 15. Gooding GA. Sonography of the spermatic cord. AJR Am J Roentgenol. 1988;151(4):721-724. 16. Benson CB, Doubilet PM, Richie JP. Sonography of the male genital tract. AJR Am J Roentgenol. 1989;153(4):705-713. 17. Rifkin MD, Kurtz AB, Pasto ME, Goldberg BB. Diagnostic capabilities of high-resolution scrotal ultrasonography: prospective evaluation. J Ultrasound Med. 1985;4(1):13-19. 18. Rifkin MD, Kurtz AB, Pasto ME, et al. The sonographic diagnosis of focal and diffuse infiltrating intrascrotal lesions. Urol Radiol. 1984;6(1): 20-26. 19. Carroll BA, Gross DM. High-frequency scrotal sonography. AJR Am J Roentgenol. 1983;140(3):511-515. 20. Woodward PJ, Sohaey R, O’Donoghue MJ, Green DE. From the archives of the AFIP: tumors and tumorlike lesions of the testis: radiologic-pathologic correlation. Radiographics. 2002;22(1):189-216.

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130. Linkowski GD, Avellone A, Gooding GA. Scrotal calculi: sonographic detection. Radiology. 1985;156(2):484. 131. Kim ED, Lipshultz LI. Role of ultrasound in the assessment of male infertility. J Clin Ultrasound. 1996;24(8):437-453. 132. Beddy P, Geoghegan T, Browne RF, Torreggiani WC. Testicular varicoceles. Clin Radiol. 2005;60(12):1248-1255. 133. Zucchi A, Mearini L, Mearini E, et al. Varicocele and fertility: relationship between testicular volume and seminal parameters before and after treatment. J Androl. 2006;27(4):548-551. 134. Gonda Jr RL, Karo JJ, Forte RA, O’Donnell KT. Diagnosis of subclinical varicocele in infertility. AJR Am J Roentgenol. 1987;148(1):71-75. 135. Doherty FJ. Ultrasound of the nonacute scrotum. Semin Ultrasound CT MR. 1991;12(2):131-156. 136. Graif M, Hauser R, Hirshebein A, et al. Varicocele and the testicular-renal venous route: hemodynamic Doppler sonographic investigation. J Ultrasound Med. 2000;19(9):627-631. 137. Howards SS. Treatment of male infertility. N Engl J Med. 1995; 332(5):312-317. 138. Tétreau R, Julian P, Lyonnet D, Rouvière O. Intratesticular varicocele: an easy diagnosis but unclear physiopathologic characteristics. J Ultrasound Med. 2007;26(12):1767-1773. 139. Atasoy C, Fitoz S. Gray-scale and color Doppler sonographic findings in intratesticular varicocele. J Clin Ultrasound. 2001;29(7):369-373. 140. Krainik A, Sarrazin JL, Camparo P, et al. Fibrous pseudotumor of the epididymis: imaging and pathologic correlation. Eur Radiol. 2000;10(10): 1636-1638. 141. al-Otaibi L, Whitman GJ, Chew FS. Fibrous pseudotumor of the epididymis. AJR Am J Roentgenol. 1997;168(6):1586. 142. Oliva E, Young RH. Paratesticular tumor-like lesions. Semin Diagn Pathol. 2000;17(4):340-358. 143. Thum G. Polyorchidism: case report and review of literature. J Urol. 1991;145(2):370-372. 144. Leung ML, Gooding GA, Williams RD. High-resolution sonography of scrotal contents in asymptomatic subjects. AJR Am J Roentgenol. 1984;143(1):161-164. 145. Pavone-Macaluso M, Smith PH, Bagshaw MA, editors. Testicular cancer and other tumors of the genitourinary tract. New York: Plenum Press; 1985. 146. Smallman LA, Odedra JK. Primary carcinoma of sigmoid colon metastasizing to epididymis. Urology. 1984;23(6):598-599. 147. Wachtel TL, Mehan DJ. Metastatic tumors of the epididymis. J Urol. 1970;103(5):624-627. 148. Yang DM, Kim SH, Kim HN, et al. Differential diagnosis of focal epididymal lesions with gray scale sonographic, color Doppler sonographic, and clinical features. J Ultrasound Med. 2003;22(2):135-142. 149. Oh C, Nisenbaum HL, Langer J, et al. Sonographic demonstration, including color Doppler imaging, of recurrent sperm granuloma. J Ultrasound Med. 2000;19(5):333-335. 150. Reddy NM, Gerscovich EO, Jain KA, et al. Vasectomy-related changes on sonographic examination of the scrotum. J Clin Ultrasound. 2004;32(8):394-398. 151. Ishigami K, Abu-Yousef MM, El-Zein Y. Tubular ectasia of the epididymis: a sign of postvasectomy status. J Clin Ultrasound. 2005;33(9):447-451. 152. Stewart VR, Sidhu PS. The testis: the unusual, the rare and the bizarre. Clin Radiol. 2007;62(4):289-302. 153. Chung JJ, Kim MJ, Lee T, et al. Sonographic findings in tuberculous epididymitis and epididymo-orchitis. J Clin Ultrasound. 1997;25(7): 390-394. 154. Carmody JP, Sharma OP. Intrascrotal sarcoidosis: case reports and review. Sarcoidosis Vasc Diffuse Lung Dis. 1996;13(2):129-134. 155. Winter 3rd TC, Keener TS, Mack LA. Sonographic appearance of testicular sarcoid. J Ultrasound Med. 1995;14(2):153-156. 156. Eraso CE, Vrachliotis TG, Cunningham JJ. Sonographic findings in testicular sarcoidosis simulating malignant nodule. J Clin Ultrasound. 1999;27(2): 81-83. 157. Mueller DL, Amundson GM, Rubin SZ, Wesenberg RL. Acute scrotal abnormalities in children: diagnosis by combined sonography and scintigraphy. AJR Am J Roentgenol. 1988;150(3):643-646.

158. Watanabe Y, Dohke M, Ohkubo K, et al. Scrotal disorders: evaluation of testicular enhancement patterns at dynamic contrast-enhanced subtraction MR imaging. Radiology. 2000;217(1):219-227. 159. Hricak H, Lue T, Filly RA, et al. Experimental study of the sonographic diagnosis of testicular torsion. J Ultrasound Med. 1983;2(8):349-356. 160. Pillai SB, Besner GE. Pediatric testicular problems. Pediatr Clin North Am. 1998;45(4):813-830. 161. Prando D. Torsion of the spermatic cord: sonographic diagnosis. Ultrasound Q. 2002;18(1):41-57. 162. Lerner RM, Mevorach RA, Hulbert WC, Rabinowitz R. Color Doppler US in the evaluation of acute scrotal disease. Radiology. 1990;176(2): 355-358. 163. Horstman WG, Middleton WD, Melson GL, Siegel BA. Color Doppler US of the scrotum. Radiographics. 1991;11(6):941-957. 164. Middleton WD, Siegel BA, Melson GL, et al. Acute scrotal disorders: prospective comparison of color Doppler US and testicular scintigraphy. Radiology. 1990;177(1):177-181. 165. Sidhu PS. Clinical and imaging features of testicular torsion: role of ultrasound. Clin Radiol. 1999;54(6):343-352. 166. Middleton WD, Middleton MA, Dierks M, et al. Sonographic prediction of viability in testicular torsion: preliminary observations. J Ultrasound Med. 1997;16(1):23-27. 167. Middleton WD, Melson GL. Testicular ischemia: color Doppler sonographic findings in five patients. AJR Am J Roentgenol. 1989;152(6): 1237-1239. 168. Chinn DH, Miller EI. Generalized testicular hyperechogenicity in acute testicular torsion. J Ultrasound Med. 1985;4(9):495-496. 169. Winter TC. Ultrasonography of the scrotum. App Radiol. 2002;31:3. 170. Vijayaraghavan SB. Sonographic differential diagnosis of acute scrotum: real-time whirlpool sign, a key sign of torsion. J Ultrasound Med. 2006;25(5): 563-574. 171. Trambert MA, Mattrey RF, Levine D, Berthoty DP. Subacute scrotal pain: evaluation of torsion versus epididymitis with MR imaging. Radiology. 1990;175(1):53-56. 172. Vick CW, Bird K, Rosenfield AT, et al. Extratesticular hemorrhage associated with torsion of the spermatic cord: sonographic demonstration. Radiology. 1986;158(2):401-404. 173. Barth RA, Shortliffe LD. Normal pediatric testis: comparison of power Doppler and color Doppler US in the detection of blood flow. Radiology. 1997;204(2):389-393. 174. Bader TR, Kammerhuber F, Herneth AM. Testicular blood flow in boys as assessed at color Doppler and power Doppler sonography. Radiology. 1997;202(2):559-564. 175. Coley BD, Frush DP, Babcock DS, et al. Acute testicular torsion: comparison of unenhanced and contrast-enhanced power Doppler US, color Doppler US, and radionuclide imaging. Radiology. 1996;199(2):441-446. 176. Luker GD, Siegel MJ. Scrotal US in pediatric patients: comparison of power and standard color Doppler US. Radiology. 1996;198(2): 381-385. 177. Albrecht T, Lotzof K, Hussain HK, et al. Power Doppler US of the normal prepubertal testis: does it live up to its promises? Radiology. 1997;203(1): 227-231. 178. Lee Jr FT, Winter DB, Madsen FA, et al. Conventional color Doppler velocity sonography versus color Doppler energy sonography for the diagnosis of acute experimental torsion of the spermatic cord. AJR Am J Roentgenol. 1996;167(3):785-790. 179. Fitzgerald SW, Erickson S, DeWire DM, et al. Color Doppler sonography in the evaluation of the adult acute scrotum. J Ultrasound Med. 1992;11(10): 543-548. 180. Burks DD, Markey BJ, Burkhard TK, et al. Suspected testicular torsion and ischemia: evaluation with color Doppler sonography. Radiology. 1990;175(3):815-821. 181. Hedayati V, Sellars ME, Sharma DM, Sidhu PS. Contrast-enhanced ultrasound in testicular trauma: role in directing exploration, debridement and organ salvage. Br J Radiol. 2012;85(1011):e65-e68. 182. Atkinson Jr GO, Patrick LE, Ball Jr TI, et al. The normal and abnormal scrotum in children: evaluation with color Doppler sonography. AJR Am J Roentgenol. 1992;158(3):613-617.

CHAPTER 22  The Scrotum 183. Bude RO, Kennelly MJ, Adler RS, Rubin JM. Nonpulsatile arterial waveforms: observations during graded testicular torsion in rats. Acad Radiol. 1995;2(10):879-882. 184. Dogra VS, Rubens DJ, Gottlieb RH, Bhatt S. Torsion and beyond: new twists in spectral Doppler evaluation of the scrotum. J Ultrasound Med. 2004;23(8):1077-1085. 185. Sanelli PC, Burke BJ, Lee L. Color and spectral Doppler sonography of partial torsion of the spermatic cord. AJR Am J Roentgenol. 1999;172(1): 49-51. 186. Alcantara AL, Sethi Y. Imaging of testicular torsion and epididymitis/orchitis: diagnosis and pitfalls. Emerg Radiol. 1998;5:394-402. 187. Dresner ML. Torsed appendage. Diagnosis and management: blue dot sign. Urology. 1973;1(1):63-66. 188. Hesser U, Rosenborg M, Gierup J, et al. Gray-scale sonography in torsion of the testicular appendages. Pediatr Radiol. 1993;23(7):529-532. 189. Basekim CC, Kizilkaya E, Pekkafali Z, et al. Mumps epididymo-orchitis: sonography and color Doppler sonographic findings. Abdom Imaging. 2000;25(3):322-325. 190. Gondos B, Wong TW. Non-neoplastic diseases of the testis and epididymis. In: Murphy WM, editor. Urological pathology. 2nd ed. Philadelphia: Saunders; 1997. p. 277-341. 191. Horstman WG, Middleton WD, Melson GL. Scrotal inflammatory disease: color Doppler US findings. Radiology. 1991;179(1):55-59. 192. Cook JL, Dewbury K. The changes seen on high-resolution ultrasound in orchitis. Clin Radiol. 2000;55(1):13-18. 193. Hourihane DO. Infected infarcts of the testis: a study of 18 cases preceded by pyogenic epididymoorchitis. J Clin Pathol. 1970;23(8):668-675. 194. Sanders LM, Haber S, Dembner A, Aquino A. Significance of reversal of diastolic flow in the acute scrotum. J Ultrasound Med. 1994;13(2): 137-139. 195. Casalino DD, Kim R. Clinical importance of a unilateral striated pattern seen on sonography of the testicle. AJR Am J Roentgenol. 2002;178(4): 927-930. 196. Harris RD, Chouteau C, Partrick M, Schned A. Prevalence and significance of heterogeneous testes revealed on sonography: ex vivo sonographicpathologic correlation. AJR Am J Roentgenol. 2000;175(2):347-352.

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197. Eke N. Fournier’s gangrene: a review of 1726 cases. Br J Surg. 2000;87(6): 718-728. 198. Jeffrey RB, Laing FC, Hricak H, McAninch JW. Sonography of testicular trauma. AJR Am J Roentgenol. 1983;141(5):993-995. 199. Kim SH, Park S, Choi SH, et al. Significant predictors for determination of testicular rupture on sonography: a prospective study. J Ultrasound Med. 2007;26(12):1649-1655. 200. Buckley JC, McAninch JW. Use of ultrasonography for the diagnosis of testicular injuries in blunt scrotal trauma. J Urol. 2006;175(1):175-178. 201. Cohen HL, Shapiro ML, Haller JO, Glassberg K. Sonography of intrascrotal hematomas simulating testicular rupture in adolescents. Pediatr Radiol. 1992;22(4):296-297. 202. Cass AS, Ferrara L, Wolpert J, Lee J. Bilateral testicular injury from external trauma. J Urol. 1988;140(6):1435-1436. 203. Learch TJ, Hansch LP, Ralls PW. Sonography in patients with gunshot wounds of the scrotum: imaging findings and their value. AJR Am J Roentgenol. 1995;165(4):879-883. 204. Gordon LM, Stein SM, Ralls PW. Traumatic epididymitis: evaluation with color Doppler sonography. AJR Am J Roentgenol. 1996;166(6): 1323-1325. 205. Elder JS. Cryptorchidism: isolated and associated with other genitourinary defects. Pediatr Clin North Am. 1987;34(4):1033-1053. 206. Harrison JH, Gittes RF, Stamey TA, et al. Campbell’s urology. 4th ed. Philadelphia: Saunders; 1979. 207. Rosenfield AT, Blair DN, McCarthy S, et al. Society of Uroradiology Award paper. The pars infravaginalis gubernaculi: importance in the identification of the undescended testis. AJR Am J Roentgenol. 1989;153(4):775-778. 208. Friedland GW, Chang P. The role of imaging in the management of the impalpable undescended testis. AJR Am J Roentgenol. 1988;151(6): 1107-1111. 209. Fritzsche PJ, Hricak H, Kogan BA, et al. Undescended testis: value of MR imaging. Radiology. 1987;164(1):169-173. 210. Kier R, McCarthy S, Rosenfield AT, et al. Nonpalpable testes in young boys: evaluation with MR imaging. Radiology. 1988;169(2):429-433.

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Overview of Musculoskeletal Ultrasound Techniques and Applications Colm McMahon and Corrie Yablon

SUMMARY OF KEY POINTS • A wide variety of inflammatory, degenerative, traumatic, and neoplastic conditions can be imaged accurately and cost-effectively with ultrasound. • Understanding optimal imaging techniques and recognizing and avoiding common artifacts is essential to musculoskeletal ultrasound.

• Ultrasound can provide higher-resolution imaging of nerves and tendons compared with standard clinical magnetic resonance imaging examinations. • Dynamic imaging may be performed with ultrasound, which can assist in the diagnosis of tendon and ligamentous injury.

CHAPTER OUTLINE GENERAL CONSIDERATIONS Doppler Imaging Elastography Extended Field of View Imaging MUSCLES

TENDONS LIGAMENTS NERVES JOINT ASSESSMENT SOFT TISSUE MASSES

GENERAL CONSIDERATIONS Ultrasound is becoming a central part of the diagnostic pathway for patients with musculoskeletal complaints. In many cases, ultrasound is performed as an alternative or complement to magnetic resonance imaging (MRI). Ultrasound has several advantages over MRI that have been described in the literature, succinctly by Nazarian in a 2008 perspective article.1 Ultrasound is well tolerated by patients and can be performed in those with contraindications to MRI, such as implanted cardiac devices or other MRI-incompatible implants, large size, or claustrophobia. Ultrasound examinations often take less time to perform than the corresponding MRI examinations. Ultrasound provides higher-resolution imaging of tendons and ligaments than routine musculoskeletal MRI. Ultrasound also provides the ability to image dynamically, which can be important in the diagnosis of disorders of impingement and subluxation of nerves or tendons. It is excellent at determining the fundamental tissue characterization of solid versus cystic in the setting of a mass lesion—this type of characterization may otherwise require the administration of intravenous contrast when MRI is used to distinguish a T2-hyperintense solid mass from a simple cyst.

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In many cases, patients can be given results at the time of their examination. As a general rule, a systematic approach to musculoskeletal ultrasound examination of the joints using defined protocols is preferred to a focal examination when time permits. Focused imaging of symptomatic areas of concern adds additional diagnostic information to the routine protocol.2 When evaluating a foreign body or palpable soft tissue mass, focal assessment can be performed, with attention to the relationship to nearby anatomic structures, critical to treatment planning. As with MRI interpretation, it is imperative that the radiologist have a clear understanding of musculoskeletal anatomy before performing or interpreting a sonographic examination, especially when previous studies are not available for comparison. High-frequency linear ultrasound probes (12-15 MHz) are recommended for musculoskeletal imaging. Higher-frequency probes (15-17 MHz) can be helpful for evaluating superficial anatomy, for example, ligaments and tendons in the fingers. Hockey stick–style high-frequency probes can be very useful for evaluation of fine structures, providing focused small field of view images and permitting good skin contact in the peripheral extremities. Lower-frequency (3-9 MHz) linear probes may be

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FIG. 23.1  Effect of Examination Technique on Power Doppler Findings.  (A) Longitudinal sonogram obtained without pressure exerted on the tendon shows hypervascularity. (B) Longitudinal sonogram obtained with the usual pressure on the transducer shows the near complete disappearance of hypervascularity. P, Patella.

needed for greater tissue penetration in deeper structure evaluation or when attempting to determine the relationships of a deep pathologic process to the underlying bone and muscle. Although lower-frequency probes provide deeper penetration of soft tissues, there is a corresponding trade-off of lower resolution. In some cases, a low-frequency curvilinear probe may be necessary (2-5 MHz), for example, in the evaluation of the thigh and hip region or the examination of deep thigh or gluteal masses. By using more than one probe, the user may obtain complementary information about a single disease process. As is the case for all ultrasound imaging, careful attention to image optimization, such as positioning the focal zone at the appropriate depth, is important. Adequate ultrasound wave transduction is facilitated by good skin contact with the transducer and the use of ultrasound gel. A standoff pad can help for imaging very superficial structures.

Doppler Imaging The role of Doppler imaging in musculoskeletal ultrasound includes characterization of neoplastic, inflammatory, and degenerative conditions.3 Doppler ultrasound is helpful in confirming vascularization of solid masses in distinction from avascular cystic lesions. It is also helpful in characterization of inflammatory conditions, including synovitis, tenosynovitis, myositis, and soft tissue infection. Finally, tendon neovascularization is a sign occasionally seen with the development of degenerative tendinosis. As in other areas of the body, setting the appropriate Doppler gain is important, and imaging with a small sample volume will minimize motion artifacts. Because many structures of interest in musculoskeletal imaging are superficial, care should be taken to avoid excessive probe pressure during imaging, because this can limit flow detection in areas of vascularization (Fig. 23.1).

Elastography An exciting recent development is imaging and quantification of tissue elasticity. This is defined by the tissue deformability and can be measured as a Young modulus for a given tissue expressed in kilopascals (kPa).4 The range of Young modulus

for musculoskeletal tissue ranges from 1 to 10 kPa. Depending on available hardware, ultrasound elastography may be performed using strain elastography or shear-wave elastography. In the musculoskeletal system, early application of elastography has shown substantial promise in the evaluation of tendinosis. In tendinosis, collagen disorganization and mucoid and lipoid degeneration result in tendon softening, which can be visualized and quantified with sonoelastography.5 Other emerging applications include diagnosis of muscle disorders such as myositis6 and characterization of soft tissue masses.7

Extended Field of View Imaging Although high-resolution linear array probes are optimal for imaging relatively superficial musculoskeletal structures with fine anatomic detail, the overall field of view during imaging is limited. This may cause difficulty when viewing the images after acquisition, because the scale and anatomic position and orientation, which are intuitive when scanning real time, may be difficult to convey in the retained static images. This can be overcome by use of cine-clips and also with use of extended field of view (panorama) imaging. With this technique, an image is acquired while the probe is moved in the direction of the probe footprint long axis. The image acquired is a composite panoramic image of the anatomy scanned during the motion path of the probe. The scanners equipped with this technology recognize the degree of probe motion by the degree of frame shift during the movement of the probe. By utilizing knowledge of this motion vector, a blended image of successively acquired image frames during the probe sweep can be formed.8 This technique can be extremely helpful in putting a specific finding in overall anatomic context, measuring a lesion that is larger than the probe field of view, and can also provide some diagnostic benefit—for example, in comparing the echogenicity and bulk of muscles of the rotator cuff.9

MUSCLES Normal muscle is composed of multiple fascicles each embedded in perimysium, a thin layer of connective tissue and fat.10 The

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FIG. 23.2  Normal Muscle.  (A) In short-axis view a normal vastus lateralis (VL) muscle demonstrates a speckled or “starry sky” appearance (arrows). (B) In long-axis view the normal muscle demonstrates a pennate appearance (arrows). F, Femur; VI, vastus intermedius.

ultrasound pattern of muscle is typically feathery, or pennate, with fiber orientation usually directed along the long axis of the muscle. In the short-axis view, the muscle fibers demonstrate a speckled appearance (Fig. 23.2). Fibers typically converge to the myotendinous junction and the muscle tapers in diameter at this point (Videos 23.1 and 23.2). A thin layer of fascia surrounds the muscle unit, separating it from adjacent muscles and subcutaneous fat. Muscle is usually overall hypoechoic, with more echogenic internal linear interfaces generated by the perimysium. Muscle injuries of different grades can be identified with ultrasound.11 A grade I injury is a minor strain and is depicted on ultrasound as just minimal fiber elongation and hypoechogenicity, but without detectible discontinuity. Ultrasound is less sensitive than MRI to these minor grades of injury, which are usually treated conservatively.12 A grade II injury is a partial tear. Fiber discontinuity is seen, with a focal anechoic or hypoechoic gap, usually filled by more echogenic hematoma. Gentle probe pressure can demonstrate muscle fibers floating freely within fluid and hematoma, referred to as the “bell-clapper” sign. At the most severe end of the spectrum of muscle injury is a grade III injury, or complete tear (Fig. 23.3). In the case of a grade III injury, the muscle is completely interrupted with retraction of the muscle ends and an interposed gap, which should be measured. A large hematoma is expected in association with a complete tear. A distinct form of muscle injury that deserves special mention is the avulsion of a muscle from its aponeurosis, a pattern of injury particularly common in the calf in the clinical spectrum of “tennis leg” (Fig. 23.4). In this injury the medial gastrocnemius muscle tears away from the aponeurosis with the underlying soleus muscle. Fluid and hematoma may dissect along the aponeurotic plane and there may be some retraction of the medial gastrocnemius. This usually occurs during forceful plantar flexion

FIG. 23.3  Muscle Tear.  Long-axis image of the medial groin region demonstrates hypoechoic fluid (arrows) at the pubic symphysis (P) origin of the adductor muscles, consistent with a grade III muscle tear.

during sports, for example, in a forceful lunge in tennis. This injury may be accompanied by a plantaris tendon tear. Symptomatic myofascial defects lend themselves well to ultrasound evaluation. In this injury a defect in the muscular fascia allows herniation of muscle fibers, leading to a palpable and often painful mass (Fig. 23.5). In some cases, the patient may have associated neuropathy resulting from compression of adjacent nerves.13 The mass may be more apparent to the patient during certain movements and activities that lead to muscle contraction, and these can be reproduced during scanning to assist in diagnosis. On ultrasound imaging, focused evaluation of the region of concern reveals focal bulging of muscle fibers through the otherwise smooth fascia. If this is equivocal or the patient reports symptoms only in certain positions such as

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FIG. 23.4  Medial Head Gastrocnemius Tear From the Aponeurosis.  (A) Long-axis image shows blunting and retraction of the medial head gastrocnemius fibers (arrows) from the aponeurosis (*) with an associated hematoma (arrowheads). (B) Short-axis image shows effacement of the normal gastrocnemius muscle (G) architecture and a hematoma of mixed echogenicity at the site of the tear from the aponeurosis (arrowheads). S, Soleus muscle.

FIG. 23.5  Forearm Muscle Herniation.  At the site of the palpable abnormality, there is focal herniation of a portion of the pronator teres muscle (PT) (arrows) through the muscle fascia (arrowheads). This patient noticed a forearm bulge while weightlifting. U, Ulna.

standing, the area should be scanned with the patient reproducing the relevant position where possible. Muscle atrophy can occur in response to denervation or chronic injury, for example, in the setting of a chronic complete rotator cuff tear. Muscle atrophy is characterized on ultrasound as a decrease in muscle bulk and a relative increase in echogenicity, reflecting replacement of muscle fibers with fatty tissue (Fig. 23.6). Comparison with adjacent muscles or the contralateral side can assist in subtle cases. As a result of increased echogenicity, the visibility of the central tendon at the myotendinous junction is diminished, and there is a loss of normal pennate pattern.14

TENDONS Imaging the musculoskeletal system with ultrasound has built on early success in evaluation of tendons, with initial reports of Achilles tendon assessment.15 Many tendons are ideally suited

to ultrasound evaluation, as they are superficial and require the high-resolution imaging that ultrasound affords. Normal tendons are composed of longitudinally oriented bundles of collagen fibers, which give a highly organized echogenic linear fibrillar or striated pattern on ultrasound when viewed in long axis (Fig. 23.7). In short-axis view, normal tendons are usually smooth and ovoid in outline, with a homogenous stippled appearance, representing the tendon fibers viewed en face. Some tendons, such as the flexor and extensor tendons of the hand and wrist, are invested in a synovial lined sheath, whereas others, such as the Achilles tendon, are enveloped in a layer of loose areolar tissue called a paratenon. It is critically important to understand the concept of aniso­ tropy when performing the sonographic evaluation of tendons (Fig. 23.8). Collagen bundles, because of their smooth parallel organization within tendons, act as specular reflectors, such that sound waves are reflected in a single direction. When these specular reflectors are imaged with ultrasound, if the angle of insonation is not perpendicular to the tendon fibers, sound waves will be reflected away from the transducer, leading to the generation of an image with artifactual hypoechogenicity within the tendon.16 This can be resolved by correcting the angle of insonation to 90 degrees when an area of hypoechogenicity is observed. The finding of focal persistent abnormal hypoechogenicity in a second plane with optimized imaging adds further corroboration to the observation of an apparent pathologic hypoechoic region. Tendon injuries are usually caused by overuse and range from tendinosis to complete tear. The term tendinosis refers to intratendinous degeneration without tearing. Histologically, tendinosis consists of tendon expansion and loss of clear demarcation of collagen bundles, with increased mucoid ground substance among collagen bundles.17 There is noninflammatory fibroblastic and myofibroblastic cellular proliferation. On ultrasound, tendinosis appears as an area of hypoechogenicity, without discontinuity, frequently associated with varying degrees of tendon thickening (Fig. 23.9). Dystrophic calcification, and even ossification, can be seen within affected tendons. An additional characteristic feature is the development of neovascularization,

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FIG. 23.6  Muscle Atrophy.  Patient with a remote history of quadriceps injury presented with noticeable volume loss in his right anterior thigh. (A) Ultrasound of the abnormal right side shows marked volume loss in the rectus femoris muscle (arrows) with echogenic fatty infiltration of the remaining muscle. (B) The normal left side demonstrates normal muscle bulk and echotexture (arrows).

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FIG. 23.7  Normal Quadriceps Tendon.  (A) In long-axis view, the normal tendon demonstrates a fibrillar appearance (arrows). (B) In short-axis view, the tendon is ovoid and echogenic with a speckled appearance (arrows). P, Patella.

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FIG. 23.8  Anisotropy.  (A) In this long-axis scan of the Achilles insertion on the calcaneus, the proximal portion of the imaged tendon demonstrates a normal fibrillar appearance (arrow), whereas the distal tendon insertion is hypoechoic (arrowhead). (B) When the transducer is angled 90 degrees to the distal tendon insertion, the tendon then becomes fibrillar and is normal in appearance (arrowhead). C, Calcaneus.

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which can be visualized on Doppler ultrasound in tendinosis but not in normal tendons.18 Tendinosis is common in the Achilles tendon, where it most commonly affects the midportion of the tendon, or “watershed,” where there is overlapping blood supply. Tendon degeneration can also occur at the bone-tendon interface or enthesis, seen in the Achilles as insertional tendinosis at the calcaneus. Tendinosis at the tendon-bone interface is the most common pattern of degeneration seen in the common flexor and extensor origins at the medial and lateral humeral epicondyles at the elbow, forming part of the clinical spectrum of epicondylitis. Similar to tendinosis elsewhere, insertional tendinosis or enthesopathy is characterized by tendon expansion and hypoechogenicity.19,20 Enthesitis, or inflammation at the enthesis, can occur in patients with rheumatoid arthritis, psoriatic arthritis, or spondyloarthropathy. The imaging features of enthesitis can overlap with tendinosis, with tendon expansion and hypoechogenicity, but neovascularization may be a more prominent feature and bony erosion may also be present.21,22 Patients with tendinosis are more prone to tendon tears. Tendon tears may be partial or complete. Partial tears may be transversely oriented (parallel to the short axis of the tendon) or longitudinally oriented (parallel to the long axis of the tendon, also referred to as a “longitudinal split tear”). Tears are manifested by anechoic or hypoechoic clefts, with focal tendon fiber

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FIG. 23.9  Tendinosis.  (A) The long-axis image of the mid Achilles tendon demonstrates fusiform, hypoechoic swelling of the tendon (arrowheads), although the fibrillar architecture can still be discerned. (B) In short-axis view, the Achilles appears thickened and is ovoid in morphology (arrowheads). (C) In a different patient, the Achilles tendon at the insertion on the calcaneus is thickened and hypoechoic with loss of the normal fibrillar pattern (arrows). There is marked hyperemia on color Doppler imaging. Note the dorsal calcaneal enthesophytes (arrowheads). C, Calcaneus.

discontinuity23 (Fig. 23.10). When a complete rupture occurs, the tendon fibers are entirely discontinuous and some degree of tendon retraction may occur because of now-unopposed muscle contraction (Fig. 23.11). The extent of retraction is of importance for surgical planning and thus should be measured. In an acute tear, there may be complex fluid and hematoma within and about the tear site. When evaluating flexor and extensor tendons at the hand and wrist, passive and active motion can facilitate accurate identification of the tendon of interest and can provide mechanical correlation for the integrity of a tendon (Video 23.3).

Sonographic Signs of Tendon Tears Discontinuity of fibers (partial or complete) with hypoechoic or anechoic gap Focal thinning of the tendon Hematoma (usually small) Bone fragment (in cases of avulsion) Nonvisualization of retracted tendon (in complete tear)

In tendons with surrounding tendon sheaths, inflammation of the tendon sheath (tenosynovitis) may occur as an overuse phenomenon or as a result of an inflammatory condition, such as rheumatoid arthritis. Tenosynovitis is manifest on ultrasound

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FIG. 23.10  Partial Tear of the Distal Achilles Tendon.  (A) There is focal anechoic clefting of the anterior fibers of the Achilles distal insertion (arrows) although the posterior fibers remain intact. (B) Color Doppler imaging in the same patient demonstrates marked hyperemia in the injured tendon.

FIG. 23.11  Achilles Tendon Rupture.  A panoramic view of the Achilles tendon demonstrates a rupture within the midportion of the tendon. The proximal aspect of the tendon is chronically thickened and hypoechoic (arrows). Refraction artifact (arrowheads) is caused by the interfaces between the ruptured tendon edges and hemorrhage. C, Calcaneus.

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FIG. 23.12  Tenosynovitis.  In this patient with rheumatoid arthritis and ankle pain, the peroneus brevis tendon (*) in long-axis (A) and short-axis (B) views is thickened and heterogeneous. The tendon sheath contains a large amount of echogenic synovium (arrows), hypoechoic fluid, and hyperemia on color Doppler imaging.

as an increase of fluid volume around a tendon within its sheath (Fig. 23.12). The tendon sheath itself can thicken and demonstrate hypervascularity on Doppler evaluation.24 In patients with imaging findings of tenosynovitis and a history of penetrating injury or foreign body, septic tenosynovitis should be considered.25

LIGAMENTS Ultrasound is an excellent technique for the evaluation of liga­ mentous injuries, with some advantages over MRI in this regard. Ultrasound permits high-resolution imaging of small ligaments

CHAPTER 23  Overview of Musculoskeletal Ultrasound Techniques and Applications in planes that can be individualized to the structure of interest in any given patient, overcoming some intrinsic difficulties that can be encountered with scan plane prescription for MRI. In addition to static imaging, dynamic assessment may provide additional diagnostic information. Normal ligaments consist of interweaved bundles of collagen, extending between bones, usually restricting joint movements to prevent pathologic motion.26 Ligament injury leads to pain and instability. Normal ligaments are linear bandlike structures and appear hyperechoic and fibrillar27 (Fig. 23.13). Low-grade injuries consist of mild sprains, which typically have a good prognosis with conservative care. Mild sprains are characterized on ultrasound by swelling, hypoechogenicity, and some loss of fibrillar pattern (Fig. 23.14). Tears can be partial or complete. In the case of complete tears, there may be retraction of the torn ligament components from each other, a finding that can be exaggerated by dynamic imaging with stress maneuvers (Figs. 23.15 and 23.16). The use of stress maneuvers is somewhat controversial, however, because of concerns that a partial tear may be exacerbated or even converted to a complete tear by additional stress.28,29

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FIG. 23.13  Normal Anterior Talofibular Ligament.  Note that the ligament (arrows) demonstrates a fibrillar appearance and that the fibers are more densely packed than those seen in a normal tendon. F, Fibula, T, talus.

FIG. 23.14  Ligament Sprain.  The anterior talofibular ligament (arrows) is diffusely thickened and hypoechoic, with intact fibers, consistent with sprain. Note the cortical irregularity at the lateral fibula (*) consistent with prior avulsion. F, Fibula, T, talus.

FIG. 23.15  Chronic Ligament Rupture.  In this patient with a history of multiple ankle sprains, the anterior talofibular ligament is absent and the joint is widened on dynamic stress maneuver. Hypoechoic fluid (*) appears in the lateral recess. F, Fibula, T, talus.

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FIG. 23.16  Elbow Joint Widening on Dynamic Valgus Stress.  (A) The medial joint is 2 mm (calipers) wide at rest in this patient with an ulnar collateral ligament (UCL) tear. Note the UCL is markedly thickened at the proximal humeral attachment and a hypoechoic cleft is present within the ligament consistent with a tear (arrows). (B) With valgus stress, the medial joint space widens to 4 mm, confirming the presence of a UCL tear. The overlying common extensor tendon (*) is intact. ME, Medial epicondyle of the humerus; U, ulna.

FIG. 23.17  Stener Lesion.  The ulnar collateral ligament (arrows) of the thumb is torn and the stump is retracted proximal to the metacarpophalangeal joint and to the adductor aponeurosis (arrowheads), which is thickened and hypoechoic. MC, Metacarpal; P, proximal phalanx.

Ultrasound has been effectively utilized to diagnose injury of ligaments at the hand and wrist, notably the ulnar collateral ligament of the thumb metacarpophalangeal joint28-30 in addition to the scapholunate ligament.31 Other ligaments, such as the anterior oblique ligament of the thumb, have been identified with ultrasound, but the role of ultrasound in diagnosis has yet to be defined.32,33 Ultrasound may also be used to evaluate the collateral ligaments of the elbow,34-39 ankle ligaments,40 and collateral ligaments of the knee.41 When evaluating ligamentous injury, it is important to assess nearby structures such as tendons, which may also have been injured (e.g., common flexor tendon origin injury in the setting of ulnar collateral ligament injury at the elbow) or which may be relevant to the ligamentous injury, as in the case of a Stener lesion. A Stener lesion occurs when a thumb metacarpal phalangeal ulnar collateral ligament tear entraps the adductor aponeurosis such that the ligament lies superficial to the aponeurosis (Fig. 23.17). This injury is important to recognize, as the treatment

is surgical. The appearance of a Stener lesion on ultrasound is of retracted hypoechoic ligament fibers displaced over the linear aponeurosis, giving rise to the “yo-yo on a string” appearance.28

NERVES Normal peripheral nerves are well visualized with high-resolution ultrasound. Nerves have a characteristic honeycomb morphology on ultrasound when imaged in short axis42 (Fig. 23.18). Nerves are tubular structures, and on longitudinal axis, they demonstrate an internal striated pattern, somewhat similar to tendons but with a coarser pattern referred to as a “fascicular pattern.”43,44 This pattern consists of alternating internal hypoechoic and hyperechoic linear components. The hypoechoic components represent fascicles or groups of fascicles, whereas the hyperechoic parts correspond with the epineurium.44 The epineurium consists of connective tissue that surrounds nerve fascicles, composed

CHAPTER 23  Overview of Musculoskeletal Ultrasound Techniques and Applications

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of collagenous and adipose components, with small blood vessels and lymphatics. On short-axis view, peripheral nerves appear ovoid or round and have punctate internal hypoechoic fat representing nerve fascicles within the echogenic epineurium. Dynamic maneuvers including flexion and extension of the imaged region should show no substantial motion of a peripheral nerve, as distinct from tendons. Assessment of peripheral nerves using ultrasound is performed primarily in the short-axis plane. The nerve is evaluated at a known anatomic location and followed proximally and distally as needed. Anisotropy is less problematic for peripheral nerves than for tendons.23 Longitudinal scanning is helpful for providing an overview and illustrating relative caliber changes of peripheral nerves detected on transverse imaging. Caution should be exercised in primary interpretation of longitudinal sonographic images of peripheral nerves because of the potential to scan in a plane, which is not parallel to the nerve with potential artifactual changes in caliber and echogenicity. Nerve dysfunction can result from compression by masses arising from or adjacent to the nerve, entrapment within fibroosseous tunnels (such as the carpal tunnel in the case of median nerve compression at the wrist), or subluxation from fibro-osseous tunnels. Masses include neurogenic tumors, neurofibromas and schwannomas, considered more fully later. Soft tissue ganglia, usually appearing anechoic on ultrasound, may also cause nerve compression.45-47 In the setting of nerve compression by any cause, the findings detectible on ultrasound relate to echotextural and caliber changes. Local compression causes venous congestion, which can lead to intraneural edema. Chronic compression can ultimately lead to intraneural fibrosis. These alterations in

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FIG. 23.18  Normal Median Nerve.  (A) In long axis, the nerve demonstrates a fascicular appearance (arrows), although coarser than a tendon. The hypoechoic fascicles are distinguishable from the intervening echogenic epineurium. (B) In short axis, in the forearm, the median nerve shows a honeycomb appearance (arrows). (C) In short axis, at the level of the carpal tunnel, the echogenic tendons (arrows) are seen adjacent to the median nerve (arrowheads).

intraneural composition lead to loss of normal hyperechogenicity of the interfascicular epineural tissue, causing an overall hypoechoic appearance of the nerve in addition to poor definition or disappearance of the normal fascicular pattern.43 One of the most common clinical forms of entrapment neuropathy is carpal tunnel syndrome. In this condition, compression and flattening of the nerve occurs within the carpal tunnel, at the palmar aspect of the wrist, and the nerve is typically swollen and expanded just proximal to the carpal tunnel. The sonographic diagnosis of carpal tunnel syndrome is made by measuring the cross-sectional area of the median nerve at the level of the pronator quadratus and comparing this to the crosssectional area of the median nerve in the carpal tunnel at the level of the pisiform. A difference of more than 2 mm2 between the two measurements is highly associated with carpal tunnel syndrome48 (Fig. 23.19). Variable cut-off values for the diagnosis of carpal tunnel syndrome based on single cross-sectional measurements of the median nerve in the carpal tunnel have been reported in the literature, in the 9- to 11-mm2 range.49-51 Bowing and thickening of the overlying flexor retinaculum can also be observed.51 Symptoms may also arise from dynamic nerve subluxation from fibro-osseous tunnels. One example of this is at the cubital tunnel, at the medial posterior aspect of the elbow. The ulnar nerve normally passes through this fibro-osseous tunnel at the posterior aspect of the humerus and is stabilized by an overlying retinaculum. This retinaculum normally passes between the olecranon and the medial epicondyle of the humerus. Developmental or posttraumatic deficiency of this retinaculum can allow the ulnar nerve to dynamically subluxate out of the cubital tunnel

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FIG. 23.19  Carpal Tunnel Entrapment of the Median Nerve.  (A) Short-axis cross-sectional area of the median nerve obtained at the level of the pronator quadratus (PQ) at the distal forearm. (B) Cross-sectional area obtained in the carpal tunnel at the level of the pisiform (P). The 4-mm2 difference in area between the two images is consistent with carpal tunnel syndrome.

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FIG. 23.20  Ulnar Nerve Dislocation at the Elbow.  (A) At rest, with the elbow extended and the probe positioned between the medial epicondyle (M) and the ulnar olecranon (O), the ulnar nerve (circled) is positioned posterior to the epicondyle. Note the ulnar nerve is enlarged at this location. (B) On flexion the ulnar nerve (circled) dislocates anterior to the medial epicondyle along with the medial head (MT) of the triceps muscle (known as “snapping triceps” syndrome). Most patients with ulnar dislocation do not exhibit medial head triceps dislocation. See also Video 23.4.

during elbow flexion, and this subluxation can be captured on dynamic imaging (Video 23.4). Scan technique is important in this diagnosis. The probe should be positioned in a transverse plane with respect to the medial posterior elbow. The nerve should normally be visible within the cubital tunnel with the elbow in an extended position. The osseous landmark of the medial epicondyle should be maintained in the visualized field as the patient slowly flexes the elbow. Excessive probe pressure should be avoided because this can limit dynamic motion of the nerve. The nerve should normally remain lateral to the medial epicondyle. Subluxation, where the nerve moves medially and anteriorly along the epicondyle, or dislocation, where the nerve snaps anteromedial to the medial epicondyle, may occur on flexion52,53 (Fig. 23.20). Patients with ulnar nerve subluxation or dislocation may experience pain or transient numbness, but this dynamic instability can also be seen in asymptomatic in healthy controls, and the association with neuropathy is debated.54,55

JOINT ASSESSMENT Ultrasound can play a helpful role in the diagnosis and follow-up of both inflammatory and noninflammatory arthropathy and may guide diagnostic and therapeutic procedures in patients with these disorders. Patients with inflammatory arthropathy such as rheumatoid arthritis present with joint pain, swelling, and stiffness. Ultrasound plays a complementary role to clinical history, physical examination, radiographs, and serology tests such as acute phase reactants (e.g., C-reactive protein, erythrocyte sedimentation rate, rheumatoid factor, and antinuclear antibody). In this role, when used systematically, ultrasound can substantially increase diagnostic certainty in patients with suspected inflammatory arthropathy.56 Ultrasound also represents a great tool in the follow-up of these patients, allowing detection of subclinical relapse in patients with clinical remission and predicting relapse and joint deterioration.57

CHAPTER 23  Overview of Musculoskeletal Ultrasound Techniques and Applications Joint effusions are frequently present in patients with inflam­ matory arthritis but are nonspecific as they may also occur in patients with osteoarthritis, with infection, and in the setting of trauma or internal derangement (Fig. 23.21). The diagnosis of an effusion rests on the visualization of increased volume of joint fluid. Joint fluid is typically anechoic but can contain some mobile low-level echoes. In addition, joint fluid is mobile and compressible.58 Normal joints contain just a trace of fluid, so an increase in this fluid volume constitutes a joint effusion. Synovitis is determined by the presence of intraarticular nondisplaceable hypoechoic to hyperechoic soft tissue, which usually demonstrates hyperemia on color Doppler assessment (Fig. 23.22). On Doppler assessment, the velocity filter should be set to detect low amounts of flow, and the gain settings should

be adjusted to just below a level where noise is visualized.59 Either color Doppler or power Doppler may be more sensitive to flow in the evaluation of synovitis, depending on individual machine, so familiarity with the hardware being used is important.60 The quantity of synovial hyperemia can be graded as described by Szkudlarek et al.61: Grade I (low) hyperemia consists of the visualization of several single vessel dots. Grade II (moderate) hyperemia is shown when there are confluent vessel signals occupying less than half of the visualized synovial tissue. Grade III (high) represents confluent vessel signals in more than half of the synovium. Doppler ultrasound has shown high degrees of sensitivity and specificity in the diagnosis of synovitis at the metacarpophalangeal joints in patients with rheumatoid arthritis when compared with dynamic contrast-enhanced MRI.61 Ultrasound has also been shown to have high interobserver and intraobserver reliability in detection of synovitis.62 Bone erosion in erosive inflammatory arthritis such as rheumatoid arthritis can be depicted on ultrasound as a cortical defect visible in two perpendicular planes63 (Fig. 23.23). Erosions may be graded as small (4 mm).64 Ultrasound is more sensitive than plain radiographs in the detection of bone erosion and thus may aid in diagnosis of early disease.65 In addition to cortical discontinuity, there may be acoustic enhancement of marrow subjacent to the inflammatory bony erosion.65 Patients with inflammatory arthropathy may also have associated tenosynovitis, enthesitis, and, in the case of rheumatoid arthritis, inflammatory periarticular nodules (rheumatoid nodules)66 (Fig. 23.24). Gout is a common inflammatory arthritis with a predilection for first metatarsophalangeal joint involvement, caused by precipitation of uric acid crystals within joints. In patients with gout, there may be joint effusion, synovial hypertrophy and hyperemia, soft tissue swelling, and juxtaarticular erosions that can be large.67 Intraarticular crystals may be evidenced by the presence of a characteristic irregular hyperechoic line along the surface of the normally hypoechoic cartilage, termed the “double contour sign”68 (Fig. 23.25). This is distinct from

FIG. 23.21  Simple Knee Joint Effusion.  Anechoic fluid is present within the suprapatellar recess of the knee (arrows). There is concomitant quadriceps tendinosis (*). F, Distal femur; P, patella.

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FIG. 23.22  Complex Ankle Joint Effusion in Rheumatoid Arthritis.  (A) A long-axis image of the tibiotalar joint demonstrates a complex joint effusion (arrows) with both anechoic fluid and echogenic, thickened synovium consistent with synovitis. (B) Color Doppler imaging of the tibiotalar joint demonstrates marked hyperemia within the echogenic synovium. T, Talus.

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FIG. 23.23  Bone Erosions in Two Different Patients Rheumatoid Arthritis.  (A) Long-axis gray-scale image at the fifth metatarsophalangeal joint demonstrates bone erosion in the fifth metatarsal head (arrow) with associated cortical irregularity and synovial hypertrophy (arrowheads). M, Metatarsal, P, proximal phalanx. (B) Color Doppler imaging of the dorsal wrist in long-axis view demonstrates hyperemia within the synovium and erosion (arrow) of the scaphoid (S). R, Distal radius, T, trapezium.

FIG. 23.24  Achilles Tendon With Rheumatoid Nodules.  Long-axis image of the Achilles tendon demonstrates hypoechoic nodular thickening (*) of the posterior tendon surface, consistent with rheumatoid nodules. No hyperemia was seen on color Doppler imaging (not shown).

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FIG. 23.25  Gout in Two Different Patients.  (A) Long-axis gray-scale image of the first metatarsal phalangeal joint demonstrates the “sugar icing” appearance where echogenic urate crystals are deposited along the synovial lining of the joint (arrowheads). The “double contour sign” is formed by the echogenic urate crystals (“sugar icing”) layering on the anechoic hyaline cartilage with the underlying echogenic cortex (arrows). (B) Long-axis gray-scale image of the fifth metatarsal phalangeal joint shows a large erosion (arrow) with a large amorphous tophus (arrowheads), part of which extends into the erosion. M, First metatarsal, P, first proximal phalanx.

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FIG. 23.26  Osteoarthritis.  Long-axis gray-scale image of the fifth metatarsophalangeal joint demonstrates osteophyte formation (arrows) at both sides of the joint. M, Metatarsal, P, proximal phalanx.

FIG. 23.27  Ganglion Cyst.  Long-axis image of the radiocarpal joint at the radioscaphoid articulation demonstrates a lobulated, hypoechoic ganglion cyst (arrows) arising from the region of the scapholunate ligament. Note the neck (arrowhead) arising from the joint. R, Radius, S, scaphoid.

chondrocalcinosis in which cartilage calcification may be seen with an intracartilaginous echogenic line. Tophi are focal crystal accumulations, which occur around joints in some patients with gout, appearing as clumps of hyperechoic material, which may have a surrounding hypoechoic rim, an appearance has been referred to as “wet sugar clumps.”68 Bony erosions may be seen adjacent to these tophi. In osteoarthritis (nonerosive), cartilage thinning and irregularity may be seen in addition to osteophytes and typically mild synovitis (Fig. 23.26). Osteophytes appear as cortical protrusions at the margin of the articular surface, with posterior acoustic shadowing.69 Synovitis may be nodular or diffuse. Joint effusions may also be demonstrated in osteoarthritis, and although they may occur in the absence of synovitis, the presence and size of effusion correlate with the presence of synovitis and the extent of synovial thickening. Joint effusion and synovitis also correlate with clinical and radiographic disease severity.70

SOFT TISSUE MASSES Palpable soft tissue masses are very common and represent a diagnostic dilemma for physicians. Although the vast majority of these masses are benign, discrimination between benign and malignant masses is not clinically possible. Ultrasound is a complementary modality to MRI in the workup of soft tissue masses. Although MRI has overall higher specificity, several soft tissue masses can be characterized as benign with ultrasound.71,72 In indeterminate cases, contrast-enhanced MRI can be performed, and this two-tiered strategy may provide an overall cost savings to the health care system if appropriately implemented. Ganglion cysts are mucin-filled lesions most often found at the wrist; they are usually closely related to a joint or tendon sheath. Approximately 10% of ganglion cysts occur secondary to trauma.73 The most common location is adjacent to the scapholunate articulation (Fig. 23.27). A neck extending from the lesion to an underlying joint or tendon sheath should be

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FIG. 23.28  Baker Cyst.  (A) Short-axis image from the medial posterior knee shows a lobulated, septated, hypoechoic Baker cyst (arrows) communicating with the joint between the medial gastrocnemius muscle (M) and the semimembranosus tendon (S). F, Posterior medial femoral condyle. (B) In a different patient, long-axis image from the posterior medial knee demonstrates an ovoid, septated complex Baker cyst (arrows) with internal debris, lined with echogenic synovium. See also Video 23.5.

FIG. 23.29  Ruptured Baker Cyst.  Longitudinal sonogram of the calf with extended field of view shows a complex mass (arrows) that is connected to a small amount of fluid in the popliteal fossa (arrowheads), representing the ruptured Baker cyst.

sought but is often not definable.74 These lesions typically appear as well-circumscribed, oval or lobulated anechoic cystic masses, with accompanying through transmission.75 Ganglion cysts may demonstrate low-level internal echoes and may be septated.74 Ganglion cysts are typically noncompressible (as opposed to bursae, which are compressible). Ganglion cysts do not usually demonstrate internal flow on color Doppler evaluation.76 Baker cysts, occurring in the medial aspect of the popliteal fossa, deserve special mention, as they are extremely common. A Baker cyst is caused by fluid distention of the semimembranosusgastrocnemius bursa, occurring between the distal semimembranosus tendon and the medial head of the gastrocnemius muscle with a narrow neck arising from the underlying knee joint (Fig. 23.28, Video 23.5). This usually occurs in the setting of an underlying cause of joint effusion, including osteoarthritis, but also in the setting of posterior horn medial meniscal tear, inflammatory arthritis, and internal derangement. Although common, they are not reliably diagnosed clinically.77 Baker cysts are typically anechoic when uncomplicated, yet may have a variable appearance, with complex fluid and hemorrhage, internal septations and debris, and thick, echogenic, hyperemic synovium lining the cyst. The narrow neck can act as a valve, and fluid

accumulation within the cyst can lead to rupture, resulting in acute pain, swelling, and erythema behind the knee and in the proximal calf.78 When this occurs, the margin of the cyst is often irregular caudally and there may be associated medial calf subcutaneous edema, with fluid tracking distally about the medial head of the gastrocnemius (Fig. 23.29). The clinical presentation of this may mimic deep venous thrombosis or developing cellulitis.79 Lipomas are the most common palpable soft tissue masses (Table 23.1). These may occur within the subcutaneous tissues, muscle, or deep soft tissues. Simple lipomas are usually homogeneously isoechoic, or slightly hyperechoic to fat, with welldefined margins and internal wavy septations mimicking the surrounding fat80 (Fig. 23.30). They should be painless, mobile, and compressible with transducer pressure.81 Simple lipomas should not demonstrate internal complexity or hypervascularity; however, vessels may be seen passing through the lipoma. MRI with contrast should be performed to exclude underlying liposarcoma in the evaluation of any suspected lipoma with the following atypical features: deep acoustic shadowing, internal complexity or hypervascularity, size greater than 5 cm, deep or intramuscular location, pain, or history of enlargement.

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TABLE 23.1  Fat-Containing Soft Tissue Lesions Diagnosis

Sonographic Findings

Follow-Up

Simple lipoma

Similar echogenicity to subcutaneous fat Mobile Soft, compressible Painless Few, small vessels Complex echogenicity Deep acoustic shadowing Hypervascularity Size > 5 cm Deep or intramuscular location Pain History of enlargement Change in appearance over time or with Valsalva maneuver

Clinical follow-up sufficient if classic sonographic appearance

Indeterminate lipomatous lesion

Fat-containing hernia

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MRI with contrast for further evaluation, with biopsy if needed

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FIG. 23.30  Lipoma.  (A) A simple lipoma (arrows) is isoechoic to the adjacent subcutaneous fat and contains thin echogenic septations that parallel the skin surface. (B) Color Doppler imaging demonstrates two small vessels traversing the lipoma. There is no hyperemia.

A pitfall in the diagnosis of lipoma is that a fat-containing hernia can have some overlapping ultrasound appearances, including similar echogenicity to subcutaneous fat and internal wavy septations.80 Anatomic location, dynamic change in appearance, and movement with Valsalva maneuver can assist in the diagnosis of hernia. When appearances are typical for benign lipoma, periodic clinical follow-up can be performed rather than additional imaging or biopsy. Nerve sheath tumors are common, usually benign masses, although malignant nerve sheath tumors may uncommonly occur. Nerve sheath tumors are usually well-circumscribed solid hypoechoic masses, ovoid or fusiform in shape, and have faint deep acoustic enhancement.82 A contiguous nerve of origin of the lesion may be identified, either centrally within the lesion in the case of neurofibroma or peripherally related to the lesion in a schwannoma (however, these findings are not absolute) (Fig. 23.31). An echogenic capsule may be seen, and occasionally cystic spaces can occur in a degenerated schwannoma. A split-fat sign, although not entirely specific, is often seen in association with benign peripheral nerve sheath tumors. This sign comprises the presence of a rim of fat about the end of the lesion, representing fat normally present about the neurovascular bundle from which the lesion arises.83 The imaging appearances of benign and malignant peripheral nerve sheath tumors overlap, but malignant lesions should be considered when a lesion is more poorly defined (reflecting its infiltrative nature), is increasing in size, or is internally heterogeneous in appearance as a result of

internal necrosis and/or hemorrhage.84 If lesions typical for benign nerve sheath tumors on imaging are not biopsied or resected, then imaging and clinical follow-up are warranted. Various benign and malignant soft tissue lesions cannot be definitively discriminated by ultrasound alone. Lesions that remain indeterminate by ultrasound may then be evaluated with contrastenhanced MRI. Lesions that remain worrisome for malignant neoplasm will typically undergo image-guided biopsy (most often with ultrasound guidance). Primary soft tissue sarcomas typically appear solid, with irregular borders, variable internal necrosis, and hemorrhage (Fig. 23.32). They may be partly calcified (especially synovial sarcomas).85 The lesions usually demonstrate internal vascularization and may show local invasion of adjacent tissues. Secondary lesions (metastases) should be considered when a solid vascularized soft tissue lesion is found in a patient with known underlying malignancy. An important pitfall in the diagnosis of sarcoma is the clinical presentation with a hemorrhagic tumor, which can be incorrectly diagnosed as a bland hematoma, potentially leading to delay in correct diagnosis.86 To further complicate the diagnosis, patients may report a history of trauma. A spontaneous hematoma in the absence of anticoagulant medication should be regarded with suspicion, as should an apparent hematoma disproportionate to the patient-reported trauma.73 Such lesions should be evaluated carefully for vascularized components, which should be targeted for biopsy. If none are found, then repeat imaging should be performed in 6 weeks to document resolution of the hematoma. Following surgical

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FIG. 23.31  Peripheral Nerve Sheath Tumor.  (A) Long-axis image obtained at the site of a palpable mass shows an ovoid, hypoechoic mass with smooth borders, arising from the ulnar nerve. Note the ulnar nerve enters and exits the mass (arrows). (B) A short-axis image of the forearm demonstrates the mass in the expected location of the ulnar nerve. Color Doppler shows marked hyperemia within the mass. FCU, Flexor carpi ulnaris; FDS, flexor digitorum superficialis and profunda.

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FIG. 23.32  Sarcoma.  (A) A myxoid liposarcoma demonstrates mildly increased through transmission (arrows) due to the myxoid content. However, the mass is solid, with internal echoes. The superficial border is microlobulated. (B) Color Doppler imaging demonstrates increased blood flow within the mass.

resection of soft tissue sarcoma, ultrasound has been shown to have acceptable diagnostic accuracy but may miss a small number of recurrences. Ultrasound could play a complementary role to MRI in follow-up of these cases.87,88

FOREIGN BODIES Embedded soft tissue foreign bodies are a common problem in both adult and pediatric populations. Whereas some materials, such as metal and glass, are radiopaque and can be seen on plain radiographs, other materials such as wood are not detected radiographically. In these cases, ultrasound is an effective means for diagnosis. Foreign bodies are typically highly echogenic and may have posterior acoustic shadowing (Fig. 23. 33). They may be surrounded by a hypoechoic halo, representing an inflammatory reaction89 or hyperemia on color Doppler imaging. A large amount of associated fluid should prompt consideration of a secondary abscess. From a practical standpoint, the patient can usually accurately direct the sonographer to the area of greatest concern, and observation of skin entry and/or exit sites is helpful to focus evaluation. Knowledge of the trajectory of foreign body entry is particularly helpful in assessment of thin linear objects such

as wooden splinters, because they are often seen in nonanatomic oblique planes. Meticulous scanning is needed because small foreign bodies may be occult to cursory scanning in the hands and feet, where they may be obscured by adjacent ligaments, tendons, nerves, and vessels.90 It is also important to determine the relationship of the object to these anatomic structures and to determine if there is associated injury to them. In addition to the visualization of nonradiopaque foreign bodies, ultrasound may help guide surgical planning by providing accurate threedimensional localization of both radiopaque and nonradiopaque objects, and the overlying skin can be marked preprocedurally as an aid. Ultrasound can also be used to directly guide foreign body retrieval with real-time imaging.91,92

SOFT TISSUE INFECTION Infection of the skin and subcutaneous soft tissue, cellulitis, is a common clinical problem, which can be effectively treated with antibiotics. On ultrasound, the skin and subcutaneous tissues are thickened and hyperechoic early in the process. Later, there may be interdigitating reticular strands of hypoechogenicity representing interstitial inflammatory exudate,93 also known as the “cobblestone” appearance (Fig. 23.34).

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FIG. 23.33  Wood Foreign Body.  A wood splinter is embedded within the dorsal soft tissues of the hand. The splinter (arrowheads) appears as a linear, echogenic structure.

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FIG. 23.34  Cellulitis.  (A) Normal subcutaneous fat in the lateral nonaffected ankle is juxtaposed with the (B) abnormal contralateral ankle in the same patient with cellulitis. Note the hypoechoic echotexture of the normal fat (left side of image) versus the echogenic, swollen subcutaneous fat with obscuration of the normal internal septations (right side of image). (C) Color Doppler imaging demonstrates increased blood flow within the echogenic, swollen subcutaneous fat. (D) Gray-scale imaging in a different patient with cellulitis demonstrates anechoic fluid (arrows) within the echogenic cellulitic tissue.

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FIG. 23.35  Forearm Abscess.  (A) Short-axis image of a complex fluid hypoechoic collection (arrows) with echogenic peripheral soft tissue rind and increased through transmission, consistent with an abscess. (B) Color Doppler image demonstrates hyperemia within the surrounding soft tissues. U, Ulna.

Cellulitis may progress to abscess formation. The development of an associated abscess is an important finding to diagnose, as this will typically not respond to antibiotics, instead requiring drainage, either surgical or image guided. Abscesses can have a variable appearance on ultrasound evaluation.94 An abscess border may be well defined or poorly defined and infiltrative (Fig. 23.35). There may be a surrounding rim of hyperemic, thickened soft tissue. The internal liquefied material may demonstrate an anechoic, hypoechoic, or complex echogenic appearance, with internal septations and low-level echoes. Foci of echogenic gas, with associated ill-defined shadowing, may be present within the abscess. With dynamic compression, swirling of the echogenic debris within the abscess can be seen. In cases of fluid collection, several other entities may be considered and differentiated from an abscess. A seroma can be distinguished from an abscess in that a seroma appears as a simple anechoic to hypoechoic fluid collection without peripheral hyperemia, and there may be increased through transmission. A hematoma may appear as a mixed echogenicity fluid collection, yet will have no internal color Doppler flow and will have scant peripheral hyperemia. A soft tissue sarcoma will demonstrate solid, hyperemic internal components, as well as posterior acoustic shadowing. If the sonographic diagnosis of the fluid collection is indeterminate, confirmation can be obtained with aspiration (sonographically guided, if needed) and microbiologic and histologic assessment of the aspirate.

CONCLUSION Ultrasound is a cost-effective means by which to provide an accurate diagnosis in many scenarios of musculoskeletal pathology, including tendon and ligament injury, arthritis, and characterization of infection and some soft tissue masses. In addition to ongoing technical developments, critical to the use of this technology in the future will be technologist and physician education and appropriate and consistent incorporation of new technology into patient care pathways.

REFERENCES 1. Nazarian LN. The top 10 reasons musculoskeletal sonography is an important complementary or alternative technique to MRI. AJR Am J Roentgenol. 2008;190(6):1621-1626. 2. Jamadar DA, Jacobson JA, Caoili EM, et al. Musculoskeletal sonography technique: focused versus comprehensive evaluation. AJR Am J Roentgenol. 2008;190(1):5-9. 3. Teh J. Applications of Doppler imaging in the musculoskeletal system. Curr Probl Diagn Radiol. 2006;35(1):22-34. 4. Klauser AS, Miyamoto H, Bellmann-Weiler R, et al. Sonoelastography: musculoskeletal applications. Radiology. 2014;272(3):622-633. 5. Ooi CC, Malliaras P, Schneider ME, Connell DA. “Soft, hard, or just right?” Applications and limitations of axial-strain sonoelastography and shear-wave elastography in the assessment of tendon injuries. Skeletal Radiol. 2014;43(1):1-12. 6. Botar Jid C, Damian L, Dudea SM, et al. The contribution of ultrasonography and sonoelastography in assessment of myositis. Med Ultrason. 2010;12(2): 120-126. 7. Magarelli N, Carducci C, Bucalo C, et al. Sonoelastography for qualitative and quantitative evaluation of superficial soft tissue lesions: a feasibility study. Eur Radiol. 2014;24(3):566-573. 8. Weng L, Tirumalai AP, Lowery CM, et al. US extended-field-of-view imaging technology. Radiology. 1997;203(3):877-880. 9. Kavanagh EC, Koulouris G, Parker L, et al. Does extended-field-of-view sonography improve interrater reliability for the detection of rotator cuff muscle atrophy? AJR Am J Roentgenol. 2008;190(1):27-31. 10. Harcke HT, Grissom LE, Finkelstein MS. Evaluation of the musculoskeletal system with sonography. AJR Am J Roentgenol. 1988;150(6):1253-1261. 11. Peetrons P. Ultrasound of muscles. Eur Radiol. 2002;12(1):35-43. 12. Draghi F, Zacchino M, Canepari M, et al. Muscle injuries: ultrasound evaluation in the acute phase. J Ultrasound. 2013;16(4):209-214. 13. Nguyen JT, Nguyen JL, Wheatley MJ, Nguyen TA. Muscle hernias of the leg: a case report and comprehensive review of the literature. Can J Plast Surg. 2013;21(4):243-247. 14. Strobel K, Hodler J, Meyer DC, et al. Fatty atrophy of supraspinatus and infraspinatus muscles: accuracy of US. Radiology. 2005;237(2): 584-589. 15. Dillehay GL, Deschler T, Rogers LF, et al. The ultrasonographic characterization of tendons. Invest Radiol. 1984;19(4):338-341. 16. Crass JR, van de Vegte GL, Harkavy LA. Tendon echogenicity: ex vivo study. Radiology. 1988;167(2):499-501. 17. Khan KM, Bonar F, Desmond PM, et al. Patellar tendinosis (jumper’s knee): findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. Radiology. 1996;200(3):821-827.

CHAPTER 23  Overview of Musculoskeletal Ultrasound Techniques and Applications 18. Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc. 2001;9(4):233-238. 19. Connell D, Burke F, Coombes P, et al. Sonographic examination of lateral epicondylitis. AJR Am J Roentgenol. 2001;176(3):777-782. 20. Dones 3rd VC, Grimmer K, Thoirs K, et al. The diagnostic validity of musculoskeletal ultrasound in lateral epicondylalgia: a systematic review. BMC Med Imaging. 2014;14:10. 21. Eder L, Barzilai M, Peled N, et al. The use of ultrasound for the assessment of enthesitis in patients with spondyloarthritis. Clin Radiol. 2013;68(3): 219-223. 22. Frediani B, Falsetti P, Storri L, et al. Ultrasound and clinical evaluation of quadricipital tendon enthesitis in patients with psoriatic arthritis and rheumatoid arthritis. Clin Rheumatol. 2002;21(4):294-298. 23. Martinoli C, Bianchi S, Dahmane M, et al. Ultrasound of tendons and nerves. Eur Radiol. 2002;12(1):44-55. 24. Breidahl WH, Stafford Johnson DB, Newman JS, Adler RS. Power Doppler sonography in tenosynovitis: significance of the peritendinous hypoechoic rim. J Ultrasound Med. 1998;17(2):103-107. 25. Jeffrey Jr RB, Laing FC, Schechter WP, et al. Acute suppurative tenosynovitis of the hand: diagnosis with US. Radiology. 1987;162(3):741-742. 26. Hodgson RJ, O’Connor PJ, Grainger AJ. Tendon and ligament imaging. Br J Radiol. 2012;85(1016):1157-1172. 27. Zbojniewicz AM. US for diagnosis of musculoskeletal conditions in the young athlete: emphasis on dynamic assessment. Radiographics. 2014;34(5): 1145-1162. 28. Ebrahim FS, De Maeseneer M, Jager T, et al. US diagnosis of UCL tears of the thumb and Stener lesions: technique, pattern-based approach, and differential diagnosis. Radiographics. 2006;26(4):1007-1020. 29. Noszian IM, Dinkhauser LM, Orthner E, et al. Ulnar collateral ligament: differentiation of displaced and nondisplaced tears with US. Radiology. 1995;194(1):61-63. 30. Melville DM, Jacobson JA, Fessell DP. Ultrasound of the thumb ulnar collateral ligament: technique and pathology. AJR Am J Roentgenol. 2014;202(2):W168. 31. Finlay K, Lee R, Friedman L. Ultrasound of intrinsic wrist ligament and triangular fibrocartilage injuries. Skeletal Radiol. 2004;33(2):85-90. 32. Gondim Teixeira PA, Omoumi P, Trudell DJ, et al. High-resolution ultrasound evaluation of the trapeziometacarpal joint with emphasis on the anterior oblique ligament (beak ligament). Skeletal Radiol. 2011;40(7):897-904. 33. Chiavaras MM, Harish S, Oomen G, et al. Sonography of the anterior oblique ligament of the trapeziometacarpal joint: a study of cadavers and asymptomatic volunteers. AJR Am J Roentgenol. 2010;195(6):W428-W434. 34. Ferreira FB, Fernandes ED, Silva FD, et al. A sonographic technique to evaluate the anterior bundle of the ulnar collateral ligament of the elbow: imaging features and anatomic correlation. J Ultrasound Med. 2015;34(3): 377-384. 35. Bica D, Armen J, Kulas AS, et al. Reliability and precision of stress sonography of the ulnar collateral ligament. J Ultrasound Med. 2015;34(3):371-376. 36. Jacobson JA, Chiavaras MM, Lawton JM, et al. Radial collateral ligament of the elbow: sonographic characterization with cadaveric dissection correlation and magnetic resonance arthrography. J Ultrasound Med. 2014;33(6): 1041-1048. 37. Nazarian LN, McShane JM, Ciccotti MG, et al. Dynamic US of the anterior band of the ulnar collateral ligament of the elbow in asymptomatic major league baseball pitchers. Radiology. 2003;227(1):149-154. 38. Jacobson JA, Propeck T, Jamadar DA, et al. US of the anterior bundle of the ulnar collateral ligament: findings in five cadaver elbows with MR arthrographic and anatomic comparison—initial observations. Radiology. 2003;227(2): 561-566. 39. Sasaki J, Takahara M, Ogino T, et al. Ultrasonographic assessment of the ulnar collateral ligament and medial elbow laxity in college baseball players. J Bone Joint Surg Am. 2002;84-A(4):525-531. 40. Hua Y, Yang Y, Chen S, Cai Y. Ultrasound examination for the diagnosis of chronic anterior talofibular ligament injury. Acta Radiol. 2012;53(10): 1142-1145. 41. De Maeseneer M, Vanderdood K, Marcelis S, et al. Sonography of the medial and lateral tendons and ligaments of the knee: the use of bony landmarks

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as an easy method for identification. AJR Am J Roentgenol. 2002;178(6): 1437-1444. 42. Fornage BD. Peripheral nerves of the extremities: imaging with US. Radiology. 1988;167(1):179-182. 43. Bianchi S. Ultrasound of the peripheral nerves. Joint Bone Spine. 2008;75(6):643-649. 44. Silvestri E, Martinoli C, Derchi LE, et al. Echotexture of peripheral nerves: correlation between US and histologic findings and criteria to differentiate tendons. Radiology. 1995;197(1):291-296. 45. Sole JS, Pingree MJ, Spinner RJ, et al. Saphenous neuropathy secondary to extraneural ganglion cyst 15 years after reconstruction of the anterior cruciate ligament. PM R. 2014;6(5):451-455. 46. Rawal A, Ratnam KR, Yin Q, et al. Compression neuropathy of common peroneal nerve caused by an extraneural ganglion: a report of two cases. Microsurgery. 2004;24(1):63-66. 47. Elias DA, Lax MJ, Anastakis DJ. Musculoskeletal images. Ganglion cyst of Guyon’s canal causing ulnar nerve compression. Can J Surg. 2001;44(5):331-332. 48. Klauser AS, Halpern EJ, De Zordo T, et al. Carpal tunnel syndrome assessment with US: value of additional cross-sectional area measurements of the median nerve in patients versus healthy volunteers. Radiology. 2009;250(1): 171-177. 49. Wiesler ER, Chloros GD, Cartwright MS, et al. The use of diagnostic ultrasound in carpal tunnel syndrome. J Hand Surg Am. 2006;31(5): 726-732. 50. Duncan I, Sullivan P, Lomas F. Sonography in the diagnosis of carpal tunnel syndrome. AJR Am J Roentgenol. 1999;173(3):681-684. 51. Roll SC, Evans KD, Li X, et al. Screening for carpal tunnel syndrome using sonography. J Ultrasound Med. 2011;30(12):1657-1667. 52. Ozturk E, Sonmez G, Colak A, et al. Sonographic appearances of the normal ulnar nerve in the cubital tunnel. J Clin Ultrasound. 2008;36(6):325-329. 53. Okamoto M, Abe M, Shirai H, Ueda N. Morphology and dynamics of the ulnar nerve in the cubital tunnel. Observation by ultrasonography. J Hand Surg [Br]. 2000;25(1):85-89. 54. Van Den Berg PJ, Pompe SM, Beekman R, Visser LH. Sonographic incidence of ulnar nerve (sub)luxation and its associated clinical and electrodiagnostic characteristics. Muscle Nerve. 2013;47(6):849-855. 55. Campbell WW. Ulnar nerve subluxation. Muscle Nerve. 2013;48(6): 997-998. 56. Rezaei H, Torp-Pedersen S, af Klint E, et al. Diagnostic utility of musculoskeletal ultrasound in patients with suspected arthritis—a probabilistic approach. Arthritis Res Ther. 2014;16(5):448. 57. Ben Abdelghani K, Miladi S, Souabni L, et al. Role of ultrasound in assessing remission in rheumatoid arthritis. Diagn Interv Imaging. 2015;96(1): 3-10. 58. Wakefield RJ, Balint PV, Szkudlarek M, et al. Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol. 2005;32(12):2485-2487. 59. Szkudlarek M, Court-Payen M, Strandberg C, et al. Power Doppler ultrasonography for assessment of synovitis in the metacarpophalangeal joints of patients with rheumatoid arthritis: a comparison with dynamic magnetic resonance imaging. Arthritis Rheum. 2001;44(9):2018-2023. 60. Torp-Pedersen S, Christensen R, Szkudlarek M, et al. Power and color Doppler ultrasound settings for inflammatory flow: impact on scoring of disease activity in patients with rheumatoid arthritis. Arthritis Rheumatol. 2015;67(2):386-395. 61. Szkudlarek M, Court-Payen M, Strandberg C, et al. Contrast-enhanced power Doppler ultrasonography of the metacarpophalangeal joints in rheumatoid arthritis. Eur Radiol. 2003;13(1):163-168. 62. Cheung PP, Dougados M, Gossec L. Reliability of ultrasonography to detect synovitis in rheumatoid arthritis: a systematic literature review of 35 studies (1,415 patients). Arthritis Care Res (Hoboken). 2010;62(3):323-334. 63. McGonagle D, Gibbon W, O’Connor P, et al. A preliminary study of ultrasound aspiration of bone erosion in early rheumatoid arthritis. Rheumatology (Oxford). 1999;38(4):329-331. 64. Wright SA, Filippucci E, McVeigh C, et al. High-resolution ultrasonography of the first metatarsal phalangeal joint in gout: a controlled study. Ann Rheum Dis. 2007;66(7):859-864.

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65. Weidekamm C, Koller M, Weber M, Kainberger F. Diagnostic value of high-resolution B-mode and Doppler sonography for imaging of hand and finger joints in rheumatoid arthritis. Arthritis Rheum. 2003;48(2): 325-333. 66. Fornage BD. Soft-tissue changes in the hand in rheumatoid arthritis: evaluation with US. Radiology. 1989;173(3):735-737. 67. Kang MH, Moon KW, Jeon YH, Cho SW. Sonography of the first metatarsophalangeal joint and sonographically guided intraarticular injection of corticosteroid in acute gout attack. J Clin Ultrasound. 2015;43(3):179-186. 68. Thiele RG, Schlesinger N. Diagnosis of gout by ultrasound. Rheumatology (Oxford). 2007;46(7):1116-1121. 69. Iagnocco A. Imaging the joint in osteoarthritis: a place for ultrasound? Best Pract Res Clin Rheumatol. 2010;24(1):27-38. 70. D’Agostino MA, Conaghan P, Le Bars M, et al. EULAR report on the use of ultrasonography in painful knee osteoarthritis. Part 1: prevalence of inflammation in osteoarthritis. Ann Rheum Dis. 2005;64(12):1703-1709. 71. Lakkaraju A, Sinha R, Garikipati R, et al. Ultrasound for initial evaluation and triage of clinically suspicious soft-tissue masses. Clin Radiol. 2009;64(6):615-621. 72. Hung EH, Griffith JF, Ng AW, et al. Ultrasound of musculoskeletal soft-tissue tumors superficial to the investing fascia. AJR Am J Roentgenol. 2014;202(6):W532-W540. 73. Carra BJ, Bui-Mansfield LT, O’Brien SD, Chen DC. Sonography of musculoskeletal soft-tissue masses: techniques, pearls, and pitfalls. AJR Am J Roentgenol. 2014;202(6):1281-1290. 74. Teefey SA, Dahiya N, Middleton WD, et al. Ganglia of the hand and wrist: a sonographic analysis. AJR Am J Roentgenol. 2008;191(3):716-720. 75. Bianchi S, Abdelwahab IF, Zwass A, Giacomello P. Ultrasonographic evaluation of wrist ganglia. Skeletal Radiol. 1994;23(3):201-203. 76. Wang G, Jacobson JA, Feng FY, et al. Sonography of wrist ganglion cysts: variable and noncystic appearances. J Ultrasound Med. 2007;26(10): 1323-1328. 77. Akgul O, Guldeste Z, Ozgocmen S. The reliability of the clinical examination for detecting Baker’s cyst in asymptomatic fossa. Int J Rheum Dis. 2014;17(2):204-209. 78. Rudikoff JC, Lynch JJ, Phillips E, Clapp PR. Ultrasound diagnosis of Baker cyst. JAMA. 1976;235(10):1054-1055. 79. Cronan JJ, Dorfman GS, Grusmark J. Lower-extremity deep venous thrombosis: further experience with and refinements of US assessment. Radiology. 1988;168(1):101-107.

80. Wagner JM, Lee KS, Rosas H, Kliewer MA. Accuracy of sonographic diagnosis of superficial masses. J Ultrasound Med. 2013;32(8):1443-1450. 81. Jacobson JA. Fundamentals of musculoskeletal ultrasound: Expert ConsultOnline. Philadelphia: Elsevier Health Sciences; 2012. 82. Beggs I. Sonographic appearances of nerve tumors. J Clin Ultrasound. 1999;27(7):363-368. 83. Abreu E, Aubert S, Wavreille G, et al. Peripheral tumor and tumor-like neurogenic lesions. Eur J Radiol. 2013;82(1):38-50. 84. Murphey MD, Smith WS, Smith SE, et al. From the archives of the AFIP. Imaging of musculoskeletal neurogenic tumors: radiologic-pathologic correlation. Radiographics. 1999;19(5):1253-1280. 85. Widmann G, Riedl A, Schoepf D, et al. State-of-the-art HR-US imaging findings of the most frequent musculoskeletal soft-tissue tumors. Skeletal Radiol. 2009;38(7):637-649. 86. Brouns F, Stas M, De Wever I. Delay in diagnosis of soft tissue sarcomas. Eur J Surg Oncol. 2003;29(5):440-445. 87. Tagliafico A, Truini M, Spina B, et al. Follow-up of recurrences of limb soft tissue sarcomas in patients with localized disease: performance of ultrasound. Eur Radiol. 2015;25(9):2764-2770. 88. Choi H, Varma DG, Fornage BD, et al. Soft-tissue sarcoma: MR imaging vs sonography for detection of local recurrence after surgery. AJR Am J Roentgenol. 1991;157(2):353-358. 89. Montechiarello S, Miozzi F, Martinelli M, Giovagnorio F. Ultrasound picture of a wooden splinter evolved in phlegmon of the hand. J Ultrasound. 2010;13(1):38-40. 90. Shiels WE 2nd, Babcock DS, Wilson JL, Burch RA. Localization and guided removal of soft-tissue foreign bodies with sonography. AJR Am J Roentgenol. 1990;155(6):1277-1281. 91. Bradley M, Kadzombe E, Simms P, Eyes B. Percutaneous ultrasound guided extraction of non-palpable soft tissue foreign bodies. Arch Emerg Med. 1992;9(2):181-184. 92. Callegari L, Leonardi A, Bini A, et al. Ultrasound-guided removal of foreign bodies: personal experience. Eur Radiol. 2009;19(5):1273-1279. 93. Bureau NJ, Chhem RK, Cardinal E. Musculoskeletal infections: US manifestations. Radiographics. 1999;19(6):1585-1592. 94. Loyer EM, DuBrow RA, David CL, et al. Imaging of superficial soft-tissue infections: sonographic findings in cases of cellulitis and abscess. AJR Am J Roentgenol. 1996;166(1):149-152.

CHAPTER

24

 

The Shoulder Colm McMahon and Corrie Yablon

SUMMARY OF KEY POINTS • In the diagnosis of full-thickness rotator cuff tears, ultrasound is of comparable accuracy to magnetic resonance imaging, although it may be less accurate in the diagnosis of partial-thickness tears. • The key to scanning the shoulder is meticulous technique using a protocol that systematically evaluates the entirety of the shoulder.

• Understanding of optimal patient positioning, probe orientation, and shoulder anatomy is critical to effective diagnostic shoulder ultrasound. • Ultrasound allows dynamic assessment of subacromial and subcoracoid impingement, biceps subluxation, and rotator cuff integrity.

CHAPTER OUTLINE CLINICAL PERSPECTIVE SHOULDER ANATOMY SCAN TECHNIQUE Biceps Tendon Evaluation Subscapularis Tendon Evaluation Supraspinatus Evaluation Infraspinatus, Teres Minor, and Posterior Shoulder Evaluation Rotator Cuff Musculature Evaluation

ROTATOR CUFF DEGENERATION AND TEARS Background Tendinosis Full-Thickness Rotator Cuff Tears Partial-Thickness Rotator Cuff Tears Postsurgical Rotator Cuff Muscle Atrophy Subacromial-Subdeltoid Bursa Calcific Tendinitis

CLINICAL PERSPECTIVE The human shoulder represents an intricate balanced anatomic system capable of exerting force in multiple directions, in multiple different positions, all possible because of a number of static and dynamic structures, which when functioning well provide for the competing needs of movement and stability. Proper function of the shoulder is critical for activities ranging from the most basic of daily life to many sporting pursuits including those of the throwing athlete. The shoulder is, however, prone to injury, related to anatomic factors such as subacromial impingement.1,2 Shoulder pain and limitation of motion are very common causes for quality-of-life impairment, medical resource use, and loss of workplace productivity.3-7 In fact, about 50% of adults have at least one episode of shoulder pain yearly.8 Clinical presentation varies from acute injury9,10 to more chronic dysfunction, which is more common with advancing age.11 Although shoulder pain and dysfunction are common clinical complaints, the underlying etiology is variable, with causes including rotator cuff pathology (degeneration, tears, calcific tendinosis), long head biceps pathology, subacromial

LONG HEAD BICEPS TENDON PATHOLOGY ARTHROPATHY Degenerative Inflammatory PITFALLS IN SHOULDER ULTRASOUND CONCLUSION

subdeltoid bursa pathology, arthropathy of the glenohumeral or acromioclavicular joint (which may be of inflammatory or degenerative cause), or osseous disease. Of these, subacromial subdeltoid bursitis and rotator cuff pathology are the most common causes of symptomatic shoulder disease.12 Correct diagnosis is crucial for treatment decision making, allowing appropriate management with surgical or nonsurgical treatment, which may diminish the personal and societal effect of shoulder problems.13,14 Of course, clinical history taking and examination are intrinsic parts of patient assessment, but the accuracy of clinical examination in diagnosis of the cause of shoulder pain is both modest and variable.15-20 In this clinical and socioeconomic setting, the advantages of ultrasound as a diagnostic test are myriad, as this technique is accurate, cost-effective, and well tolerated by patients. In the diagnosis of full-thickness rotator cuff tears, ultrasound is of comparable accuracy to magnetic resonance imaging (MRI), although it may be less accurate in the diagnosis of partialthickness tears.21-30 Ultrasound can also determine muscle atrophy, an important parameter in predicting successful surgical outcome of rotator cuff repair.31 Ultrasound is a good alternative to MRI in patients who are claustrophobic, are of large size, or have

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incompatible implanted metallic and electronic devices. Patients with shoulder pain tolerate ultrasound better than MRI owing to relatively increased patient comfort and diminished examination time.32 Ultrasound provides several benefits that MRI cannot. Ultrasound offers the possibility of dynamic assessment of the rotator cuff, allowing the patient to be imaged while engaging in the motion that causes pain or clicking. Ultrasound can assess subacromial impingement, subcoracoid impingement, and biceps tendon subluxation dynamically, in real time, and cine clips can be obtained. If there is a question as to pathology versus a normal variant, comparison to the contralateral side can be easily made. Dynamic compression of rotator cuff tears can aid in the assessment of cuff integrity. Ultrasound is also more sensitive than MRI to the detection of calcium deposits within the tendon. Finally, patients can receive the results of their examination instantaneously, and this adds tremendously to patients’ satisfaction with the modality.33 It should be noted that ultrasound is not without limitations. In the clinical setting of instability, ligamentous injury, or suspected glenoid labral injury, MRI or MRI arthrography are preferred. Ultrasound is also of limited value in the evaluation of bony disorders, and plain radiography should be considered complementary in the assessment of patients with shoulder pain to further diagnosis of fracture, bone lesions, subacromial spurs, acromioclavicular osteophytes, acromiohumeral interval narrowing, glenohumeral and acromioclavicular alignment and joint space abnormality, and soft tissue calcification. In view of these considerations, ultrasound should be considered a first-line investigation in patients with acute or chronic shoulder pain in whom rotator cuff tear is suspected. Imaging algorithms detailing the role of shoulder ultrasound in specific common scenarios have been published in a consensus statement Acromion

by the Society of Radiologists in Ultrasound, a highly useful resource.34

SHOULDER ANATOMY The shoulder consists of the osseous shoulder girdle with associated muscles and ligamentous structures.35 Central to understanding the anatomy of the shoulder and scan technique is the anatomy of the scapula (Fig. 24.1). The scapula consists of a flat triangular bone with anterior and posterior surfaces in addition to the glenoid fossa laterally. The glenoid fossa is deepened by a fibrocartilaginous labrum, and lined with hyaline cartilage for articulation with the humerus at the synovial glenohumeral joint. The glenoid neck tapers to the flatter triangular body of the scapula. At the anterior aspect of the scapular body is the subscapular fossa, a concavity with oblique ridges that gives origin to the subscapularis muscle. The posterior surface of the scapula is convex posteriorly and divided into superior and inferior portions by the scapular spine. Above the spine is the supraspinatus fossa, which provides origin to the supraspinatus muscle. Below the spine is the infraspinatus fossa, with the infraspinatus muscle originating from the medial two-thirds, and the teres minor originating along the medial border. Extending superolaterally from the scapular spine is the acromion, a flattened hooklike structure that curves from posterior to anterior where it articulates with the clavicle at the acromioclavicular joint. The acromion and scapular spine give origin to the deltoid muscle. The acromion is important functionally and for the purpose of ultrasound technique as it overlies the supraspinatus and infraspinatus in the neutral position, prohibiting accurate visualization unless specific positioning maneuvers are undertaken. Also, osseous spurs (subacromial spurs) along the undersurface of the acromion may be a cause for subacromial

Clavicle

Humeral head

Humeral head

Greater tuberosity

Lesser tuberosity Glenoid

Glenoid

Humerus Scapula

Anterior View

Posterior View

FIG. 24.1  Illustration of the Scapula and Osseous Landmarks.

CHAPTER 24  The Shoulder

Acromion

Coracoid process

Clavicle

Subscapularis

879

Supraspinatus

Supraspinatus

Capsular ligament (cut)

Humerus

Teres minor

Scapula

Infraspinatus

Right Shoulder Anterior View

Right Shoulder Posterior View

FIG. 24.2  Illustration of Rotator Cuff Anatomy.

impingement. These typically form at the attachment of the coracoacromial ligament. Furthermore, osteoarthritis at the acromioclavicular joint may result in osteophyte formation, which, when present inferiorly, may cause rotator cuff tendon impingement. The coracoid process is a fingerlike curved process extending anteriorly from the scapular neck, giving attachment to the short head of biceps, coracobrachialis, and pectoralis minor muscles in addition to the coracohumeral ligament, and also the coracoclavicular ligaments, which help stabilize the acromioclavicular joint. The rotator cuff consists of four muscles: the subscapularis, supraspinatus, infraspinatus, and teres minor muscles (Fig. 24.2). These originate from the scapula and insert on the proximal humerus. Normal rotator cuff tendons are about 4 to 6 mm in thickness,36 tapering out smoothly from medial to lateral along the insertional footprint at the greater tuberosity. The subscapularis muscle is a multipennate structure that originates from the anterior surface of the scapula, which converges to a flat tendon laterally to insert on the lesser tuberosity. Of note, the inferior one-third of the subscapularis remains muscular to the level of the lesser tuberosity.37 The supraspinatus muscle originates from and occupies the supraspinatus fossa, with its tendon extending laterally to insert on the greater tuberosity of the humerus at its anterior aspect. The tendon has a more cordlike component anteriorly and is flatter and more quadrilateral in short axis at its mid and posterior fibers. The infraspinatus muscle originates at the infraspinatus fossa and passes laterally to insert on the posterosuperior aspect of the greater tuberosity. The fibers of the supraspinatus and infraspinatus tendons merge at their posterior and anterior borders, respectively, forming a conjoint insertion. The teres minor originates along the lateral border of

the scapular body and inserts along the posterior aspect of the greater tuberosity, inferior to the infraspinatus. The long head of biceps tendon originates from a bony tubercle at the superior glenoid, the supraglenoid tubercle, and from the superior labrum. It passes inferolaterally between the subscapularis and supraspinatus tendons, which form the inferior and superior borders of the rotator interval (Fig. 24.3). Within the rotator interval, the tendon is stabilized by a ligamentous sling formed by the coracohumeral and superior glenohumeral ligaments. Passing inferolaterally out of the rotator interval, the long head of biceps tendon becomes extraarticular and extends inferiorly in the bicipital or intertubercular groove, which lies between the greater and lesser tuberosities. The biceps tendon is stabilized in the groove by the transverse ligament, formed by tendinous fibers at the subscapularis insertion.38 The subacromial-subdeltoid bursa is a synovium-lined flat, thin structure that lies between the rotator cuff tendons and the overlying deltoid muscle and acromion.39 It serves to reduce friction between the rotator cuff and the overlying structures, permitting smooth movement.

SCAN TECHNIQUE For consistent and accurate shoulder ultrasound performance, a standard protocol is suggested with comprehensive evaluation in every case, rather than targeted scanning (Table 24.1).40-44 The patient should be sitting upright if possible, either on a rotating stool or at the edge of a bed. A chair with a backrest should not be used, because this would interfere with patient positioning. Likewise, the sonographer should also sit on a rotating stool, with the seat position somewhat higher than the patient’s, so

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Acromion

Acromioclavicular Coracoid joint process Clavicle

Subscapularis

Supraspinatus Lesser tuberosity Greater tuberosity Bicipital tendon sheath Subscapularis tendon Bicipital tendon Biceps muscle (long head)

Glenohumeral joint

Scapula FIG. 24.3  Illustration of the Long Head Biceps Tendon in the Rotator Interval and in the Bicipital Groove.

TABLE 24.1  Routine Shoulder Ultrasound Protocol Long head of biceps tendon Subscapularis tendon

Supraspinatus tendon

Infraspinatus tendon Teres minor tendon Supraspinatus and infraspinatus muscles Posterior shoulder Acromioclavicular joint

Long and short-axis static images Long and short-axis static images Dynamic evaluation for subcoracoid impingement Long and short-axis static images Dynamic evaluation for subacromial impingement Long and short-axis static images Long and short-axis static images Sagittal images—panorama if possible Axial plane image Coronal plane image

Biceps Tendon Evaluation Biceps tendon evaluation is best performed with the arm in a neutral position, resting the forearm on the patient’s ipsilateral thigh, with elbow flexed and the palm up (Fig. 24.4). In this position, the biceps tendon is seen anteriorly.45 The tendon can be imaged in its short axis within the bicipital groove by holding the probe transversely with respect to the upper arm and following the course of the tendon inferiorly where it passes deep to the pectoralis major tendon insertion on the humerus. In short axis, the tendon appears as a homogeneous, echogenic, round or ovoid structure that may be accompanied by a trace of fluid within its tendon sheath. The normal biceps tendon is 2 to 4 mm thick.36 The tendon can be followed superiorly and medially into the rotator interval, by angling the probe more obliquely to remain orthogonal to its short axis. Finally, the probe can be rotated 90 degrees to view the tendon in its long axis where it should appear smooth and fibrillar.

Subscapularis Tendon Evaluation that the sonographer’s arm can be held in a natural, ergonomic position. If a patient is wheelchair-bound, it is helpful if possible to temporarily remove the backrest. If the patient cannot sit upright, more limited scanning is possible with the patient lying supine, with the affected shoulder at the edge of the bed. A high-frequency 12- to 15-MHz linear array transducer is used to permit high-resolution scanning. Occasionally, in larger patients, a lower-frequency probe (9 MHz) may be needed to achieve tissue penetration to the required depth, but this incurs a reduction in resolution. When scanning any tendon, care should be taken to maintain an angle of close to 90 degrees between the probe and the tendon of interest to avoid artifactual hypoechogenicity due to anisotropy. This is discussed in more detail later in the chapter.

The subscapularis is scanned with the patient’s arm at the side, in external rotation with the palm facing up44 (Fig. 24.5). The tendon should be evaluated in long axis, with the probe aligned with the subscapularis tendon, and in short axis, with the probe held perpendicular to the subscapularis tendon. The coracoid process of the scapula, medial to the subscapularis and palpable in many patients, is a useful anatomic landmark when locating the subscapularis tendon. The tendon fibers can be seen emanating from the broad multipennate muscle belly. The normal hypoechoic muscle should not be mistaken for fluid. In this position the patient’s arm can be rotated from external rotation to neutral position, while observing the passage of the tendon fibers deep to the coracoid process to assess for subcoracoid impingement (Video 24.1). This dynamic maneuver is also useful to assess for long head biceps tendon subluxation from the bicipital groove.

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FIG. 24.4  Long Head Biceps Tendon (LHBT).  (A) Photograph of the probe position for imaging the LHBT in short axis. The patient’s shoulder is externally rotated, with the elbow flexed and held tight to the body, with the forearm palm up, resting on the patient’s lap. This position rotates the LHBT anteriorly. (B) Short-axis image of LHBT (arrow). (C) Photograph of probe position for imaging the LHBT in long axis. The probe is rotated 90 degrees to the short-axis starting position. Patient position remains the same as for the short-axis image. (D) Long-axis image of LHBT (arrowheads).

Supraspinatus Evaluation In neutral position the supraspinatus tendon is largely obscured from view by the overlying acromion. To draw the tendon out from under the acromion, specific maneuvers are needed. The position, originally described by Crass46 (Fig. 24.6), consists of asking the patient to place his or her hand behind the back, reaching toward the opposite back pocket with the back of the hand. This results in flexion, internal rotation, and adduction of the shoulder. In this position, the greater tuberosity is located anteriorly, so the supraspinatus tendon courses anterolaterally to its insertion and is drawn out from under the acromion, allowing visualization. Patients with shoulder pain often find this position difficult to achieve and maintain, so an alternative position is the “modified Crass position” (Fig. 24.7) in which the patient puts the palm of the hand on the ipsilateral hip or buttock, with elbow flexed and directed posteriorly. In this position, the greater tuberosity is similarly positioned as in the original Crass position, but the maneuver is usually well tolerated by patients. The supraspinatus tendon will again course anterolaterally to the greater tuberosity. To visualize the supraspinatus in long axis, the probe should parallel the long-axis orientation of the tendon, resulting in an

oblique sagittal probe position relative to the patient, with the probe directed toward the patient’s ear (see Fig. 24.7A). The long head biceps tendon in long axis with the patient in the modified Crass position is a useful landmark for locating the most anterior portion of the supraspinatus tendon (Fig. 24.8). If the probe in long axis is then moved posteriorly in the same plane, the entire supraspinatus will be assessed. Correctly imaged, the normal supraspinatus should appear smooth, echogenic, and fibrillar, tapering at its insertion or “footprint” with a so called “bird’s beak appearance.” Normal rotator cuff tendons possess a fibrocartilaginous interface at their bony attachment that may manifest as a thin hypoechoic band paralleling the insertional cortex, similar in echogenicity to hyaline cartilage.37 This should not be mistaken for a tear. The probe is then rotated 90 degrees to image the tendon in short axis. In this position, the more cordlike anterior fibers of the supraspinatus tendon are seen merging with the flatter quadrilateral mid and posterior fibers. While visualizing the supraspinatus tendon in short axis, it is important to move the probe anteriorly so that the long head biceps tendon is imaged in short axis. This ensures that the entire anterior leading edge of the supraspinatus has been evaluated. In short axis, the rotator interval is well seen

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FIG. 24.5  Subscapularis Tendon.  (A) Long-axis probe position. From the long head biceps tendon (LHBT) starting position, the patient now externally rotates the elbow, keeping the elbow tight to the body with the palm up. This position elongates the subscapularis tendon and rotates the tendon out from under the coracoid process, allowing visualization. The probe is placed across from the coracoid process. Note that the probe position is similar for imaging the LHBT in short axis, but the patient’s position is different. (B) Long-axis image of subscapularis tendon (arrowheads). (C) Short-axis probe position. From the long-axis starting position, the probe is simply turned 90 degrees to image the subscapularis in short axis, with the patient remaining in the same position. Note that the probe position is similar to the LHBT long-axis probe position, but the patient’s position is different. (D) Short-axis image of subscapularis tendon (arrowheads). See also Video 24.1.

anterior to the tendon, with the biceps tendon coursing through the interval, also in short axis, stabilized by the coracohumeral ligament and superior glenohumeral ligament. As with all tendons, the supraspinatus should be scanned through its entirety from anterior to posterior in long axis and medial to lateral in short axis. When the posterior fibers of the supraspinatus tendon are reached, the more posteriorly oriented fibers of the infraspinatus tendon are routinely encountered; this is a helpful landmark to ensure the entire supraspinatus tendon has been studied. It is important to note that as the transducer is moved posteriorly, the greater tuberosity changes shape, from ledgelike to flat. This area of transition is where the anterior infraspinatus fibers overlap the posterior supraspinatus fibers. A discrete overlap of fibers can be visualized at this juncture (Fig. 24.9, Video 24.2). Continuing posteriorly from this overlap, the infraspinatus fibers can be evaluated in their entirety, looking for the similar normal fibrillar pattern in the long axis, and the echogenic appearance in the short axis.

The rotator cable is a thin fibrous band contiguous with the coracohumeral ligament that passes along the deep surface of the supraspinatus and infraspinatus tendons.47 This bandlike structure is oriented perpendicular to the long axis of the rotator cuff, running in an anterior to posterior direction, and is felt to have a biomechanical role in stress distribution, likened to the cable of a suspension bridge.48 It can be visualized consistently with ultrasound, seen in its short axis where it appears elliptical, when scanning the long axis of the supraspinatus and infraspinatus (Fig. 24.10). It is located about 1 cm (average 9 mm, range 4-15 mm47) medial to the rotator cuff insertion at the greater tuberosity. Dynamic assessment for subacromial impingement of the supraspinatus can now be performed. The patient’s arm rests in a neutral position at his or her side, and the probe is positioned in a coronal plane, with the acromion at the medial aspect of the field of view, and the greater tuberosity laterally. The patient then abducts the arm slowly, and the motion of the supraspinatus

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tendon under the acromion is observed. The motion should be smooth and uninterrupted, without deformation of the tendon under the acromion, deformation of the bursa, or pooling of bursal fluid (Video 24.3). A useful alternative technique to assess the supraspinatus has been described by Turrin and Cappello.49 In this technique, the patient lies supine with the affected shoulder at the edge of the bed, but allows the arm to drop over the side of the bed, with the elbow extended and the forearm pronated. This can be particularly helpful in patients who are unable to sit—for example following cerebrovascular accident with hemiplegia, when associated shoulder pain is not uncommon, though of varied etiology (related to subluxation, spasticity, adhesive capsulitis, or rotator cuff tears), and standard positioning in the seated position may be difficult.50

FIG. 24.6  Crass Position.  The patient places her arm behind her back with the dorsum of the hand resting on the contralateral back pocket. This position rotates the supraspinatus tendon from underneath the acromion.

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Infraspinatus, Teres Minor, and Posterior Shoulder Evaluation Several methods of evaluation of the infraspinatus have been described. The patient can remain in the modified Crass position, or with the arm hanging at the side, and scanning can simply

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FIG. 24.7  Supraspinatus Tendon and Modified Crass Position.  Probe position for supraspinatus in long axis, with the patient in the modified Crass position. The patient places her arm behind her back, palm on the ipsilateral back pocket, with the elbow straight back, as tight to the body as possible. This position rotates the supraspinatus from underneath the acromion. This position is usually better tolerated by patients who have a rotator cuff tear. (A) The probe is placed somewhat obliquely, directed toward the patient’s ear. (B) Long-axis image of the supraspinatus tendon (arrowheads). (C) Short-axis probe position. The patient remains in the modified Crass position and the probe is rotated 90 degrees from the long-axis starting position. (D) Short-axis image of the supraspinatus tendon (arrowheads). Note that the long head of biceps tendon is visualized anterior to the supraspinatus tendon (arrow).

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be continued posteriorly from the supraspinatus both in long and short axis. An alternate position of scanning the infraspinatus has been described, in which the patient is asked to bring the arm forward across the chest, resting the hand on the contralateral shoulder.44,51 These positions allow imaging of the infraspinatus tendon and muscle. The probe is held in an oblique transverse orientation, placed on the posterior shoulder to parallel the long axis of the infraspinatus tendon, using the inferior border of the scapular spine as a visual landmark (Fig. 24.11). In long axis the tendon appears similar to the supraspinatus in morphology, although having a more elongated tapered appearance at its insertion, lacking the bird’s beak appearance seen at the supraspinatus footprint. The probe is then rotated 90 degrees, to the short axis of the infraspinatus, and the tendon and muscle are evaluated. The normal muscle is hypoechoic and positioned below the scapular spine in the infraspinatus fossa.

FIG. 24.8  Long-Axis Biceps Tendon Image, With Shoulder in the Modified Crass Position. This is a good starting point for imaging the supraspinatus tendon in long axis. Once the long head biceps tendon is seen well in long axis (arrowheads), the probe can simply be moved posteriorly to image the supraspinatus tendon.

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The teres minor tendon is also evaluated in this position and is seen inserting at the posterior aspect of the greater tuberosity, inferior to the infraspinatus insertion. The teres minor muscle can be seen arising from the posterolateral scapula, inferior to the infraspinatus muscle. Also in this position, the posterior shoulder is seen, with visualization of glenohumeral joint fluid and limited views of the posterior labrum and spinoglenoid notch. Scanning the posterior shoulder with external rotation may aid visualization of a glenohumeral effusion.52

Rotator Cuff Musculature Evaluation Using the scapular spine as a visual landmark, the supraspinatus muscle in the supraspinatus fossa can be imaged by placing the probe perpendicular to the scapular spine (Fig. 24.12). This demonstrates the muscle in its short axis. The normal muscle should be hypoechoic and convex in contour, and should fill the

FIG. 24.9  Overlap of Posterior Supraspinatus (Arrow) and Anterior Infraspinatus Fibers (Arrowheads) Seen in Long Axis.  See also Video 24.2.

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FIG. 24.10  Rotator Cable.  (A) The rotator cable (arrows) is visualized in short axis along the articular surface of the supraspinatus tendon, when this tendon is imaged in long axis. (B) The rotator cable (arrows) is visualized as a linear structure in its long axis (arrows) along the articular surface of the supraspinatus tendon, when this tendon is imaged in short axis. (Courtesy of Dr. Yoav Morag, Ann Arbor, MI.)

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FIG. 24.11  Infraspinatus Tendon.  (A) Long-axis probe position. The patient can simply rest the arm at the side, with the forearm palm up in the lap. The probe is placed under the scapular spine and moved laterally to see the distal insertion on the greater tuberosity. (B) Long-axis image of infraspinatus tendon (arrowheads). (C) Short-axis probe position. The probe is rotated 90 degrees to the infraspinatus long-axis starting position. (D) Short-axis image of infraspinatus tendon (arrowheads).

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FIG. 24.12  Rotator Cuff Musculature.  (A) Probe position for supraspinatus muscle. The probe is placed at the top of the shoulder, medial to the acromioclavicular joint, and posterior to the clavicle. (B) Probe position for infraspinatus and teres minor muscles. The probe is placed 90 degrees to the scapular spine, just inferior to the scapular spine (arrowheads). (C) Extended field-of-view image of supraspinatus (straight arrow), infraspinatus (arrowheads), and teres minor (curved arrow). Note the spine of the scapula (*) separating the supraspinatus and infraspinatus muscles.

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supraspinatus fossa. The central tendon should be visible within the muscle. To image the infraspinatus and teres minor muscles, the transducer is moved distal to the scapular spine, remaining perpendicular to the spine. A relative comparison and assessment of muscle volume and echogenicity can easily be made by using an extended field-of-view scan technique.

ROTATOR CUFF DEGENERATION AND TEARS Background Rotator cuff dysfunction, either due to tear or to tendon degeneration, is the most common cause of referral for evaluation of the shoulder.53 Likewise, rotator cuff disease is the most frequent cause for referral for shoulder ultrasound. The supraspinatus tendon is the most commonly injured tendon in the rotator cuff.54 The incidence of rotator cuff tears rises as patients age. Up to 22% of patients age 65 and older have rotator cuff tears.55 It is interesting to note that 70% of imaged patients age 65 and older have asymptomatic rotator cuff defects.56 Rotator cuff tears in patients younger than 40 are uncommon, but they do occur in the setting of acute trauma or sports-related injuries. Rotator cuff tears in patients older than 40 are usually secondary to tendon degeneration.

Tendinosis Tendinosis of the rotator cuff is a degenerative process that may be associated with shoulder pain. Histologically, there is no inflammatory component (hence the term “tendinitis” is not appropriate for this condition), but rather mucoid degeneration and frequently chondroid metaplasia are present. On ultrasound, tendinosis appears heterogeneous or hypoechoic, with tendon thickening, and loss of the normal fibrillar pattern57 (Fig. 24.13). Although discrete defects or tears are not encompassed by this diagnosis, they may coexist.

Full-Thickness Rotator Cuff Tears Ultrasound is a reliable method for diagnosis of rotator cuff tears, with sensitivity and specificity over 90%21,26,28,29,58,59 for full-thickness tears, and low interobserver variability.60,61 Fullthickness tears are visualized as a hypoechoic or anechoic gap within the rotator cuff (Fig. 24.14), which may also have a concave contour at its bursal border.30,62 Alternatively, a greatly retracted tear can result in nonvisualization of the rotator cuff tendon62 (Fig. 24.15). This occurs because the tendon may retract deep to the acromion, and is likely in cases in which the degree of retraction exceeds 3 cm.63 When a full-thickness tear is present, the gap between the retracted tendon end and the greater tuberosity or distal tendon stump may be filled with hypoechoic fluid or echogenic debris (Fig. 24.16) and granulation tissue. Alternatively, the subacromial-subdeltoid bursa (frequently thickened) and the deep surface of the deltoid muscle may occupy the defect created by the tear.29 Small foci of debris within the tear gap may give the appearance of mobile or “floating” bright spots.59 Fluid within the tear gap my accentuate visualization of the underlying humeral head articular cartilage owing to enhanced through transmission of the ultrasound beam, referred to as the “cartilage interface sign”64 (Fig. 24.17). Occasionally one may be uncertain as to whether abnormal echotexture in the location of the rotator cuff represents a partial tear or a full-thickness tear with intervening granulation tissue and debris. Dynamic compression of the abnormal area may clarify this confusion by causing complex fluid and debris to swirl within the rotator cuff tear. It may be helpful to ascertain if a tear is more likely to be acute or chronic because acute tears are felt to have a greater chance of successful surgical outcome. In this regard, the findings of glenohumeral and bursal effusions are more common in acute tears. In addition, midsubstance tears, medial to the bone-tendon junction, are more likely to be acute. On the other hand, severely retracted tears are more likely to be chronic.65 In chronic full-thickness tears, the tendon gap may be filled with

FIG. 24.13  Tendinosis of the Supraspinatus.  Long-axis image of the supraspinatus tendon (arrowheads) demonstrates hypoechogenicity and diffuse loss of normal fibrillar echotexture.

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FIG. 24.14  Focal Full-Thickness Supraspinatus Tear.  (A) Long-axis image of the anterior supraspinatus tendon demonstrates intact fibers (arrowheads). (B) Long-axis image of more posterior fibers of supraspinatus show a full-thickness tear with hypoechoic fluid (arrow) within the gap between the torn tendon end (arrowheads) and the greater tuberosity (*). (C) Short-axis image of supraspinatus. Intact anterior fibers (white arrowhead) are shown, with a fluid-filled gap (straight arrow) at the posterior supraspinatus tear. Intact anterior infraspinatus fibers (curved arrow) are visible posterior to the tear. Assisting in orientation, the long head biceps tendon (black arrowhead) appears anteriorly.

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FIG. 24.15  Full-Thickness Supraspinatus Tear With Retraction of the Tendon Beneath the Acromion.  Image in the expected location of the supraspinatus tendon in long (A) and short (B) axis demonstrates absence of the tendon above the humeral head (*) and greater tuberosity (white arrow). Fluid and debris are seen in place of the normal tendon (arrowheads). Note the intact long head biceps tendon anteriorly (black arrow).

noncompressible, complex echogenic debris and granulation tissue that are contiguous with the subacromial subdeltoid bursa, and this may give the false impression of rotator cuff volume to the novice practitioner.

Partial-Thickness Rotator Cuff Tears As with full-thickness rotator cuff tears, partial-thickness tears occur in both younger and older patients. Partial tears

occur more commonly than full-thickness tears in younger patients, and most commonly occur in young athletes. Partial articular-sided supraspinatus tears are the most common subtype in the young athlete.66 In the older patient population, partial-thickness tears also most commonly occur in the supraspinatus tendon, but the most common cause is tendon degeneration, with increased incidence as patients age.

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FIG. 24.16  Focal Full-Thickness Tear of Supraspinatus Tendon.  In this long-axis image of the supraspinatus tendon, there is a focal full-thickness tear, and the gap between the tendon retracted end and the greater tuberosity is filled with echogenic debris (arrow) and fluid.

tuberosity.67,68 This type of tear is most commonly seen in athletes who engage in overhead-throwing activities. Partial-thickness tears vary from small, 1- to 2-mm tears to those involving more than 50% of tendon thickness. Although tears of 50% or greater have typically been referred for repair, patients with tears involving as little as 25% of the tendon may benefit from arthroscopic debridement.69,70 Surgical decisions, however, are made in the context of the individual patient performance status, limitation by the injury, comorbidities, and patient preference. Partial tears occur most commonly along the articular side of the tendon in younger patients.70 Care must be taken to adequately assess the anterior leading edge fibers of the supraspinatus tendon, where these tears can often occur.71 Bursalsided partial-thickness tears may manifest as flattening of the bursal contour of the tendon of varying severity.29 This may lead to an hourglass-like diameter shift between areas of normal and attenuated tendon.28 An associated sign frequently observed in the setting of both partial- and full-thickness rotator cuff tears is the finding of cortical irregularity of the greater tuberosity, a finding with a 75% positive predictive value for the presence of an associated rotator cuff tear.72 This is more severe in full-thickness tears and represents bony remodeling with irregularity, pitting, and erosion.73 A second sign that can be seen in both partial articularsided and full-thickness tears is the “cartilage interface” sign, mentioned earlier. In analysis of partial- and full-thickness tears, it is important to quantify the extent of the tear in both its long and short axis (tear length and width); for example, in the case of a supraspinatus tendon tear, a measurement of the medial to lateral tear length should be made in long axis, and a measurement of the anterior to posterior tear width should be made on short-axis imaging.

Postsurgical Rotator Cuff FIG. 24.17  Full-Thickness Supraspinatus Tear With Associated Cartilage Interface Sign.  A hyperechoic line (arrowheads) is seen along the surface of the normal hypoechoic cartilage (arrow), along the superior aspect of the humeral head (*).

Partial-thickness tears are characterized by a focal area of hypoechogenicity or mixed echogenicity involving one side of the tendon, but not extending through the entire thickness.58 There are several subtypes of partial-thickness tears of the rotator cuff (Figs. 24.18 and 24.19). Bursal-sided partial-thickness tears (Fig. 24.19A and B) occur superficially, just deep to the subacromial subdeltoid bursa. Articular-sided tears (see Fig. 24.19C and D) occur at the undersurface of the tendon in contiguity with the joint space. Intrasubstance tears (Fig. 24.19E) can occur either within the substance of the tendon footprint at the enthesis or longitudinally within the tendon fibers. These tendons may not be identified at arthroscopy because they do not communicate with either the bursal or the articular surfaces of the tendon. A specific partial-thickness tear type is the “rim-rent” tear (see Fig. 24.19F), occurring at the articular side of the supraspinatus tendon, extending into the tendon footprint on the greater

After surgical rotator cuff repair, the appearance of the rotator cuff and surrounding soft tissues is abnormal, as can be expected, with loss of normal soft tissue planes and abnormal echotexture of the rotator cuff tendon. Because of loss of normal interface with the overlying subacromial bursa, dynamic assessment may aid in identification and visualization of the supraspinatus tendon.74 Bony irregularity at the site of anchor placement is expected, and echogenic suture material within the tendon may contribute to the heterogeneous appearance of the postoperative rotator cuff tendon (Fig. 24.20, Video 24.4). A gap within the tendon and nonvisualization of the tendon owing to retraction are the most reliable signs for a recurrent tear.75,76 A thinned tendon or one with subtle contour abnormality is considered intact.

Muscle Atrophy Ultrasound may also be used to assess for rotator cuff muscle atrophy, which may occur in the setting of a subacute or chronic rotator cuff tear. This is characterized by decreased muscle bulk and increased muscle echogenicity (related to increased fat interposed among muscle fibers77 (Fig. 24.21). Ultrasound appearances also include lack of clarity of the muscle contour, and loss of visibility of the central tendon within the myotendinous

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Classification of Partial Tears based on depth of defect Articular surface

Bursal surface

Grade 1 10 MHz). Transducers with a small footprint (“hockey stick”) are particularly well suited to superficial injections. These factors should be assessed before skin preparation. The immiscible nature of the steroid anesthetic mixture may likewise produce temporary contrast effect (Fig. 25.2, Video 25.1). In vitro experiments suggest that this property is caused by alterations in acoustic impedance by the scattering material, formed by the suspension of steroid in an aqueous background; this results in an increase in echo intensity of about 20 dB.19 This contrast effect has the advantage of increasing the conspicuity of the delivered agent during real time, enabling the operator to better define the distribution of delivered agent during ultrasoundguided therapy.

INJECTION TECHNIQUE FIG. 25.1  Needle as Specular Reflector With Reverberation Artifact.  A 25-gauge needle (N) has been positioned into the retrocalcaneal bursa deep to the Achilles tendon (T). Note that the needle is a specular reflector with a characteristic reverberation artifact (arrows). BASELINE

We use a sterile technique; the area in question is cleaned with iodine-based solution and draped with a sterile drape. The transducer is cleaned with iodine-based or alcohol-based solutions EARLY

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FIG. 25.2  Contrast Effect.  A suspension of anesthetic and triamcinolone has been injected into a cyst phantom. Baseline: Before injection, anechoic “cyst” is shown in a scattering medium, with baseline pixel intensities listed. Early: The early mixing phase is obtained immediately after injection. A contrast effect is evident, in which the cyst becomes almost isoechoic to the background. Late: 20 minutes after injection. In the late phase, apparent gravitational effect results in settling of the suspension toward the dependent portions of the cyst phantom and development of a contrast gradient.

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FIG. 25.3  Long-Axis Approach: Injection of Left Hip.  The long-axis approach is suitable for deep joint injections, such as the hip or shoulder. (A) Before injection, 22-gauge spinal needle (N) has been positioned at the femoral head-neck junction in a 50-year-old woman with a labral tear demonstrated on magnetic resonance imaging (not shown), to assess relief after therapeutic injection. (B) After injection, confirmation of intraarticular deposition of injected material is obtained by the presence of microbubbles (arrows) deep to the joint capsule. fh, Femoral head; fn, femoral neck. See also Video 25.1. PRE-INJECTION

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FIG. 25.4  Short-Axis Approach for Injection of First Metatarsophalangeal (MTP) Joint.  (A) Long-axis view shows 25-gauge needle positioned in MTP joint of 53-year-old woman with plantar plate injury; needle (N) is seen in cross section. M, Metatarsal head; P, proximal phalanx. (B) While monitoring the injection in real time, the joint capsule distends and fills with echogenic material. C, Capsule.

and surrounded by a sterile drape. A drape is also placed over portions of the ultrasound unit. A sonographer or radiologist positions the transducer; a radiologist positions the needle and performs the procedure. We use 1% lidocaine and bupivacaine (0.25%-0.75%) for local anesthesia. Once the needle is in position, the procedure is undertaken while imaging in real time. Depending on anatomic location, a 1.5-inch or spinal needle with stylet is used to administer the anesthetic-corticosteroid mixture, generally consisting of local long-acting anesthetic and one of the standard injectable corticosteroid derivatives (e.g., triamcinolone). Two approaches to performing injections are long axis and short axis, which relate needle orientation to the structure being injected.9 The long-axis approach refers to needle placement in the plane parallel to the structure of interest (Fig. 25.3). For example, longitudinal imaging of the hip to display a hip effusion might be used as the plane to direct the needle for ultrasoundguided aspiration. Alternatively, the short-axis approach refers to needle entry in the plane perpendicular to the long axis of a structure (Fig. 25.4). For example, injection of the retrocalcaneal bursa or metatarsophalangeal (MTP) joint might use a lateral

approach. In my experience, the short-axis approach works well when performing injections or aspirations in small joints and tendon sheaths of the hand and foot. The long-axis approach appears better suited for deep joint injections, such as in the hip or shoulder. It is important to recognize, however, that such approaches serve merely as guidelines and that no single method necessarily applies to any specific injection.

INJECTION MATERIALS Most injections involve use of a long-acting corticosteroid in combination with a local anesthetic in relatively small volumes. Injectable steroids usually come in either a crystalline form, associated with a slower rate of absorption, or a soluble form, characterized by rapid absorption.20-22 Crystalline agents include triamcinolone and methylprednisolone acetate (Depo-Medrol). A common soluble agent is Celestone, which includes a rapidly absorbed betamethasone salt. A reactive inflammatory response or flushing response may occur with crystalline steroids, but typically not with soluble agents.13

CHAPTER 25  Musculoskeletal Interventions The most significant complications associated with injectable steroid use in the musculoskeletal system relate to chondrolysis (when used in weight-bearing joints), depigmentation, fat necrosis, and impaired healing response (when used in soft tissues).11-14 Impaired healing has been associated with tendon, ligament, and plantar fascia rupture. The most frequently used mixtures contain insoluble particles, so a systemic injection could theoretically result in an “embolic phenomenon,” which has been implicated as a mechanism for neurologic complications associated with transforaminal epidural injections. We have not encountered this as a complication when performing injections in the appendicular skeletal system. The most common anesthetics are lidocaine (Xylocaine) and bupivacaine (Marcaine).22,23 Both are characterized as “local injectable anesthetics” but differ in the onset of effect and duration. Lidocaine is characterized by early onset (seconds) and short duration (1-2 hours). Bupivacaine becomes effective in 5 to 10 minutes, and its effects generally last 4 to 6 hours. In addition to allergic reactions, potential adverse effects include neurotoxicity and cardiotoxicity; these are generally rare when small doses are used under image guidance, taking care to avoid an intravascular injection. Bupivacaine has also been associated with chondrolysis when used for intraarticular applications, but only with constant infusions during arthroscopy and in vitro.24 Chondrolysis is probably not an issue with the small, fixed volumes of bupivacaine typically used during injections in the musculoskeletal system.

INJECTION OF JOINTS A high-frequency linear transducer is used for hand, wrist, elbow, foot, and ankle injections. A short-axis approach is often technically easier for small joint injections. The needle should enter the skin parallel to the plane of the joint space. Superficial joints usually appear as separations between the normally continuous specular echoes produced by cortical surfaces. As in other fluidcontaining structures, the presence of an effusion is a helpful feature in visualizing the needle as it enters the joint, because it provides a fluid standoff. The short-axis approach entails scanning across the joint and looking for the transition from one cortical surface to the next, marking the skin (with a surgical marker), and then placing a needle into the joint using ultrasound guidance. When imaging the joint in long axis, the needle will be seen in cross section (Fig. 25.5). Needle placement is confirmed by injecting a small amount of 1% lidocaine, which should display distention of the joint, as well as echoes filling the joint. Small joint injections generally require 0.5 to 1 mL of the therapeutic mixture. In my experience, this approach works well in the metatarsophalangeal (MTP) or metacarpophalangeal (MCP) and interphalangeal (IP) joints, midfoot, ankle, and elbow. Occasionally a long-axis approach may be efficacious, as in the radiocarpal joint or lateral gutter of the ankle. Ultrasound guidance allows the clinician to negotiate osteophytes and joint bodies. It allows identification of capsular outpouching, thereby affording a more convenient, indirect approach into a joint than slipping a needle into a small joint space.

C

901

N

R CA

L

FIG. 25.5  Long-Axis Approach for Therapeutic Radiocarpal Joint Injection.  A 25-gauge needle (N) has been positioned deep to the dorsal capsule (C) and above the lunate bone (L) of a 19-year-old female patient with chronic wrist pain, to assess relief. CA, Capitate; R, radius.

D N I

G

H

Left shoulder FIG. 25.6  Long-Axis Approach for Glenohumeral Joint Injection.  A 22-gauge needle (N) has been positioned deep to the posterior capsule (arrows) during a glenohumeral joint injection in 42-year-old woman with adhesive capsulitis. Mild fluid distention of the posterior recess of the joint is evident. D, Deltoid muscle; G, glenoid; H, humeral head; I, infraspinatus muscle.

A long-axis approach and a spinal needle are used when performing injections of large joints such as the hip or shoulder (Fig. 25.6). A greater volume is usually injected, typically 5 mL of the steroid-anesthetic mixture. In the case of adhesive capsulitis, significantly larger volumes of local anesthetic (5-10 mL) may be added to provide additional joint distention. We generally approach the glenohumeral joint using a posterior approach, with the patient in a decubitus position and the arm placed in crossadduction. An intermediate-frequency, linear or curvilinear transducer will suffice in most cases. A linear transducer often results in better anatomic detail than curved arrays. The interface of the glenohumeral joint is usually seen with the patient in the decubitus position, as well as the hypoechoic articular cartilage overlying the humeral head. We perform this injection using a long-axis approach, with the needle directed toward the joint along the articular cartilage and deep to the posterior capsule. A test injection with 1% lidocaine should show bright echoes filling the posterior recess or distributed along the articular cartilage. The hip is approached similarly in long axis, with the transducer placed over the proximal anterior thigh at the level of the joint25 (see Fig. 25.3, Video 25.1). The approach is similar to that

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C

A

CL

AC JT FIG. 25.7  Short-Axis Approach to Injection of Acromioclavicular (AC) Joint.  A 25-gauge needle (long thin arrow) is seen in cross section in a distended hypertrophic AC joint during therapeutic injection in 73-year-old woman with pain centered over AC joint. The joint appears widened, containing echogenic material caused by the contrast effect (short thick arrow) of the therapeutic agent. A, Acromion; C, distended capsule; CL, clavicle.

used in evaluating the joint for an effusion. Ideally, the anterior capsule is imaged at the head-neck junction of the femur. In this approach the scan plane is lateral to the neurovascular bundle. The needle may be directed into the joint while maintaining its position in the scan plane of the transducer. A test injection of 1% lidocaine confirms the intraarticular needle position, and the therapeutic injection follows. Fibrous joints, such as the acromioclavicular (AC) joint, can likewise be injected using ultrasound guidance (Fig. 25.7). A short-axis technique is employed similar to that used in the foot. The majority of these injections can be performed using a 1.5-inch needle with a small volume (0.5-1.0 mL) of therapeutic mixture. In addition to the AC joint, this approach is useful in the sternoclavicular joint and pubic symphysis.

SUPERFICIAL PERITENDINOUS AND PERIARTICULAR INJECTIONS Peritendinous injection of anesthetic and long-acting corticosteroid is an effective means to treat tenosynovitis, bursitis, and ganglion cysts in the hand, foot, and ankle. These structures are superficially located and well delineated on sonography. Ultrasound-guided injections are an effective means to ensure correct localization of therapeutic agents.

Foot and Ankle In my experience, peritendinous injections in the foot and ankle are most often requested for patients with chronic achillodynia or those with medial or lateral ankle pain caused by posterior tibial or peroneal tendinosis or tenosynovitis. Less often, patients are referred to help differentiate pain from posterior impingement and stenosing tenosynovitis of the flexor hallucis longus (FHL) tendon.26 This distinction can be difficult, sometimes requiring diagnostic and therapeutic injection of the corresponding tendon sheath. Patients with plantar foot pain caused by plantar fasciitis and forefoot pain resulting from painful neuromas are also frequently referred for ultrasound-guided injections.27,28 The large majority of patients with achillodynia have pain referable to the enthesis, with associated retrocalcaneal bursitis

and Achilles tendinosis. Enthesis is the site of attachment of a muscle or ligament to bone where the collagen fibers are mineralized and integrated into bone. A retrocalcaneal bursal injection may help alleviate local pain and inflammation (Fig. 25.8). I scan the patient in a prone position with the ankle in mild dorsiflexion, using a linear transducer of 10 MHz or higher frequency. A 1.5-inch needle usually suffices in these patients, with placement using a short-axis approach. The deep retrocalcaneal bursa is usually well seen. A small amount of anesthetic will help confirm position by active distention of the bursa in real time. We similarly approach posterior tibial or peroneal tendons in short axis (Fig. 25.9). Patients with pain in this distribution have been shown to benefit from local tendon sheath injections. The presence of preexisting tendon sheath fluid can facilitate needle visualization. However, careful scanning should be done before the procedure to assess the needle trajectory relative to adjacent neurovascular structures. Use of color or power Doppler imaging can facilitate visualization of the neurovascular bundle. The posterior tibial nerve is closely related to adjacent vascular structures and is usually well seen before bifurcating into medial and lateral plantar branches. Fluid frequently is seen in relation to the posterior tibial tendon, in the submalleolar region. The location of the peroneal tendon is less predictable. Use of power Doppler sonography in conjunction with real-time guidance can help localize areas of inflammation for guided injection. In stenosing tenosynovitis the tendons may be surrounded only by a thickened retinaculum, proliferative synovium, or scar tissue. In this case, use of a test injection of local anesthesia can be invaluable to confirm the distribution of the therapeutic agent within the tendon sheath in real time. The flexor hallucis longus (FHL) tendon poses a more challenging problem because of its close relation to the neurovascular bundle of the posterior medial ankle. One helpful feature in performing FHL tendon sheath injections is that tendon sheath effusions tend to localize at the posterior recess of the tibiotalar joint. The neurovascular bundle is easily circumvented by placing the needle lateral to the Achilles tendon while scanning medially (Fig. 25.10). This approach allows flexibility in needle placement while maintaining the needle perpendicular to the insonating beam. Ultrasound diagnosis of plantar fasciitis includes thickening of the medial band of the plantar fascia and fat pad edema. One treatment option for severe plantar fasciitis is regional corticosteroid injection, typically performed using anatomic landmarks. However, “blind” injections into the heel have been associated with rupture of the plantar fascia and failure of the longitudinal arch.13 Ultrasound can be used to guide a needle along the plantar margin of the fascia, thus avoiding direct intrafascial injection.26 The plantar fascia is imaged with the patient prone and the foot mildly dorsiflexed, using a long-axis approach. The transducer is centered over the medial band, which is most often implicated in these patients. A mark is placed over the posterior aspect of the heel and the needle advanced superficial to the plantar fascia, approximately to the margin of the medial tubercle (Fig. 25.11). I perform a perifascial injection using this approach, monitoring the distribution of injected material in real time.

T

T N

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FIG. 25.8  Retrocalcaneal Bursa Injection.  (A) Short-axis view shows Achilles tendon (T) in 59-year-old man with retrocalcaneal pain and history of Haglund deformity. A 25-gauge needle (N) enters perpendicular to the tendon’s long axis and terminates in a small, retrocalcaneal bursal effusion. (B) Rotating transducer 90 degrees results in the more typical short-axis view, with the needle (arrow) seen in cross section. (C) Under observation in real time, the bursa distends (arrows) and fills with echogenic material (contrast effect). The needle is still evident within the distended bursa.

C PRE-INJECTION

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FIG. 25.9  Tendon Sheath Injection Using Short-Axis Approach.  A 17-year-old female patient with medial ankle pain was referred for ultrasound-guided injection of posterior tibial tendon sheath. (A) Preinjection view shows 25-gauge needle (N) within a small tendon sheath effusion (long arrow) in the inframalleolar portion of the tendon (T). The tendon, which is inhomogeneous, is seen in cross section. (B) Postinjection view shows that the tendon sheath is distended, confirming appropriate deposition of the injected material. Note that the tendon margins are better delineated because of a tenosonographic effect of the injected fluid. The vascular pedicle (short arrow) of the tendon is evident. PRE-INJECTION

POST-INJECTION

N TA

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FIG. 25.10  Flexor Hallucis Longus (FHL) Tendon Sheath Injection.  Short-axis approach with ultrasound guidance in 31-year-old professional dancer with posteromedial ankle pain during plantar flexion. (A) Preinjection image depicts the tendon (T) at the level of the posterior sulcus of the talus (TA). The arrows show relationship of the tendon to the neurovascular structures. (B) Postinjection image depicts 25-gauge needle (N) situated within the distended tendon sheath (arrows) below the neurovascular structures.

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Interdigital (Morton) neuromas, a common cause of forefoot pain especially in women, have been described at sonography as hypoechoic masses replacing the normal hyperechoic fat in the interdigital web spaces. Occasionally a dilated hypoechoic tubular structure can be seen associated with the neuroma, reflecting the enlarged feeding interdigital nerve. The second and third web spaces are most often involved. I generally inject Morton neuromas using a dorsal approach while imaging the neuroma in long axis28 (Fig. 25.12). This approach is well tolerated by the majority of patients. In certain patients, however, a plantar approach to injecting the nodule is preferred, such as those with severe subluxation at the MTP joint. In either case, the needle is positioned directly within the neuroma and/or adjacent intermetatarsal bursa (if present) and a small volume of therapeutic mixture injected, similar to that used for a small joint injection (0.5-0.75 mL).

administration of antiinflammatory agents (Fig. 25.13). Injections are also frequently requested for patients with rheumatoid arthritis or psoriatic arthritis. These patients typically experience severe tenosynovitis, which can lead to secondary tendon rupture and deformity. The approach is similar to that used for superficial structures in the foot and ankle. A short-axis approach avoids the surrounding neurovascular structures, and the corresponding tendon sheaths are injected.

Hand and Wrist

Anterior shoulder pain with radiation into the arm may be secondary to bicipital tendinitis or tenosynovitis.29 The biceps tendon can be palpated, but if nondistended, the sheath may offer less than 2 mm of clearance to place a needle. This is complicated by the caudal extension of the subacromial subdeltoid bursa, which may overlie the bicipital tendon sheath. A nonimageguided injection could therefore result in delivery into an extratendinous synovial space, or possibly result in an intratendinous injection. Ultrasound guidance enables localization of therapeutic agent to the biceps tendon sheath.10 The patient is placed recumbent with the forearm supinated and the shoulder mildly elevated. The bicipital groove is oriented anteriorly. A linear transducer, typically 7.5 MHz, is used with a lateral approach and 25- or 22-gauge needle (Fig. 25.14). The long head of the biceps tendon is scanned in short axis. When fluid distends the bicipital tendon sheath, the tip is directed into the fluid. Otherwise, the needle is directed along the superficial margin of the tendon, and a test injection of local anesthetic is used to confirm local distention of the sheath, which is then followed by administration of the long-acting corticosteroid. The

INJECTION OF DEEP TENDONS Frequently requested deep tendon injections include those for the bicipital tendon sheath, iliopsoas tendon, gluteal tendon insertion onto the greater trochanter, and hamstring tendon origin.

Biceps Tendon

In the hand and wrist, de Quervain tendinosis is a frequently encountered tendinopathy involving the abductor pollicis longus and extensor pollicis brevis tendons that respond to local

N

PF calc

FIG. 25.11  Plantar Fascia Injection.  The proximal medial band of the plantar fascia (PF) is thickened and inhomogeneous in a 36-year-old man with hindfoot pain. calc, Calcaneus. A 25-gauge needle (N) has been positioned superficial to this plantar fascia and a perifascial injection performed. The injected material (arrows) loculates along the superficial margin of the medial band.

PRE-INJECTION

POST-INJECTION

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FIG. 25.12  Morton Neuroma Injection.  (A) Preinjection image shows 25-gauge needle (N) positioned in a third web space neuroma using a dorsal approach in 45-year-old woman with forefoot pain. Neuroma appears as a heterogeneous hypoechoic nodule (arrows) within the normal echogenic fat. (B) After injection and needle removal, the nodule appears expanded and echogenic (arrows). The injected material often decompresses into an adjacent adventitial bursa, which frequently accompanies these nodules.

CHAPTER 25  Musculoskeletal Interventions PRE-INJECTION

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POST-INJECTION

N T

ra

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A

FIG. 25.13  Injection of First Dorsal Compartment of Wrist.  This 70-year-old woman with de Quervain tendinosis had clinical symptoms of wrist pain radiating along the extensor surface of the forearm. (A) Preinjection image shows 25-gauge needle (N) positioned in the first dorsal compartment tendon sheath under ultrasound guidance. The tendons (T) are inhomogeneous, with a small effusion evident (arrows) in the dependent part of the tendon sheath. (B) After injection and needle removal, the injected material distends the sheath (arrows), producing a tenosonographic effect; the intrinsic tendon abnormalities become more conspicuous. ra, Radial artery. PRE-INJECTION

POST-INJECTION

N

A

bg

B

bg

FIG. 25.14  Biceps Tendon Sheath Injection.  Biceps tendinosis was clinically suspected and a biceps tendon sheath injection requested for this 41-year-old man with development of anterior shoulder pain after arthroscopic surgery for labral tear. (A) Preinjection image shows 25-gauge needle (N) placed superficial to the long head of the biceps tendon (arrow). (B) After injection and needle removal, there is distention of the tendon sheath by fluid (arrows) containing low-level echoes caused by contrast effect. bg, Bicipital groove.

presence of fluid distention of the sheath with superficially located microbubbles helps to confirm a successful injection. A technique to obviate the need to directly approach the tendon sheath, which can sometimes be challenging in the absence of an effusion, entails direct positioning of the needle within the rotator interval adjacent to the intraarticular portion of the biceps tendon and deep to the biceps pulley mechanism.30 Stone and Adler reported 100% success in distending the sheath in their series.30 Therapeutic mixture was also noted to distribute within the rotator interval (Fig. 25.15, Video 25.2).

Iliopsoas Tendon The iliopsoas tendon lies superficial to and along the medial margin of the anterior capsule of the hip. The tendon inserts onto the lesser trochanter. A bursa that frequently communicates with the hip is present in this location and may be distended because of underling joint pathology or a primary iliopsoas bursitis. Alternatively, iliopsoas tendinosis may occur in the absence of a preexisting bursitis for which a peritendinous injection is requested.31 A lateral approach to the tendon often requires use of a lower-frequency transducer and curved linear

or sector geometry. The neurovascular bundle lies medial and superficial to the tendon, so it is advantageous to approach from the lateral margin of the tendon and perform a small test injection to confirm needle position. A successful injection will show the appearance of fluid or microbubbles distending a bursa that follows the course of the long axis of the tendon (Fig. 25.16).

Abductor and Hamstring Tendons The most commonly requested peritendinous injections in my experience are about the abductor tendon insertion and hamstring tendon origin. In the first two of these injections, the needle is directed to the greater trochanteric bursa. These injections can be fairly straightforward when the bursa is distended. They become more challenging when there is no preexisting bursal distention. One must then employ anatomic landmarks and test injections with anesthetic for localization (Figs. 25.17 and 25.18). Injections at the hamstring origin are generally peritendinous because no true anatomic bursa exists. An adventitial bursa may be present over the ischium. A lateral approach while scanning the tendons in short axis is preferred for each of these injections, directing

A

B

C

D

FIG. 25.15  Biceps Tendon Sheath Injection: Rotator Interval Approach.  A 44-year-old woman with anterior shoulder pain. (A) Gray-scale ultrasound image obtained slightly oblique to the intraarticular biceps tendon (arrow). The greater tuberosity (gt), humeral head (hh), and deltoid (D) are labeled. (B) A 25-gauge needle is positioned using a short-axis lateral approach adjacent to the margin of the biceps tendon within the rotator interval. The tip of the needle is indicated (arrow). A test injection with anesthetic is performed to ensure appropriate needle position. Fluid should not accumulate by the needle tip and the needle position should be adjusted accordingly. (C) Short-axis view of the biceps tendon within the sheath before needle placement and injection. The tendon (arrow) and bicipital groove (BG) are labeled. (D) Postinjection image at approximately the same anatomic level as (C) depicting the distended biceps tendon sheath. See also Video 25.2. PRE-INJECTION

fa

POST-INJECTION

fn N T

e

A

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FIG. 25.16  Ultrasound-Guided Iliopsoas Bursa Injection for Pain Relief.  This 66-year-old woman with a total hip arthroplasty had developed pain with hip flexion. (A) Preinjection image shows 22-gauge spinal needle (N) positioned deep to the tendon (T) at the level of the iliopectineal eminence (e), using a short-axis approach. fa, Femoral artery; fn, femoral nerve. (B) After injection and needle removal, fluid surrounds the tendon within the distended iliopsoas bursa (arrow).

CHAPTER 25  Musculoskeletal Interventions

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FIG. 25.17  Ultrasound-Guided Greater Trochanteric Bursal Injection.  A 53-year-old woman with right lateral hip pain. (A) Axial T2-weighted fat-suppressed image depicts the greater trochanter (GT) and abductor tendon complex (T). The image is oriented similar to the manner in which it would be viewed during an injection with the patient in a lateral decubitus position. A trace amount of T2-bright fluid (arrow) is present in the bursa. (B) A 22-gauge spinal needle (arrow) is positioned near the posterior margin of the greater trochanter, superficial to the gluteus medius tendon and deep to the gluteus maximus. A test injection with local anesthetic helps ensure appropriate needle placement, which is followed by injection of the therapeutic mixture. (C) Short-axis postinjection image at the greater trochanter shows anterior extension of the greater trochanteric bursa (B) at the level of the anterior facet. (D) Postinjection short-axis image centered more posteriorly over the lateral and posterior facets depicts the posterior extension of the bursa (B) abutting the posterior facet of the greater trochanter, also referred to as the “bare area” of the greater trochanter. I usually inject a large volume (10 mL).

the needle toward the posterior facet of the greater trochanter in the case of a trochanteric bursal injection, or adjacent to the margin of the hamstring origin if a peritendinous injection is requested.

BURSAL, GANGLION CYST, AND PARALABRAL INJECTIONS Distended bursae around tendinous insertions provide anatomic localization for therapeutic agents. Injection of these areas is often requested for the patient with localized bursitis and

abnormality of the adjacent tendon. Examples include the retrocalcaneal, iliopsoas, greater trochanteric, and ischial bursae (Fig. 25.19). Alternatively, the presence of a bursitis, distended synovial cyst, or ganglion cyst may cause mechanical impingement of adjacent tendons. The decompression of these cysts with subsequent administration of a therapeutic agent may alleviate these symptoms32 (Fig. 25.20). Ganglion cysts typically contain clear gelatinous material, most often occurring in the hand, wrist, foot, and ankle. Not infrequently they may come in close proximity to neurovascular structures and may extend along nerves as perineural ganglia. This occurs most often in the knee, at the

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FIG. 25.18  Ultrasound-Guided Hamstring Peritendinous Injection.  A 50-year-old female runner with left buttock pain. (A) Axial fat-suppressed T2-weighted sequence positioned in a manner similar to that viewed by a sonographer. The hamstring origin (T) and ischium (I) are labeled. The sciatic nerve (arrow) appears as a mildly hyperintense ellipse lateral to the ischium and superficial to the quadratus femoris. F, Femur. (B) A 22-gauge spinal needle (N) is positioned in short axis, using a lateral approach, adjacent to the margin of the hamstring tendon origin (T). The sciatic nerve (arrow) and ischium (I) are labeled.

nv N

fh

e

B

A

FIG. 25.19  Ultrasound-Guided Aspiration and Injection of Multiloculated Iliopsoas Bursa.  (A) Image shows 22-gauge spinal needle (N) positioned into the lateral component of the bursa in a 65-year-old woman with groin pain. e, Iliopectineal eminence; fh, femoral head. (B) After aspiration of the lateral component, the needle has been advanced into the medial component for aspiration and subsequent injection with therapeutic mixture. nv, Neurovascular structures.

PRE-INJECTION

POST-INJECTION

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mhg

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FIG. 25.20  Ultrasound-Guided Aspiration and Injection of Clinically Suspected Baker Cyst.  (A) Preinjection image shows 22-gauge needle (N) positioned in the cyst (C) under ultrasound guidance in 59-year-old woman with posterior knee pain and swelling. mhg, Medial head of gastrocnemius muscle. (B) After cyst aspiration and injection of the therapeutic mixture, the anechoic fluid is replaced by echogenic fluid resulting from contrast effect (arrows).

CHAPTER 25  Musculoskeletal Interventions

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C

FIG. 25.21  Ultrasound-Guided Aspiration and Injection of Multiloculated Ganglion Cyst.  (A) Baseline sonogram shows a multiloculated cyst (c) within the vastus lateralis muscle of the left knee and superficial to the lateral margin of the femur (f) in a 41-year-old woman. (B) A 20-gauge spinal needle (N) was initially positioned into the proximal component of the cyst. (C) Subsequently the needle was redirected into the distal component. Multiple lavages and aspiration enabled complete decompression of the cyst (not shown).

tibiofibular joint.33,34 Ultrasound guidance allows the clinician to avoid intratendinous injections as well as adjacent neurovascular structures. Furthermore, the needle may be redirected as necessary in the presence of a multiloculated cyst (Fig. 25.21). We find that performing a lavage technique similar to that employed in treating calcific tendinosis results in progressive dilution of the cyst contents, thereby permitting complete aspiration. In the upper extremity, where cosmesis may also be an issue, use of a rapidly absorbed corticosteroid may reduce potential complications, such as depigmentation and local atrophy. Similar considerations apply when aspirating and injecting parameniscal and paralabral cysts. These cysts occur at sites of torn and/or degenerated fibrocartilage and are most often present in the knee, hip, and shoulder. These cysts are similar to ganglion cysts in consistency but often contain additional echogenic debris. In the shoulder, paralabral cysts have been associated with development of a compressive neuropathy, because they can occur in close proximity to the suprascapular nerve.35 The approach used in aspirating these cysts is variable, depending on location and orientation, as well as location of adjacent neurovascular structures (Figs. 25.22 and 25.23, Video 25.3).

Calcific Tendinitis The presence of symptomatic intratendinous calcification involves the deposition of calcium hydroxyapatite. This often appears as a nodular echogenic mass within the tendon, which may or may not display posterior acoustic shadowing.36 Although most often affecting the shoulder, this may occur elsewhere in the musculoskeletal system. Ultrasound-guided fragmentation and

lavage, also known as barbotage, has been described as an excellent method to fenestrate the calcification and reduce the level of calcification and to deposit therapeutic agents.37-40 Singleand dual-needle techniques have been described and appear to be comparably effective. I currently use a single-needle technique, with the needle acting as inflow for anesthetic and sterile saline and as an outflow for the calcium solution (Fig. 25.24). The elasticity of the pseudocapsule encasing the calcification is sufficient to decompress the calcific mass in the majority of cases (Video 25.4). After multiple lavages, the needle is used to inject the anesthetic and antiinflammatory mixture. The injected mixture is distributed within the adjacent subdeltoid bursa in most cases. If the calcification is too small or fragmented, precluding lavage and decompression, the single needle is used to fenestrate the calcium deposit, and a peritendinous therapeutic injection has been shown to be effective.

INTRATENDINOUS INJECTIONS: PERCUTANEOUS TENOTOMY Image guidance can be useful for performing percutaneous tenotomy and intratendinous injections with either autologous blood or platelet-rich plasma (PRP).41-45 These methods are associated with secondary release of local growth factors, such as platelet-derived growth factor, which in turn may produce a direct healing response.44 Preliminary data show significant promise in promoting ultrasound-guided tendon repair. “Dry needling” techniques have been employed successfully in patients with lateral epicondylitis refractory to other conservative

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measures.41 Likewise, autologous blood injections and PRP injections have been successfully used in both the elbow and the knee42-44 (Figs. 25.25 and 25.26, Video 25.5). The advantage of performing these injections under ultrasound guidance becomes evident when the clinician wants to generalize such techniques to include tendons close to neurovascular structures, such as the hamstring tendon origin. Newer technology is now available that allows sonographically directed emulsification of focal tendinosis, calcifications, and enthesopathic spurs followed by removal during the course of the procedure.46 The technique employs a coaxial system with a mechanically active hollow tip that disrupts the tissue and is connected to vacuum suction, while the outer tube supplies sterile water to cool the tip and remove debris as part of the suctioned material (Fig. 25.27, Video 25.6). This technique is relatively new, and no definitive long-term trials are available to assess efficacy, but preliminary results appear promising.

FIG. 25.22  Ultrasound-Guided Aspiration of Paralabral Cyst in the Hip.  A 54-year-old woman with left hip pain. (A) Sagittal fluid–sensitive image of the hip showing a multiloculated paralabral cyst (arrow) associated with a tear of the anterior superior labrum (not shown). (B) The same cyst (arrow) shown on ultrasound as a septated hypoechoic collection overlying the anterior joint margin. The acetabulum (a), femoral head (fh), and labrum (L) are labeled. (C) Ultrasoundguided aspiration of the cyst is depicted. A 22-gauge spinal needle (N) is positioned within the cyst (c) for purposes of aspiration and injection. The needle tip is depicted (arrow).

PERINEURAL INJECTIONS Ultrasound has shown promise in evaluating and treating patients with painful lesions of peripheral nerves due to compressive neuropathies, such as in carpal or cubital tunnel syndromes, or in cases of posttraumatic or postsurgical neuromas.35 These injections can include nerve blocks with long-acting anesthetic, therapeutic injections using an injectable steroid, or neurolytic therapy with an agent that promotes cellular death such as absolute ethanol.47,48 A rapidly absorbed injectable steroid, such as dexamethasone, may be preferable for superficial lesion to minimize potential complications, such as depigmentation or atrophy of the subcutaneous fat. A thorough knowledge of the normal sonographic appearances of nerves and their anatomic course is a prerequisite.35,36 In the case of small sensory nerves, which can be difficult to visualize, knowledge of the anatomic relationships of the nerves to adjacent

CHAPTER 25  Musculoskeletal Interventions

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FIG. 25.23  Ultrasound-Guided Paralabral Cyst Aspiration in the Spinoglenoid Notch of the Shoulder. Spinoglenoid Notch Cyst Aspiration.  (A) Axial fatsuppressed proton-density image that has been inverted for purposes of comparison with ultrasound. The cyst (C) is depicted appearing as a homogeneously T2-bright structure. The cyst produces bony remodeling of the adjacent glenoid. (B) Anechoic cyst (C) remodeling the spinoglenoid notch (sgn). The humeral head (hh) is labeled. (C) A 20-gauge spinal needle (arrow) is positioned within the cyst. See also Video 25.3.

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FIG. 25.24  Ultrasound-Guided Aspiration and Injection for Calcific Tendinosis.  (A) Image shows 20-gauge spinal needle (N) positioned into the calcification (arrow) under ultrasound guidance in 42-year-old man with shoulder pain. D, Deltoid; H, humeral head. (B) Series of repeat lavage and aspirations of the calcification are performed, with the calcification eventually largely replaced by fluid contents within the surrounding pseudocapsule of the calcific mass. T, Rotator cuff tendons. Note that the degree of posterior acoustic shadowing has diminished and that the center of the calcification (arrow on A) is partially replaced by fluid. After numerous lavages, the calcification is typically fenestrated, and a therapeutic mixture is injected and often decompresses into the subdeltoid bursa (not shown).

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FIG. 25.25  Ultrasound-Guided Injection of Autologous Blood to Induce Healing Response.  (A) Coronal inversion-recovery magnetic resonance imaging scan of the affected elbow in a 43-year-old man with medial epicondylitis shows increased signal intensity (arrow) of the common flexor tendon mass and adjacent collateral ligament. (B) Long-axis ultrasound image of the tendon (T) and adjacent medial epicondyle (me) shows that tendon is predominantly hypoechoic, reflecting underlying tendinosis. (C) Image shows 22-gauge needle (N) placed within the common flexor tendon mass, for purposes of mechanical fenestration, and injection of 5 mL of autologous blood, obtained from an antecubital vein. Tendon echogenicity (small arrow) is increased by microbubbles within the injected blood.

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FIG. 25.26  Baseline Image Before Autologous Blood Injection.  Common extensor tendon mass (T) in 50-year-old woman with partial tear of the deep portion of the tendon (short arrow, extensor carpi radialis brevis) as it inserts on the medial epicondyle (me); rc, radiocapitellar joint; long arrow, plane of needle entry for percutaneous tenotomy and autologous blood injection. See also Video 25.5.

Ultrasound allows direct targeting of the perineural soft tissue or a neuroma for injection (Fig. 25.28, Video 25.7). The nerve is best approached in short axis, usually with a 1.5-inch 25-gauge needle or occasionally a spinal needle. In the case of a perineural injection, it is helpful to position the needle in close proximity to the nerve, injecting small amounts of anesthetic until a clear-cut fluid plane outlining the epineurium is evident. When this is achieved, the therapeutic mixture can be instilled. The same procedure is used when performing ultrasound-guided neurolytic therapy. I typically inject a mixture of long-acting anesthetic (0.75% bupivacaine) with a total of 0.5 to 1 mL of absolute ethanol for peripheral nerve lesions. In my experience, absolute ethanol may require multiple injections and can produce a marked postinjection inflammatory response that can last for several days. The volume injected can be variable and in general does not exceed 1 mL. Multiple small injections have been advocated to be efficacious for Morton neuromas (0.25-0.5 mL).

CONCLUSION anatomic compartments is of value. Nerves are best visualized in short axis as clusters of hypoechoic fascicles with echogenic septations (internal epineurium), which have a surrounding echogenic epineurial sleeve (external epineurium). An enlarged hypoechoic nerve may indicate neuritis, whereas a focal hypoechoic nodule seen in relationship to the nerve may represent a neuroma in the appropriate clinical setting.

Ultrasound offers distinct advantages in providing guidance for delivery of therapeutic injections. Most important, ultrasound allows the operator to visualize the needle and make adjustments in real time, to ensure that medication is delivered to the appropriate location. Current ultrasound technology provides excellent depiction of relevant musculoskeletal anatomy. The needle has a unique sonographic appearance and can be monitored with

CHAPTER 25  Musculoskeletal Interventions

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FIG. 25.27  Percutaneous Tenotomy Using Tenex Device.  A 47-year-old man with lateral epicondylitis. (A) Coronal fat-suppressed proton-density image depicting a partial torn and degenerated common extensor tendon and radial collateral ligament (arrow). The lateral epicondyle (le) is labeled. (B) The common extensor mechanism (arrow) is shown in long axis. Hypoechoic areas within the tendon represent interstitial tearing. In addition, punctate echogenic foci within the tendon substance are characteristic for dystrophic calcification. The lateral epicondyle (le) is labeled. See also Video 25.6.

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FIG. 25.28  A 58-Year-Old Woman With Postoperative Sural Nerve Entrapment and Neuropathic Pain.  (A) A 1.5-inch 25-gauge needle is positioned adjacent to the outer epineurium of the sural nerve (arrow). (B) Hypoechoic fluid consisting of anesthetic and corticosteroid surrounds the nerve. Ideally, fluid hydrodissection of the epineurial fat from the adjacent perineural soft tissues is achieved. See also Video 25.7.

real-time imaging, as can the steroid-anesthetic mixture. Given these advantages, ultrasound guidance should become the method of choice to perform a large variety of guided musculoskeletal interventions. REFERENCES 1. Christensen RA, Van Sonnenberg E, Casola G, Wittich GR. Interventional ultrasound in the musculoskeletal system. Radiol Clin North Am. 1988;26(1):145-156. 2. Cunnane G, Brophy DP, Gibney RG, FitzGerald O. Diagnosis and treatment of heel pain in chronic inflammatory arthritis using ultrasound. Semin Arthritis Rheum. 1996;25(6):383-389. 3. Brophy DP, Cunnane G, Fitzgerald O, Gibney RG. Technical report: ultrasound guidance for injection of soft tissue lesions around the heel in chronic inflammatory arthritis. Clin Radiol. 1995;50(2):120-122.

4. Cardinal E, Chhem RK, Beauregard CG. Ultrasound-guided interventional procedures in the musculoskeletal system. Radiol Clin North Am. 1998;36(3):597-604. 5. Koski JM. Ultrasound guided injections in rheumatology. J Rheumatol. 2000;27(9):2131-2138. 6. Grassi W, Farina A, Filippucci E, Cervini C. Sonographically guided procedures in rheumatology. Semin Arthritis Rheum. 2001;30(5): 347-353. 7. Sofka CM, Collins AJ, Adler RS. Use of ultrasonographic guidance in interventional musculoskeletal procedures: a review from a single institution. J Ultrasound Med. 2001;20(1):21-26. 8. Sofka CM, Adler RS. Ultrasound-guided interventions in the foot and ankle. Semin Musculoskelet Radiol. 2002;6(2):163-168. 9. Adler RS, Sofka CM. Percutaneous ultrasound-guided injections in the musculoskeletal system. Ultrasound Q. 2003;19(1):3-12. 10. Adler RS, Allen A. Percutaneous ultrasound-guided injections in the shoulder. Tech Shoulder Elbow Surg. 2004;5(2):122-133.

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11. Unverferth LJ, Olix ML. The effect of local steroid injections on tendon. J Sports Med. 1973;1(4):31-37. 12. Ford LT, DeBender J. Tendon rupture after local steroid injection. South Med J. 1979;72(7):827-830. 13. Gottlieb NL, Riskin WG. Complications of local corticosteroid injections. JAMA. 1980;243(15):1547-1548. 14. Oxlund H, Manthorpe R. The biochemical properties of tendon and skin as influenced by long term glucocorticoid treatment and food restriction. Biorheology. 1982;19(5):631-646. 15. Stapczynski JS. Localized depigmentation after steroid injection of a ganglion cyst on the hand. Ann Emerg Med. 1991;20(7):807-809. 16. Shrier I, Matheson GO, Kohl 3rd HW. Achilles tendonitis: are corticosteroid injections useful or harmful? Clin J Sport Med. 1996;6(4):245-250. 17. Bouffard JA, Eyler WR, Introcaso JH, van Holsbeeck M. Sonography of tendons. Ultrasound Q. 1993;11:259-286. 18. Koski JM, Saarakkala SJ, Heikkinen JO, Hermunen HS. Use of air-steroidsaline mixture as contrast medium in greyscale ultrasound imaging: experimental study and practical applications in rheumatology. Clin Exp Rheumatol. 2005;23(3):373-378. 19. Luchs JS, Sofka CM, Adler RS. Sonographic contrast effect of combined steroid and anesthetic injections: in vitro analysis. J Ultrasound Med. 2007;26(2):227-231. 20. Curatolo M, Bogduk N. Pharmacologic pain treatment of musculoskeletal disorders: current perspectives and future prospects. Clin J Pain. 2001;17(1):25-32. 21. Caldwell JR. Intra-articular corticosteroids. Guide to selection and indications for use. Drugs. 1996;52(4):507-514. 22. Kannus P, Jarvinen M, Niittymaki S. Long- or short-acting anesthetic with corticosteroid in local injections of overuse injuries? A prospective, randomized, double-blind study. Int J Sports Med. 1990;11(5):397-400. 23. Cox B, Durieux ME, Marcus MA. Toxicity of local anaesthetics. Best Pract Res Clin Anaesthesiol. 2003;17(1):111-136. 24. Gomoll AH, Kang RW, Williams JM, et al. Chondrolysis after continuous intra-articular bupivacaine infusion: an experimental model investigating chondrotoxicity in the rabbit shoulder. Arthroscopy. 2006;22: 813-819. 25. Sofka CM, Saboeiro G, Adler RS. Ultrasound-guided adult hip injections. J Vasc Interv Radiol. 2005;16(8):1121-1123. 26. Mehdizade A, Adler RS. Sonographically guided flexor hallucis longus tendon sheath injection. J Ultrasound Med. 2007;26(2):233-237. 27. Tsai WC, Wang CL, Tang FT, et al. Treatment of proximal plantar fasciitis with ultrasound-guided steroid injection. Arch Phys Med Rehabil. 2000;81(10):1416-1421. 28. Sofka CM, Adler RS, Ciavarra GA, Pavlov H. Ultrasound-guided interdigital neuroma injections: short-term clinical outcomes after a single percutaneous injection—preliminary results. HSS J. 2007;3:44-49. 29. Middleton WD, Reinus WR, Totty WG, et al. US of the biceps tendon apparatus. Radiology. 1985;157(1):211-215.

30. Stone TJ, Adler RS. Ultrasound-guided biceps peritendinous injections in the absence of a distended tendon sheath: a novel rotator interval approach. J Ultrasound Med. 2015;34(12):2287-2292. 31. Adler RS, Buly R, Ambrose R, Sculco T. Diagnostic and therapeutic use of sonography-guided iliopsoas peritendinous injections. Am J Roentgenol. 2005;185(4):940-943. 32. Breidahl WH, Adler RS. Ultrasound-guided injection of ganglia with corticosteroids. Skeletal Radiol. 1996;25(7):635-638. 33. Martinoli C, Bianchi S, Derchi LE. Tendon and nerve sonography. Radiol Clin North Am. 1999;37(4):691-711, viii. 34. Bianchi S. Ultrasound of the peripheral nerves. Joint Bone Spine. 2008;75(6):643-649. 35. Tung GA, Entzian D, Stern JB, Green A. MR imaging and MR arthrography of paraglenoid labral cysts. AJR Am J Roentgenol. 2000;174(6): 1707-1715. 36. Farin PU, Jaroma H. Sonographic findings of rotator cuff calcifications. J Ultrasound Med. 1995;14(1):7-14. 37. Farin PU, Jaroma H, Soimakallio S. Rotator cuff calcifications: treatment with US-guided technique. Radiology. 1995;195(3):841-843. 38. Farin PU, Rasanen H, Jaroma H, Harju A. Rotator cuff calcifications: treatment with ultrasound-guided percutaneous needle aspiration and lavage. Skeletal Radiol. 1996;25(6):551-554. 39. Aina R, Cardinal E, Bureau NJ, et al. Calcific shoulder tendinitis: treatment with modified US-guided fine-needle technique. Radiology. 2001;221(2): 455-461. 40. Lin JT, Adler RS, Bracilovic A, et al. Clinical outcomes of ultrasound-guided aspiration and lavage in calcific tendinosis of the shoulder. HSS J. 2007;3(1): 99-105. 41. McShane JM, Nazarian LN, Harwood MI. Sonographically guided percutaneous needle tenotomy for treatment of common extensor tendinosis in the elbow. J Ultrasound Med. 2006;25(10):1281-1289. 42. James SL, Ali K, Pocock C, et al. Ultrasound guided dry needling and autologous blood injection for patellar tendinosis. Br J Sports Med. 2007;41(8):518-521. 43. Connell DA, Ali KE, Ahmad M, et al. Ultrasound-guided autologous blood injection for tennis elbow. Skeletal Radiol. 2006;35(6):371-377. 44. Mishra A, Pavelko T. Treatment of chronic elbow tendinosis with buffered platelet-rich plasma. Am J Sports Med. 2006;34(11):1774-1778. 45. Gamradt SC, Rodeo SC, Warren RF. Platelet-rich plasma in rotator cuff repair. Tech Orthop. 2007;22:26-33. 46. Barnes D. Ultrasonic energy in tendon treatment. Oper Tech Orthop. 2013;23(2):78-83. 47. Tagliafico A, Serafini G, Lacelli F, et al. Ultrasound-guided treatment of meralgia paresthetica (lateral femoral cutaneous neuropathy): technical description and results of treatment in 20 consecutive patients. J Ultrasound Med. 2011;30(10):1341-1346. 48. Lee J, Lee YS. Percutaneous chemical nerve block with ultrasound-guided intraneural injection. Eur Radiol. 2008;18(7):1506-1512.

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26

 

The Extracranial Cerebral Vessels Edward I. Bluth, Stephen I. Johnson, and Laurie Troxclair

SUMMARY OF KEY POINTS • The combination of gray-scale, color-flow Doppler, and Doppler spectral analysis is highly accurate in determining plaque characterization and degree of carotid stenosis. • Accurate diagnosis of carotid stenosis is critical for patients who would benefit from surgical and interventional treatment. • Clinicians can accurately follow changes in noncritical carotid stenosis or plaque using ultrasound. • The assessment of the vertebral arteries is an integral component of the carotid ultrasound examination. However, the degree of stenosis of the vertebral arteries cannot be accurately assessed.

• Carotid atherosclerotic plaque with resultant stenosis usually involves the internal carotid artery within 2 cm of the carotid bifurcation. • Homogenous plaque, which is stable, has uniform echo pattern with a smooth surface. The amount of sonolucency is less than 50%. • Heterogeneous plaque, which can be unstable, has a more complex echo pattern with sonolucent areas of more than 50%. • Either the consensus table by the Society of Radiologists in Ultrasound or other standard reporting tables and criteria can be used to grade carotid stenosis as long as there is appropriate quality outcome feedback for accuracy.

CHAPTER OUTLINE INTRODUCTION: INDICATIONS FOR CAROTID ULTRASOUND EXAMINATION CAROTID ARTERY ANATOMY CAROTID ULTRASOUND EXAMINATION CAROTID ULTRASOUND INTERPRETATION Visual Inspection of Gray-Scale Images Vessel Wall Thickness and IntimaMedia Thickening Plaque Characterization Ultrasound Plaque Classification System Plaque Ulceration Gray-Scale Evaluation of Stenosis Doppler Spectral Analysis Standard Examination

Spectral Broadening Pitfalls in Interpretation High-Velocity Blood Flow Patterns Color Doppler Ultrasound Optimal Settings for Low-Flow Vessel Evaluation Advantages and Pitfalls Power Doppler Ultrasound Pitfalls and Adjustments Internal Carotid Artery Occlusion Follow-Up of Stenosis Preoperative Strategies for Patients With Carotid Artery Disease Postoperative Ultrasound Carotid Artery Stents and Revascularization Grading Carotid Intrastent Restenosis

INTRODUCTION: INDICATIONS FOR CAROTID ULTRASOUND EXAMINATION Stroke secondary to atherosclerotic disease is the third leading cause of death in the United States. Many stroke victims survive the catastrophic event with some degree of neurologic impairment depending on collateral flow.1,2 Annually, stroke kills more than

NONATHEROSCLEROTIC CAROTID DISEASE Pulsatile Neck Masses in the Carotid Region TRANSCRANIAL DOPPLER SONOGRAPHY VERTEBRAL ARTERY Anatomy Sonographic Technique and Normal Examination Subclavian Steal Stenosis and Occlusion INTERNAL JUGULAR VEINS Sonographic Technique Thrombosis Acknowledgment

130,000 people in the United States with an incidence of more than 795,000 cases of cerebrovascular accident (CVA).3,4 Ischemia from severe, flow-limiting stenosis caused by atherosclerotic disease involving the extracranial carotid arteries is implicated in 20% to 30% of strokes with a decreasing incidence due to improved control of hypertension and hyperlipidemia with medications.3,5 An estimated 80% of CVAs are thromboembolic in origin, often with carotid plaque as the embolic source.6 Cardioembolic stroke carries a higher risk of death, recurrent

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stroke, hospital readmission, and severe disability than other types of stroke.6 Carotid atherosclerotic plaque with resultant stenosis usually involves the internal carotid artery (ICA) within 2 cm of the carotid bifurcation. This location is readily amenable to examination by sonography as well as surgical intervention. Carotid endarterectomy (CEA) initially proved to be more beneficial than medical therapy in symptomatic patients with carotid stenoses of more than 70%, as reported in the North American Symptomatic Carotid Endarterectomy Trial (NASCET) and the European Carotid Surgery Trial (ECST).7,8 Subsequent NASCET results for moderate stenoses have shown a net benefit for surgical intervention with carotid narrowing between 50% and 69% of vessel diameter. A 15.7% reduction in the 5-year ipsilateral stroke rate was seen in patients treated surgically versus 22.2% stroke reduction in those treated medically. These results are not as compelling as those for the higher degree of stenosis seen in the earlier NASCET trial. The benefit from surgery was greatest in men, patients with recent stroke, and those with hemispheric symptoms. In addition, the NASCET trials dealing with moderate carotid stenoses required rigorous surgical expertise, such that the risks for disabling stroke or death should not exceed 2% to achieve the statistical surgical benefit.9 The Asymptomatic Carotid Atherosclerosis Study (ACAS) trials published in 1995 reported a reduction in ipsilateral stroke in asymptomatic patients with greater than 60% ICA stenoses who undergo CEA.3 However, these results were less clear-cut than the NASCET trials. According to the Carotid Revascularization Endarterectomy Versus Stenting Trial (CREST), carotid artery stenting has been shown to be comparable to CEA with respect to rates of ipsilateral stroke and death. However, there are increased adverse effects in women and elevated stroke rates and deaths in older patients.10 With implementation of new medical management regimens—including aspirin, clopidogrel, statins, antihypertensive medications, diabetic management, smoking cessation, and lifestyle changes—future trials may change how carotid disease is treated.10 Accurate diagnosis of carotid stenosis clearly is critical to identify patients who would benefit from surgical treatment. In addition, ultrasound can assess plaque morphology, such as determining heterogeneous or homogeneous plaque, known to be an independent risk factor for stroke and transient ischemic attack (TIA). Carotid sonography is the principal screening method for suspected extracranial carotid atherosclerotic disease. Gray-scale examination, color Doppler, power Doppler, and pulsed Doppler imaging techniques are routinely employed in the evaluation of patients with neurologic symptoms and suspected extracranial cerebral disease.11,12 Ultrasound is an inexpensive, noninvasive, and highly accurate method of diagnosing carotid stenosis. Magnetic resonance angiography (MRA) and computed tomography angiography (CTA) are additional noninvasive screening tools for the identification of carotid bifurcation disease as well as for clarification of ultrasound findings. Angiography is often now reserved for those patients for whom the ultrasound or MRA was equivocal or inadequate.

Other carotid ultrasound applications include the evaluation of carotid bruits, monitoring the progression of known atherosclerotic disease,11,13,14 assessment during or after CEA or stent placement,15 screening before major vascular surgery, and evaluation after the detection of retinal cholesterol emboli.11 Also, nonatherosclerotic carotid diseases can be evaluated, including follow-up of carotid dissection,16-21 examination of fibromuscular dysplasia or Takayasu arteritis,22-24 assessment of malignant carotid artery invasion,25,26 and workup of pulsatile neck masses and carotid body tumors.27-29

Indications for Carotid Ultrasound Evaluation of patients with hemispheric neurologic symptoms, including stroke, transient ischemic attack, and amaurosis fugax Evaluation of patients with a carotid bruit Evaluation of pulsatile neck masses Evaluation of patients scheduled for major cardiovascular surgical procedures Evaluation of nonhemispheric or unexplained neurologic symptoms Follow-up of patients with proven carotid disease Evaluation of patients after carotid revascularization, including stenting Intraoperative monitoring of vascular surgery Evaluation of suspected subclavian steal syndrome Evaluation of a potential source of retinal emboli Follow-up of carotid dissection Follow-up of radiation therapy to the neck in select patients

CAROTID ARTERY ANATOMY The first major branch of the aortic arch is the innominate or brachiocephalic artery, which divides into the right subclavian artery and right common carotid artery (CCA). The second major branch is the left CCA, which is generally separate from the third major branch, the left subclavian artery (Fig. 26.1). The right and left CCAs ascend into the neck posterolateral to the thyroid gland and lie deep to the jugular vein and sternocleidomastoid muscle. The CCAs have different proximal configurations, with the right originating at the bifurcation of the innominate (brachiocephalic) artery into the common carotid and subclavian arteries. The left CCA usually originates directly from the aortic arch but often arises with the brachiocephalic trunk. This is known as a “bovine arch” configuration. The CCA usually has no branches in its cervical region. Occasionally, however, it may give off the superior thyroid artery, vertebral artery, ascending pharyngeal artery, and occipital or inferior thyroid artery. At the carotid bifurcation, the CCA divides into the external carotid artery (ECA) and the internal carotid artery (ICA). The ICA usually has no branching vessels in the neck. The ECA, which supplies the facial musculature, has multiple branches in the neck. The ICA may demonstrate an ampullary region of mild dilation just beyond its origin.

CHAPTER 26  The Extracranial Cerebral Vessels

CAROTID ULTRASOUND EXAMINATION Carotid artery ultrasound examinations are performed with the patient supine, the neck slightly extended, and the head turned away from the side being examined. Some operators prefer to perform the examination at the patient’s side, whereas others prefer to sit at the patient’s head. The examination sequence also varies with operator preference. This sequence includes the gray-scale examination, Doppler spectral analysis, and color

E

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FIG. 26.1  Branches of Aortic Arch and Extracranial Cerebral Arteries.  A, Aortic arch; C, common carotid artery; E, external carotid artery; I, internal carotid artery; In, innominate artery; L, left side; R, right side; S, subclavian artery; V, vertebral artery.

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Doppler blood flow interrogations. Power Doppler sonography may or may not be employed. A 5- to 12-MHz transducer is used for gray-scale imaging and a 3- to 7-MHz transducer for Doppler sonography; the choice depends on the patient’s body habitus and technical characteristics of the ultrasound machine. Color Doppler flow imaging and power Doppler imaging may be performed with 5- to 10-MHz transducers. In cases of critical stenosis, the Doppler parameters should be optimized to detect extremely slow flow. Gray-scale sonographic examination begins in the transverse projection. Scans are obtained along the entire course of the cervical carotid artery, from the supraclavicular notch cephalad to the angle of the mandible (Fig. 26.2). Inferior angulation of the transducer in the supraclavicular area images the CCA origin. The left CCA origin is deeper and more difficult to image consistently than the right. The carotid bulb is identified as a mild widening of the CCA near the bifurcation. Transverse views of the carotid bifurcation establish the orientation of the external and internal carotid arteries and help define the optimal longitudinal plane in which to perform Doppler spectral analysis (Video 26.1). When the transverse ultrasound images demonstrate occlusive atherosclerotic disease, the percentage of “diameter stenosis” or “area stenosis” can be calculated directly using electronic calipers and software analytic algorithms available on most duplex equipment. After transverse imaging, longitudinal scans of the carotid artery are obtained. The examination plane necessary for optimal longitudinal scans is determined by the course of the vessels demonstrated on the transverse study. In some patients, the optimal longitudinal orientation will be nearly coronal, whereas in others it will be almost sagittal. In most cases, the optimal longitudinal scan plane will be oblique, between sagittal and coronal. In approximately 60% of patients, both vessels above the carotid bifurcation and the CCA can be imaged in the same plane (Fig. 26.3); in the remainder, only a single vessel will be imaged in the same plane as the CCA. Images are obtained to display the relationship of both branches of the carotid bifurcation to the visualized plaque disease, and the cephalocaudal extent

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FIG. 26.2  Carotid Sonographic Anatomy.  (A) Transverse image of the left internal carotid artery (I) and external carotid artery (E). The internal carotid artery is lateral and larger in relation to the external carotid artery. (B) Color Doppler image of the left internal carotid artery (I) and the external carotid artery (E). Note normal color-flow separation in the internal carotid artery.

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of the plaque is measured. Several anatomic features differentiate the ICA from the ECA. In about 95% of patients, the ICA is posterior and lateral to the ECA. This may vary considerably, and the ICA may be medial to the ECA in 3% to 9% of people.15 The ICA frequently has an ampullary region of dilation just beyond its origin and is usually larger than the ECA. One reliable distinguishing feature of the ECA is that it has branching vessels (Fig. 26.4A). A useful method to identify the ECA is the tapping of the ipsilateral superficial temporal artery in the preauricular area, the temporal tap. The pulsations are transmitted back to the ECA where they cause a sawtooth appearance on the spectral waveform (Fig. 26.4B). Although the tap helps identify the ECA, this tap deflection may be transmitted into the CCA and even the ICA in certain rare situations. The superior thyroid artery is often seen as the first branch of the ECA after the bifurcation of the CCA. Occasionally, an aberrant superior thyroid artery branch will arise from the distal CCA. The ICA usually has no branches in the neck, although

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FIG. 26.3  Carotid Bifurcation.  Longitudinal image demonstrates common carotid artery (C); external carotid artery (E); and large, posterior internal carotid artery (I).

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in rare cases the ICA gives rise to the ascending pharyngeal, occipital, facial, laryngeal, or meningeal arteries. In some patients, a considerable amount of the ICA will be visible, but in others, only the immediate origin of the vessel will be accessible. Very rarely, the bifurcation may not be visible at all.28 Rarely, the ICA may be hypoplastic or congenitally absent.30,31

CAROTID ULTRASOUND INTERPRETATION Each facet of the carotid sonographic examination is valuable in the final determination of the presence and extent of disease. In most cases, the gray-scale, color Doppler, and power Doppler sonographic images and assessments will agree. However, when there are discrepancies between Doppler ultrasound imaging findings and measured velocities, every attempt should be made to discover the source of the disagreement. The more closely the image and spectral Doppler findings correlate, the higher the degree of confidence in the diagnosis. Generally, gray-scale and color or power Doppler images better demonstrate and quantify low-grade stenoses, whereas high-grade occlusive disease is more accurately defined by Doppler spectral analysis. For plaque characterization, assessment must be made in gray-scale only, without color or power Doppler ultrasound.

Visual Inspection of Gray-Scale Images Vessel Wall Thickness and Intima-Media Thickening Longitudinal views of the layers of the normal carotid wall demonstrate two nearly parallel echogenic lines, separated by a hypoechoic to anechoic region (Fig. 26.5). The first echo, bordering the vessel lumen, represents the lumen-intima interface; the second echo is caused by the media-adventitia interface. The media is the anechoic/hypoechoic zone between the echogenic lines. The distance between these lines represents the combined thickness of the intima and media (I-M complex). The far wall of the CCA is measured. Many consider measurement of

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FIG. 26.4  Normal External Carotid Artery (ECA).  (A) Color Doppler ultrasound of bifurcation demonstrates two small arteries originating from the ECA. (B) ECA spectral Doppler shows the reflected temporal tap (TT) as a serrated (sawtooth) flow disturbance.

CHAPTER 26  The Extracranial Cerebral Vessels intima-media thickness (IMT) to be a surrogate marker for atherosclerotic disease in the whole arterial system, not only the cerebrovascular system.32,33 Some believe that thickening of the I-M complex greater than 0.8 mm is abnormal and may represent the earliest changes of atherosclerotic disease. However, because thickness of the I-M increases with age, absolute measurements of IMT for any given person may not be a reliable indicator of atherosclerotic risk factors34 (Fig. 26.6). Carotid artery IMT is an independent predictor of new cardiovascular events in persons without a history of cardiovascular disease.35 Numerous studies support the relationship between IMT and increased risk for myocardial infarction

FIG. 26.5  Normal Intima-Media (I-M) Complex of Common Carotid Artery.  The I-M complex (arrows) is seen in a left common carotid artery.

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or stroke in asymptomatic patient populations.19,36-43 Assessment of IMT has been advocated as a means of assessing effectiveness of medical interventions to reduce the progression of I-M thickening or even reverse carotid wall thickening. However, because of concerns regarding minimal impact on prediction models and difficulty in standardizing measurement technique, the 2013 American College of Cardiology/American Heart Association (ACC/AHA) Guideline on the Assessment of Cardiovascular Risk does not recommend the carotid IMT test.44

Plaque Characterization Atheromatous carotid plaques should be carefully evaluated to determine plaque extent, location, surface contour, and texture, as well as to assess luminal stenosis.45 The plaque should be scanned and evaluated in both the sagittal and the transverse projections.46 The most common cause of TIAs is embolism, not flow-limiting stenosis; less than half of patients with documented TIA have hemodynamically significant stenosis. It is important to identify low-grade atherosclerotic lesions that may contain hemorrhage or ulceration, which can serve as a nidus for emboli that cause both TIAs and stroke.1 Polak et al.47 showed that plaque is an independent risk factor for developing a stroke. Of patients with hemispheric stroke symptoms, 50% to 70% demonstrate hemorrhagic or ulcerated plaque. Plaque analysis of CEA specimens has implicated intraplaque hemorrhage as an important factor in the development of neurologic symptoms.48-55 However, the relationship between sonographic plaque morphology and the onset of symptoms is controversial. Currently, substantial gaps in knowledge of the mechanisms involved in atherosclerotic plaque rupture exist and this is a critical barrier to developing methodologies for the prevention of myocardial infarction and stroke. Myocardial infarction and stroke, complications of atherosclerosis, are the most common causes of death in developed countries and are caused by inflammation-driven rupture of atherosclerotic plaques. Stable plaques are characterized by a necrotic core with an overlying fibrous cap composed of vascular smooth muscle cells in a

B

FIG. 26.6  Abnormal Intima-Media (I-M) Complex of Common Carotid Artery (CCA).  (A) Early I-M hyperplasia with loss of the hypoechoic component of the I-M complex and thickening (arrows). (B) Thickening of the I-M complex with hyperplasia (arrows).

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collagen-rich matrix.56,57 In vulnerable/ruptured plaques, the fibrous cap has thinned, exhibiting fewer vascular smooth muscle cells, decreased collagen, and increased inflammatory cells. Heterogeneous plaque has been suggested as unstable and vulnerable, in contrast to homogeneous plaque. Some have suggested that environmental factors and toxins cause abnormal flow patterns, damaging the internal structure of the vessels.58 This can lead to intimal proliferation and potential wall ischemia and the degradation of the vasa vasorum.58 Because the vasa vasorum do not have a muscular media, these vessels are subsequently at risk to rupture, perhaps leading, in part, to intraplaque hemorrhage.58 Others have suggested that a bacterial infection etiology may play a role in inflammatory angiogenesis.58 Recently, several groups have demonstrated that microRNAs play a key role in the development and thinning of the fibrous cap.59-69 MicroRNAs are a class of noncoding RNAs (ncRNAs) that are approximately 21 nucleotides in length and are potent

effectors of gene expression, doing so by binding to messenger RNA and inhibiting protein translation. A role for ncRNA in cardiovascular diseases is emerging, including microRNAs (miRNAs) and their inhibition by circular RNA (circRNAs). MicroRNA-221 and microRNA-222 (miR-221/miR-222) are short ncRNAs that inhibit the expression of the cyclin-dependent kinase inhibitor p27Kip1, promoting vascular smooth muscle cell proliferation and intimal thickening. Bazan et al. recently demonstrated an important role for the downregulation of miR-221/222 in the shoulder region of carotid plaques shortly after rupture70 through increased p27Kip1 and propose that vascular smooth muscle cell volume is lost, leading to intimal thinning.

Ultrasound Plaque Classification System Plaque texture is generally classified as homogeneous or heterogeneous.14,38,41,45,46,48-50,71-75 The accurate evaluation of plaque can only be made with gray-scale ultrasound, without the use of

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FIG. 26.7  Spectrum of Patterns of Homogeneous Plaque.  (A) Sagittal and (B) transverse images show homogeneous plaque in left common carotid artery (type 4). Note the uniform echo texture. (C) Sagittal and (D) transverse images show homogeneous plaque in proximal left internal carotid artery (type 3). Note the focal hypoechoic area within the plaque, estimated at less than 50% of plaque volume.

CHAPTER 26  The Extracranial Cerebral Vessels

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FIG. 26.7, cont’d (E) Sagittal and (F) transverse images demonstrate homogeneous plaque (type 3). Associated calcifications best seen on image E obscure uniformity of plaque. (G) Sagittal and (H) transverse images demonstrate homogeneous plaque (type 3) in the carotid bifurcation. The sonolucent areas are less than 50% of the volume of the plaque.

color or power Doppler. The plaque must be evaluated in both sagittal and transverse planes.46 Homogeneous plaque has a generally uniform echo pattern and a smooth surface (Fig. 26.7). Sonolucent areas may be seen, but the amount of sonolucency is less than 50% of the plaque volume. The uniform acoustic texture corresponds pathologically to dense fibrous connective tissue (Videos 26.2 through 26.4). Calcified plaque produces posterior acoustic shadowing and is common in asymptomatic individuals (Fig. 26.8, Video 26.5). Heterogeneous plaque has a more complex echo pattern and contains one or more focal sonolucent areas corresponding to more than 50% of the plaque volume (Fig. 26.9, Videos 26.6 through 26.11). Heterogeneous plaque is characterized pathologically by containing intraplaque hemorrhage and deposits of lipid, cholesterol, and proteinaceous material.15,73 Homogeneous plaque is identified much more often than heterogeneous plaque, occurring in 80% to 85% of patients examined.47 Sonography accurately determines the presence or absence of intraplaque hemorrhage (sensitivity, 90%-94%; specificity, 75%-88%).48,54,73,76-80 Some sources suggest classifying plaque according to four types. Plaque types 1 and 2, similar to heterogeneous plaque and much more likely to be associated with intraplaque hemorrhage and ulceration, are considered unstable and subject to abrupt increases in plaque size after hemorrhage or embolization.14,46,74,81-84 Types 1 and 2 plaque are typically found in

FIG. 26.8  Calcified Plaque.  The calcified plaque creates a shadow that obscures characterization of plaque in the left internal carotid artery.

symptomatic patients with stenoses greater than 70% of diameter. Plaque types 3 and 4 are generally composed of fibrous tissue and calcification. These plaque types are similar to homogeneous plaque. These are generally more benign, stable plaques typically seen in asymptomatic individuals (see Fig. 26.8).

922

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Small Parts, Carotid Artery, and Peripheral Vessel Sonography

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FIG. 26.9  Spectrum of Patterns of Heterogeneous Plaque in the Internal Carotid Artery (ICA).  (A) Sagittal and (B) transverse images show plaque (arrows) virtually completely sonolucent, consistent with heterogeneous plaque (type 1). Note smooth plaque surface. (C) Sagittal and (D) transverse images show focal sonolucent areas within the plaque greater than 50% of plaque volume, corresponding to heterogeneous plaque (type 2). Note the irregular surface of the plaque. (E) Sagittal image demonstrates heterogeneous plaque in the carotid bulb and homogeneous plaque in the internal carotid artery (type 2). (F) Transverse image demonstrates heterogeneous plaque (type 2). (G) and (H) Sagittal and transverse images demonstrate subtle heterogeneous plaque (type 2).

Ultrasound Types of Plaque Morphology Type 1: Predominantly echolucent, with a thin echogenic cap Type 2: Substantially echolucent with small areas of echogenicity (>50% sonolucent) Type 3: Predominantly echogenic with small areas of echolucency (95%), the velocity measurements may actually decrease, and the waveform becomes dampened.99,108

CHAPTER 26  The Extracranial Cerebral Vessels

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FIG. 26.20  Internal Carotid Artery (ICA) Stenosis.  (A) ICA stenosis of 50% to 69% diameter shows a peak systolic velocity (PSV) of 187 cm/ sec. (B) Left ICA demonstrates a visible high-grade stenosis on color Doppler with end diastolic velocities (EDVs) of greater than 180 cm/sec and PSVs that alias at greater than 350 cm/sec. This is consistent with a very high-grade stenosis. (C) Right carotid bulb seen in longitudinal projection with color Doppler demonstrates a high-grade narrowing and spectral broadening with an approximately 500 cm/sec velocity in peak systole and 250 cm/sec in end diastole, consistent with an 80% to 95% stenosis. (D) and (E) Power transverse and long images demonstrate high-grade stenosis of the ICA.

In these cases, correlation with color or power Doppler imaging is essential to diagnose correctly the severity of the stenoses. Velocity increases are focal and most pronounced in and immediately distal to a stenosis, emphasizing the importance of sampling directly in these regions. Moving further distal from a stenosis, flow begins to reconstitute and assume a more normal pattern, provided a tandem lesion does not exist distal to the initial site of stenosis. Spectral broadening results in the jets of high-velocity flow associated with carotid stenosis; however, correlation with gray-scale and color Doppler images can define other causes of spectral broadening. An awareness of normal flow spectra combined with appropriate Doppler techniques can obviate many potential diagnostic pitfalls. The degree of carotid stenosis that is considered clinically significant in the symptomatic or asymptomatic patient is in evolution. Initially, it was thought that lesions causing 50% diameter stenosis were significant; this perception changed as more information was gathered from two large clinical trials. As noted earlier, NASCET demonstrated that CEA was more beneficial than medical therapy in symptomatic patients with 70% to 99% ICA stenosis.7 ECST demonstrated a CEA benefit when the degree of stenosis was greater than 60%.8 Interestingly, the method used to grade stenoses in the ECST study was

substantially different than that used in the NASCET trials. The NASCET trials compared the severity of the ICA stenosis on arteriogram with the residual lumen of a presumably more normal distal ICA. The ECST methodology entailed assessment of the severity of stenosis with a “guesstimation” of the lumen of the carotid artery at the level of the stenosis. The ECST assessment is more comparable to ultrasound’s visible assessment of the degree of narrowing, whereas velocity tables currently in use have been derived to correspond to the NASCET angiographic determinations for stenosis. The ECST method for grading carotid artery stenosis tends to give a more severe assessment of narrowing than the NASCET technique (Fig. 26.21). The initial NASCET trials retrospectively compared velocity data obtained on the Doppler examination with angiographic measurements of stenosis. No standardized ultrasound protocol was employed by the numerous centers involved in the trials. Despite the lack of uniformity, moderate sensitivity and specificity ranging from 65% to 77% were obtained for grading ICA stenoses using Doppler velocities. If ultrasound technique is standardized and criteria are validated in a given laboratory, peak systolic velocity (PSV) and peak systolic ratios have proved to be an accurate method for determining carotid stenosis.109 The ECST group compared three different angiographic measurement

930

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PART III ICA C B

ECA

A

Measurement Methodology ECST =

B–A

x 100

B NASCET = 1– ACAS

A

x 100

C

CCA FIG. 26.21  Comparative Measurement Methodology.  Different methodologies for grading internal carotid artery stenoses, from the North American Symptomatic Carotid Endarterectomy Trial (NASCET), Asymptomatic Carotid Atherosclerosis Study (ACAS), and European Carotid Surgery Trial (ECST). CCA, Common carotid artery; ECA, external carotid artery; ICA, internal carotid artery.

techniques: the NASCET, the ECST, and a technique comparing distal CCA measurements with those of ICA stenosis. Researchers concluded that the ECST and NASCET techniques were similar in their prognostic value, whereas the CCA/stenosis measurement was the most reproducible of the three techniques. They also concluded that the CCA method, although reproducible, would be invalidated by the presence of CCA disease.110 Virtually all investigators advocate using the NASCET angiographic measurement technique. The results of these trials, as well as the more recent ACAS and moderate NASCET studies, have generated reappraisals of the Doppler velocity criteria that most accurately define 70% or greater stenosis and, more recently, greater than 50% diameter stenoses.111 Attempts have been made to determine the Doppler parameters or combination of parameters that most reliably identify a certain-diameter stenosis. Most sources agree that the best parameter is the PSV of the ICA in the region of a stenosis.108 Using multiple parameters can improve diagnostic confidence, particularly when combined with color and power Doppler imaging (see Video 26.19). The degree of stenosis is best assessed using the gray-scale and pulsed Doppler parameters, including ICA PSV, ICA end diastolic velocity (EDV), CCA PSV, CCA EDV, peak systolic ICA/CCA ratio, and peak end diastolic ICA/CCA ratio (EDR)108,109,112 (Videos 26.21 and 26.22).108,109,112 PSV has proved accurate for quantifying high-grade stenoses.98,109 The relationship of PSV to the degree of luminal narrowing is well defined and easily measured.113,114 Although Doppler velocities have proved reliable for defining 70% or greater stenosis, Grant et al.109 showed less favorable results for substenosis classification between 50% to 69% using PSV and ICA/CCA PSV ratios. In

our experience, however, using all four parameters and determining a correct category for the degree of stenosis is the most efficacious way to ensure accuracy. Agreement for all four parameters for a clinical situation is most common. When there is an outlying parameter, further assessment and careful attention to technique and detail are required. EDV and EDR are particularly useful in distinguishing between high grades of stenosis. Additionally, correlating the visual estimation of the degree of stenosis and the velocity numbers will help in correctly grading stenosis, particularly when the degree of stenosis is “near occlusion” (Figs. 26.22 and 26.23; see also Fig. 26.20D and E). On rare occasions, alternate imaging methodologies (e.g., MRA, CTA) may need to be recommended. No criteria for grading external carotid artery stenoses have been established. A good general rule is that if the ECA velocities do not exceed 200 cm/sec, no significant stenosis is present. However, we usually rely on a visible assessment of the degree of narrowing associated with velocity changes. Occlusive plaque involving the ECA is less common than in the ICA and is rarely clinically significant. Similarly, velocity criteria used to grade common carotid artery stenoses have not been well established.115,116 However, if one is able to visualize 2 cm proximal and 2 cm distal to a visible CCA stenosis, a PSV ratio obtained 2 cm proximal to the stenosis (vs. in region of greatest visible stenosis) can be used to grade the “percent diameter stenosis” in a manner similar to that used in peripheral artery studies. A doubling of the PSV across a lesion would correspond to at least a 50% diameter stenosis, and a velocity ratio in excess of 3.5 corresponds to a greater than 75% stenosis. One persistent problem with duplex Doppler with gray-scale ultrasound evaluation of the carotid arteries is that different institutions use PSVs ranging from 130 cm/sec117 to 325 cm/ sec111 to diagnose greater than 70% ICA stenosis.118,119 Factors adding to these discrepancies include technique and equipment.120 While there is a strong level of correlation between techniques and criteria, the choice of criteria has a significant impact on which patients go to surgery.119 This wide range of PSVs reinforces the need for individual ultrasound laboratories to determine which Doppler parameters are most reliable in their own institution.120 Correlation of the velocity ranges obtained by ultrasound with angiographic and surgical results is necessary to achieve accurate, reproducible examinations in a particular ultrasound laboratory.121 The Society of Radiologists in Ultrasound, representing multiple medical and surgical specialties, held a consensus conference in 2002 to consider carotid Doppler ultrasound.122 In addition to guidelines for performing and interpreting carotid ultrasound examinations, panelists devised a set of criteria widely applicable among vascular laboratories (Table 26.1).122 Although the conference did not recommend all established laboratories with internally validated velocity charts alter their practices, they suggested physicians establishing new laboratories consider using the consensus criteria; those with preexisting charts might consider comparing in-house criteria with those provided by the consensus conference. Velocity criteria corresponding to specific degrees of vascular stenosis are listed in the tables. Our

CHAPTER 26  The Extracranial Cerebral Vessels

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A

D

931

C

FIG. 26.22  Abnormal High-Resistance Waveforms.  High-resistance waveforms: (A) CCA, (B) proximal ICA, and (C) distal ICA. Color-flow Doppler imaging of the carotid bulb in (D) transverse and (E) sagittal projections demonstrates a significantly narrowed ICA. These findings are consistent with a greater than 95% stenosis of the ICA and a distal tandem stenosis of the intracranial carotid artery.

E

TABLE 26.1  Diagnostic Criteria for Carotid Ultrasound Examinations

Normal 90 >2.15 ≥2.7 ≥4.15 >2 >125 2.45 4.3

ICA/CCA PSV Ratio

≥3.8 >4

>4

CCA, Common carotid artery; EDV, end diastolic velocity; ICA, internal carotid artery; PSV, peak systolic velocity. Modified from Chahwan S, Miller MT, Pigott JP, et al. Carotid artery velocity characteristics after carotid artery angioplasty and stenting. J Vasc Surg. 2007;45(3):523-526206; Fleming SE, Bluth EI, Milburn J. Role of sonography in the evaluation of carotid artery stents. J Clin Ultrasound. 2005;33(7):321-328.198

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B

FIG. 26.39  Fibromuscular Dysplasia.  (A) Longitudinal color Doppler image of the middle to distal portion of the ICA shows velocity elevation and significant stenosis. (B) Same patient’s proximal portion of the ICA shows no stenosis. (C) Angiogram demonstrates typical appearance of fibromuscular dysplasia in the mid and distal ICA. Note the beaded appearance resulting from focal bands (arrow) of thickened tissue that narrow the lumen.

carotid dissection or subsequent thromboembolic events (Fig. 26.39). Arteritis resulting from autoimmune processes (e.g., Takayasu arteritis, temporal arteritis) or radiation changes can produce diffuse concentric thickening of carotid walls, which most frequently involves the CCA23,216,217 (Fig. 26.40). Cervical trauma can produce carotid dissections or aneurysms. Carotid artery dissection results from a tear in the intima, allowing blood to dissect into the wall of the artery, which produces a false lumen. The false lumen may be blind ended or may reenter the true lumen. The false lumen may occlude or narrow the true lumen, producing symptoms similar to carotid plaque disease. Dissections may arise spontaneously or secondary

to trauma or to intrinsic disease with elastic tissue degeneration (e.g., Marfan syndrome) or may be related to atherosclerotic plaque disease.20 The ultrasound examination of a carotid dissection may reveal a mobile or fixed echogenic intimal flap, with or without thrombus formation.218 Frequently, there is a striking image/Doppler mismatch with a paucity of gray-scale abnormalities seen in association with marked flow abnormalities (Fig. 26.41). Color or power Doppler ultrasound can readily clarify the source of this mismatch by demonstrating abrupt tapering of the patent, filled lumen to the point of an ICA occlusion. When the ICA is occluded, the proximal ipsilateral CCA will demonstrate

CHAPTER 26  The Extracranial Cerebral Vessels

A

C

Internal Carotid Artery Dissection: Spectrum of Findings INTERNAL CAROTID ARTERY Absent flow or occlusion Echogenic intimal flap, with or without thrombus Hypoechoic thrombus, with or without luminal narrowing Normal appearance COMMON CAROTID ARTERY High-resistance waveform Dampened flow Normal appearance

a high-resistance waveform. When the ICA is severely narrowed (secondary to hemorrhage and a thrombus in the area of the false lumen), flow in the ICA may demonstrate high velocities. In these nonoccluded ICA cases, flow velocity waveforms in the CCA may be normal. Although conventional angiography, MRA,

947

B

FIG. 26.40  Long-Segment Stenosis of CCA Caused by Takayasu Arteritis.  Power Doppler images of (A) left and (B) right CCA shows long-segment concentric narrowing caused by greatly thickened walls of the artery (arrows). (C) Spectral Doppler waveform shows a mildly tardus-parvus waveform.

or CTA can be used initially to diagnose a dissection, ultrasound can be used to follow patients to assess the therapeutic response to anticoagulation. Repeat sonographic evaluation of patients with ICA dissection after anticoagulation therapy reveals recanalization of the artery in as many as 70% of cases.219-221 It is important to consider the diagnosis of dissection as a cause of neurologic symptoms, particularly when the clinical presentation, age, and patient history are atypical for that of atherosclerotic disease or hemorrhagic stroke.

Pulsatile Neck Masses in the Carotid Region The most common CCA aneurysm occurs in the region of the carotid bifurcation. These aneurysms may result from atherosclerosis, infection, trauma, surgery, or contagious disease, such as syphilis. The normal CCA usually measures no more than 1 cm in diameter. Carotid body tumors, one of several paragangliomas that involve the head and neck, are usually benign,

948

Small Parts, Carotid Artery, and Peripheral Vessel Sonography

PART III

A

C

B

D

E

FIG. 26.41  Carotid Artery Dissection.  (A) Abnormal high-resistance waveforms (arrow) at the origin of the right ICA with no evidence of flow distal to this point (curved arrow). (B) Gray-scale evaluation of the vessel in the area of the occlusion demonstrates only a small, linear echogenic structure (arrow) without evidence of significant atherosclerotic narrowing. (C) Subsequent angiogram demonstrates the characteristic tapering to the point of occlusion (arrow) associated with carotid artery dissection and thrombotic occlusion. (D) Transverse and (E) longitudinal images of another patient show an intimal flap (arrow) in an ECA. I, Internal carotid artery.

well-encapsulated masses located at the carotid bifurcation.29 These tumors may be bilateral, particularly in the familial variant, and are very vascular, often producing an audible bruit.29 Some of these tumors produce catecholamines, leading to sudden changes in blood pressure during or after surgery. Color Doppler ultrasound demonstrates an extremely vascular soft tissue mass at the carotid bifurcation29 (Fig. 26.42). Color Doppler ultrasound can also be used to monitor embolization or surgical resection of carotid body tumors. A classic nonmass is the ectatic innominate/proximal CCA, frequently occurring as a pulsatile supraclavicular mass in older women. The request to rule out a carotid aneurysm almost invariably shows the classic normal features of these tortuous vessels (Fig. 26.43). Extravascular masses (e.g., lymph node masses [Fig. 26.44], hematomas, abscesses) that compress or displace the carotid arteries can be readily distinguished from primary vascular masses, such as aneurysms or pseudoaneurysms. Posttraumatic pseudoaneurysms can usually be distinguished from true carotid aneurysms by the characteristic to-and-fro

waveforms in the neck of the pseudoaneurysm, as well as the internal variability (yin-yang) characteristic of a pseudoaneurysm (Fig. 26.45).

TRANSCRANIAL DOPPLER SONOGRAPHY In transcranial Doppler (TCD) ultrasound, a low-frequency 2-MHz transducer is used to evaluate blood flow within the intracranial carotid and vertebrobasilar system and the circle of Willis. Access is achieved through the orbits, foramen magnum, or, most often, the region of temporal calvarial thinning (transtemporal window).222,223 However, many patients (up to 55% in one series224) may not have access to an interpretable TCD examination. Women, particularly African American women, have a thick temporal bone through which it is difficult to insonate the basal cerebral arteries.224,225 This difficulty limits the feasibility of TCD imaging as a routine part of the noninvasive cerebrovascular workup.223,224

CHAPTER 26  The Extracranial Cerebral Vessels

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ECA

ICA

A

B

FIG. 26.42  Carotid Body Tumor.  (A) Transverse image of the carotid bifurcation shows a mass (arrows) splaying the internal carotid artery (ICA) and external carotid artery (ECA). (B) Pulsed Doppler traces of the carotid body tumor show typical arteriovenous shunt (low-resistance) waveform.

,

(

, FIG. 26.43  Ectatic CCA.  Color Doppler image shows ectatic proximal common carotid artery (CCA) arising from the innominate artery (I) and responsible for a pulsatile right supraclavicular mass. FIG. 26.44  Pathologic Lymph Node Near Carotid Bifurcation.  Power Doppler image shows a malignant lymph node (arrow) lateral to the carotid bifurcation. E, External carotid artery; I, internal carotid artery.

950

PART III

Small Parts, Carotid Artery, and Peripheral Vessel Sonography

By using spectral analysis, various parameters are determined, including mean velocity, PSV, EDV, and the pulsatility and resistive indices of the blood vessels. Color or power Doppler ultrasound can improve velocity determination by providing better angle theta determination and localizing the course of vessels.222 TCD applications include (1) evaluation of intracranial stenoses and collateral circulation, (2) detection and follow-up of vasoconstriction from subarachnoid hemorrhage, (3) determination of brain death, (4) evaluation of patients with sickle cell disease, and (5) identification of arteriovenous malformation.219-223,226,227 TCD is

most reliable in diagnosing stenoses of the middle cerebral artery, with sensitivities as high as 91% reported. TCD is less reliable for detecting stenoses of the intracranial vertebrobasilar system, anterior and posterior cerebral arteries, and terminal ICA. However, TCD is helpful in assessing vertebral artery patency and flow direction when no flow is detected in the extracranial vertebral artery (Fig. 26.46). Diagnosis of an intracranial stenosis is based on an increase in the mean velocity of blood flow in the affected vessel compared to that of the contralateral vessel at the same location.223-225 Advantages of TCD ultrasound also include its availability for monitoring patients in the operating room or angiographic suite for potential cerebrovascular complications.225 Intraoperative TCD monitoring can be performed with the transducer strapped over the transtemporal window, allowing evaluation of blood flow in the middle cerebral artery during CEA. The adequacy of cerebral perfusion can be assessed while the carotid artery is clamped.225,228 TCD is also capable of detecting intraoperative microembolization, which produces high-amplitude spikes (high-intensity transient signals [“HITS”]) on the Doppler spectrum.223,224,227,229-231 The technique can be used for the serial evaluation of vasospasms. This diagnosis is usually based on serial examinations of the relative increase in blood flow velocity and resistive index changes resulting from a decrease in the lumen of the vessel caused by vasospasms.225 More description of transcranial Doppler is in Chapter 47.

VERTEBRAL ARTERY FIG. 26.45  Pseudoaneurysm of the Common Carotid Artery (CCA).  Transverse image of the right CCA demonstrates a jet of flow into a pseudoaneurysm, which resulted from an attempted central venous line placement.

A

The vertebral arteries supply the majority of the posterior brain circulation. Through the circle of Willis, the vertebral arteries also provide collateral circulation to other portions of the brain

B

FIG. 26.46  Transcranial Doppler Imaging.  (A) Transcranial duplex scan of the posterior fossa in a patient with an incomplete left subclavian steal syndrome demonstrates retrograde systolic flow (arrow) and antegrade diastolic flow (curved arrow). The scan is obtained in a transverse projection from the region of the foramen magnum (open arrowhead). (B) Color Doppler image obtained in the same patient demonstrates that there is retrograde flow not only within the left vertebral artery but also within the basilar artery (arrow).

CHAPTER 26  The Extracranial Cerebral Vessels

951

B

6

9 $

C

S

FIG. 26.47  Vertebral Artery Course.  Lateral diagram of vertebral artery (arrows) shows its course through the cervical spine transverse foramina en route to joining the contralateral vertebral artery to form the basilar artery (B). C, Carotid artery; S, subclavian artery.

in patients with carotid occlusive disease. Evaluation of the extracranial vertebral artery seems a natural extension of carotid duplex and color Doppler imaging.232,233 Historically, however, these arteries have not been studied as intensively as the carotids. Symptoms of vertebrobasilar insufficiency also tend to be rather vague and poorly defined compared with symptoms referable to the carotid circulation. It is often difficult to make an association confidently between a lesion and symptoms. Furthermore, interest in surgical correction of vertebral lesions has been limited. The anatomic variability, small size, deep course, and limited visualization resulting from overlying transverse processes make the vertebral artery more difficult to examine accurately with ultrasound.232,234-236 The clinical utility of vertebral artery duplex scanning in diagnosing subclavian steal and presteal phenomena is well established.237-239 Less clear-cut is the use of vertebral duplex scanning in evaluating vertebral artery stenosis, dissection, or aneurysm.240

Anatomy The vertebral artery is usually the first branch off the subclavian artery (Fig. 26.47). However, variation in the origin of the vertebral arteries is common. In 6% to 8% of people, the left vertebral artery arises directly from the aortic arch proximal to the left subclavian artery.234,241 In 90%, the proximal vertebral artery ascends superomedially, passing anterior to the transverse process

FIG. 26.48  Normal Vertebral Artery and Vein.  Longitudinal color Doppler image shows a normal vertebral artery (A) and vein (V) running between the transverse processes of the second to sixth cervical vertebrae (C2-C6), which are identified by their periodic acoustic shadowing (S).

of the seventh cervical vertebra (C7), and enters the transverse foramen at the C6 level. The rest of the vertebral arteries enter into the transverse foramen at the C5 or C7 level and, rarely, at the C4 level. The size of vertebral arteries is variable, with the left larger than the right in 42%, the two vertebral arteries equal in size in 26%, and the right larger than the left in 32% of cases.242 One vertebral artery may even be congenitally absent. Usually, the vertebral arteries join at their confluence to form the basilar artery. Rarely, the vertebral artery may terminate in a posterior inferior cerebellar artery.

Sonographic Technique and Normal Examination Vertebral artery visualization with Doppler flow analysis can be obtained in 92% to 98% of vessels232,243 (Fig. 26.48). Vertebral artery duplex examinations are performed by first locating the CCA in the longitudinal plane. The direction of flow in the CCA and jugular vein is determined. A gradual sweep of the transducer laterally demonstrates the vertebral artery and vein running between the transverse processes of C2 to C6, which are identified by their periodic acoustic shadowing. Angling the transducer caudad allows visualization of the vertebral artery origin in 60% to 70% of the arteries, in 80% on the right side, and in 50% on the left. This discrepancy may relate to the left vertebral artery origin being deeper and arising directly from the aortic arch in 6% to 8% of cases.234,241 The presence and direction of flow should be established. Visible plaque should be assessed. The vertebral artery usually has a low-resistance flow pattern similar to that of the CCA, with continuous flow in systole and diastole; however, wide variability in waveform shape has been noted in angiographically

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W

R

FIG. 26.49  Normal Vertebral Artery Waveform.  Normal lowresistance waveform of the vertebral artery with filling of the spectral window.

normal vessels.244 Because the vessel is small, flow tends to demonstrate a broader spectrum. The clear spectral window seen in the normal carotid system is often filled in the vertebral artery102 (Fig. 26.49). The vertebral vein (often a plexus of veins) runs parallel and adjacent to the vertebral artery. Care must be taken not to mistake its flow for that of the adjacent artery, particularly if the venous flow is pulsatile. Comparison with jugular venous flow during respiration should readily distinguish between vertebral artery and vein. At times, the ascending cervical branch of the thyrocervical trunk can be mistaken for the vertebral artery. This can be avoided by looking for landmark transverse processes that accompany the vertebral artery and by paying careful attention to the waveform of the visualized vessel. The ascending cervical branch has a high-impedance waveform pattern similar to that of the ECA.237 TCD sonographic examination of the vertebrobasilar artery system can be performed as an adjunct to the extracranial evaluation. The examination is conducted with a 2-MHz transducer with the patient sitting, using a suboccipital midline nuchal approach, or with the patient supine, using a retromastoidal approach. Color or power Doppler facilitates TCD imaging of the vertebrobasilar system.245

Subclavian Steal The subclavian steal phenomenon occurs when there is highgrade stenosis or occlusion of the proximal subclavian or innominate arteries with patent vertebral arteries bilaterally. The artery of the ischemic limb “steals” blood from the vertebrobasilar circulation through retrograde vertebral artery flow, which may result in symptoms of vertebrobasilar insufficiency (Fig. 26.50). Symptoms are usually most pronounced during exercise of the

L

S

FIG. 26.50  Hemodynamic Pattern in Subclavian Steal Syndrome.  Proximal left subclavian artery occlusive lesion (arrowhead) decreases flow to the distal subclavian artery (S). This produces retrograde flow (large arrows) down the left vertebral artery (L) and stealing from the right vertebral artery (R) and other intracranial vessels through the circle of Willis (W).

upper extremity but can be produced by changes in head position. However, there is often poor correlation between vertebrobasilar symptoms and the subclavian steal phenomenon. In most cases, flow within the basilar artery is unaffected unless severe stenosis of the vertebral artery supplying the steal exists.245 Also, surgical or angioplastic restoration of blood flow may not result in relief of symptoms.246 The subclavian steal phenomenon is most often caused by atherosclerotic disease, although traumatic, embolic, surgical, congenital, and neoplastic factors have also been implicated. Although the proximal subclavian stenosis or occlusion may be difficult to image, particularly on the left, the vertebral artery waveform abnormalities correlate with the severity of the subclavian disease. Doppler evaluation of the vertebral artery reveals four distinct abnormal waveforms that correlate with subclavian or vertebral

CHAPTER 26  The Extracranial Cerebral Vessels

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FIG. 26.51  Reversal of Vertebral Artery Flow in Subclavian Steal.  Subclavian steal causes reversed flow in vertebral artery. Spectral Doppler (A) demonstrates complete vertebral artery flow reversal due to right subclavian artery occlusion. Color-flow Doppler (B) demonstrates flow toward the transducer.

Abnormal Vertebral Artery Waveforms COMPLETE SUBCLAVIAN STEAL Reversal of flow within vertebral artery ipsilateral to stenotic or occluded subclavian or innominate artery INCOMPLETE OR PARTIAL SUBCLAVIAN STEAL Transient reversal of vertebral artery flow during systole May be converted into a complete steal using provocative maneuvers Suggests stenotic, not occlusive, lesion PRESTEAL PHENOMENON “Bunny” waveform: systolic deceleration less than diastolic flow May be converted into partial steal by provocative maneuvers Seen with proximal subclavian stenosis

FIG. 26.52  Incomplete Subclavian Steal.  Flow in early systole is antegrade, flow in peak systole is retrograde, and flow in late systole and diastole (arrow) is again antegrade.

artery pathology on angiography. These include the complete subclavian steal, partial or incomplete steal, presteal phenomenon, and tardus-parvus vertebral artery waveforms.239,244 In a complete subclavian steal, flow within the vertebral artery is completely reversed (Fig. 26.51). Incomplete steal or partial steal demonstrate transient reversal of vertebral flow during systole239,245

TARDUS-PARVUS (DAMPENED) WAVEFORM Seen with vertebral artery stenosis

(Fig. 26.52). Incomplete steal suggests high-grade stenosis of the subclavian or innominate artery rather than occlusion. Provocative maneuvers, such as exercising the arm for 5 minutes or 5-minute inflation of a sphygmomanometer on the arm to induce rebound hyperemia on the side of the subclavian or innominate lesion, can enhance the sonographic findings and convert an incomplete steal to a complete steal.155,185

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FIG. 26.53  Incomplete Subclavian Steal and Provocative Maneuver.  (A) Presteal left vertebral artery waveform. Flow decelerates in peak systole but does not reverse. (B) After provocative maneuver, there is reversal of flow in peak systole in response to a decrease in peripheral arterial pressure.

The presteal (“bunny”) waveform shows antegrade flow but with a striking deceleration of velocity in peak systole to a level less than EDV. This is seen in patients with proximal subclavian stenosis, which is usually less severe than in those with partial steal waveform.239 The bunny waveform can be converted into a partial steal or complete steal waveform by provocative maneuvers (Fig. 26.53). A tardus-parvus waveform (also called a dampened waveform) can be seen in patients with high-grade proximal vertebral stenosis.238,239 With a subclavian steal, color Doppler may show two similarly color-encoded vessels between the transverse processes, representing the vertebral artery and vein.129 Transverse images of the vertebral artery with color Doppler show reversed flow compared with those of the CCA. A Doppler spectral waveform must be produced in all such cases to avoid mistaking flow reversal within an artery for flow in a pulsatile vertebral vein.129,237

Stenosis and Occlusion Diagnosis of vertebral artery stenosis is more difficult than diagnosis of flow reversal. Most hemodynamically significant stenoses occur at the vertebral artery origin, situated deep in the upper thorax and seen in only 60% to 70% of patients.234,243,241 Even if the vertebral artery origin is visualized, optimal adjustments of the Doppler angle for accurate velocity measurements may

be difficult because of the deep location and vessel tortuosity. No accurate reproducible criteria for evaluating vertebral artery stenosis exist. Because flow is normally turbulent within the vertebral artery, spectral broadening cannot be used as an indicator of stenosis. Velocity measurements are not reliable as criteria for stenosis because of the wide normal variation in vertebral artery diameter. Although velocities greater than 100 cm/ sec often indicate stenosis, they can occur in angiographically normal vessels. For example, high-flow velocity may be present in a vertebral artery that is serving as a major collateral pathway for cerebral circulation in cases of carotid occlusion34,188,247 (Fig. 26.54). Thus only a focal increase in velocity of at least 50%, visible stenosis on gray-scale or color Doppler, or a striking tardus-parvus vertebral artery waveform is likely to indicate significant vertebral stenosis. The variability of resistive indices in normal and abnormal vertebral arteries precludes the use of this parameter as an indicator of vertebral disease.244 Diagnosis of vertebral artery occlusion is also difficult. Often, the inability to detect arterial flow results from a small or congenitally absent vertebral artery or a technically difficult examination. The differentiation of severe stenosis from occlusion is difficult for the same reasons. Extremely dampened blood flow velocity in high-grade stenoses may result in a Doppler

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FIG. 26.54  Increased Flow Velocity in Vertebral Artery.  Pulsed Doppler spectral trace from a left vertebral artery demonstrates strikingly high velocities and disturbed flow (arrow). Although this degree of velocity elevation and flow disturbance could be associated with a focal stenosis, in this case there was increased velocity throughout the vertebral artery from bilateral internal carotid artery occlusion and increased collateral flow into the vertebral artery.

signal with amplitude too low to be detected.235 Power Doppler imaging may prove useful in this situation. Visualization of only a vertebral vein may indicate vertebral artery occlusion or congenital absence.

INTERNAL JUGULAR VEINS The internal jugular veins are the major vessels responsible for the return of venous blood from the brain. The most common clinical indication for duplex and color Doppler flow ultrasound of the internal jugular vein is the evaluation of suspected jugular venous thrombosis.248-256 Thrombus formation may be related to central venous catheter placement. Other indications include a diagnosis of jugular venous ectasia254,255,257,258 and guidance for internal jugular or subclavian vein cannulation,259-265 particularly in difficult situations where vascular anatomy is distorted.

Sonographic Technique The normal internal jugular vein is easily visualized. The vein is scanned with the neck extended and the head turned to the contralateral side. Longitudinal and transverse scans are obtained with light transducer pressure on the neck to avoid collapsing the vein. A coronal view from the supraclavicular fossa is used to image the lower segment of the internal jugular vein and the medial segment of the subclavian vein as they join to form the brachiocephalic vein. The jugular vein lies lateral and anterior to the CCA, lateral to the thyroid gland, and deep to the sternocleidomastoid muscle. The vessel has sharply echogenic walls and a hypoechoic or

FIG. 26.55  Normal Jugular Vein.  Complex venous pulsations in a normal jugular vein (J) reflect the cycle of events in the right atrium.

anechoic lumen. Normally, a valve can be visualized in its distal portion.251,260,266 The right internal jugular vein is usually larger than the left.259 Real-time ultrasound demonstrates venous pulsations related to right heart contractions, as well as changes in venous diameter that vary with changes in intrathoracic pressure. Doppler examination graphically depicts these flow patterns (Fig. 26.55). On inspiration, negative intrathoracic pressure causes flow toward the heart and the jugular veins to decrease in diameter. During expiration and during Valsalva maneuver, increased intrathoracic pressure causes a decrease in the blood return, and the veins enlarge, with minimal or no flow noted. The walls of the normal jugular vein collapse completely when moderate transducer pressure is applied. Sudden patient sniffing reduces intrathoracic pressure, causing momentary collapse of the vein on real-time ultrasound, accompanied by a brief increase in venous flow toward the heart as shown by Doppler.250,252,254

Thrombosis Clinical features of jugular venous thrombosis include a tender, poorly defined, nonspecific neck mass or swelling. The correct diagnosis may not be immediately obvious.251 Thrombosis of the internal jugular vein can be completely asymptomatic because of the deep position of the vein and the presence of abundant collateral circulation.254 Internal jugular thrombosis most often results from complications of central venous catheterization.249,253,254 Other causes include intravenous drug abuse, mediastinal tumor, hypercoagulable states, neck surgery, and local inflammation or adenopathy.251 Some cases are idiopathic or spontaneous.251 Possible complications of jugular venous thrombosis include suppurative thrombophlebitis, clot propagation, and pulmonary embolism.251,255 Real-time examination reveals an enlarged, noncompressible vein, which may contain a visible echogenic intraluminal thrombus. An acute thrombus may be anechoic and

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FIG. 26.56  Internal Jugular Vein (IJV) Thrombosis: Spectrum of Appearances.  (A) Transverse image of an acute left internal jugular vein thrombus (arrow). The vein is distended and noncompressible. C, Common carotid artery. (B) Longitudinal image of a different patient demonstrates a hypoechoic thrombus and no Doppler signal. (C) Longitudinal color Doppler image shows a small amount of thrombus arising from the posterior wall of the IJV. (D) Transverse image shows an echogenic thrombus, indicating chronic thrombus in IJV. (E) Longitudinal image demonstrates a thrombus (arrow) around jugular vein catheter. (F) Longitudinal images show a thrombus arising from anterior wall. This thrombus probably results from previous catheter placement in this region.

indistinguishable from flowing blood; however, the characteristic lack of compressibility and absent Doppler or color Doppler flow in the region of a thrombus quickly lead to the correct diagnosis. In addition, there is visible loss of vein response to respiratory maneuvers and venous pulsation. Spectral and color Doppler interrogations reveal absent flow (Fig. 26.56). Collateral veins may be identified, particularly in cases of chronic internal jugular vein thrombosis. Central liquefaction or other heterogeneity of the thrombus also suggests chronicity. Chronic thrombi may be difficult to visualize because they tend to organize and are difficult to separate from echogenic perivascular fatty tissue.260 The absence of cardiorespiratory plasticity in a patent jugular or subclavian vein can indicate a more central, nonocclusive thrombus (Fig. 26.57). The confirmation of bilateral loss of venous pulsations strongly supports a more central thrombus, which can be documented by angiographic or magnetic resonance venography. A thrombus that is related to catheter insertion is often demonstrated at the tip of the catheter, although it may be seen

anywhere along the course of the vein. The catheter can be visualized as two parallel echogenic lines separated by an anechoic region. Flow is not usually demonstrated in the catheter, even if the catheter itself is patent. Sonography is a reliable means of diagnosing jugular and subclavian vein thrombosis. Sonography has limited access and cannot image all portions of the jugular and subclavian veins, especially those located behind the mandible or below the clavicle, although knowledge of the full extent of a thrombus is not typically a critical factor in treatment planning.251,255 Serial sonographic examination to evaluate response to therapy after the initial assessment can be performed safely and inexpensively. Sonography can also document venous patency before vascular line placement, facilitating safer and more successful catheter insertion.

Acknowledgment Thanks to Kathleen McFadden and Barbara Siede for their assistance with manuscript preparation.

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Small Parts, Carotid Artery, and Peripheral Vessel Sonography

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Small Parts, Carotid Artery, and Peripheral Vessel Sonography

201. Zhou W, Lin PH, Bush RL, et al. Management of in-sent restenosis after carotid artery stenting in high-risk patients. J Vasc Surg. 2006;43(2): 305-312. 202. Daou B, Chalouhi N, Starke RM, et al. Predictors of restenosis after carotid artery stenting in 241 cases. J Neurointerv Surg. 2016;8(7):677-679. 203. Miyazaki Y, Mori T, Iwata T, et al. Continuous daily use of cilostazol prevents in-stent restenosis following carotid artery stenting: serial angiographic investigation of 229 lesions. J Neurointerv Surg. 2016;8(5):471-475. 204. Robbin ML, Lockhart ME, Weber TM, et al. Carotid artery stents: early and intermediate follow-up with Doppler US. Radiology. 1997;205(3): 749-756. 205. Barros P, Felgueiras H, Pinheiro D, et al. Restenosis after carotid artery stenting using a specific designed ultrasonographic protocol. J Stroke Cerebrovasc Dis. 2014;23(6):1416-1420. 206. Chahwan S, Miller MT, Pigott JP, et al. Carotid artery velocity characteristics after carotid artery angioplasty and stenting. J Vasc Surg. 2007;45(3): 523-526. 207. Setacci C, Chisci E, Setacci F, et al. Grading carotid intrastent restenosis: a 6-year follow-up study. Stroke. 2008;39(4):1189-1196. 208. Zhou W, Felkai DD, Evans M, et al. Ultrasound criteria for severe in-stent restenosis following carotid artery stenting. J Vasc Surg. 2008;47(1): 74-80. 209. Lal BK, Hobson RW 2nd, Tofighi B, et al. Duplex ultrasound velocity criteria for the stented carotid artery. J Vasc Surg. 2008;47(1):63-73. 210. Armstrong PA, Bandyk DF, Johnson BL, et al. Duplex scan surveillance after carotid angioplasty and stenting: a rational definition of stent stenosis. J Vasc Surg. 2007;46(3):460-465. 211. Chi YW, White CJ, Woods TC, Goldman CK. Ultrasound velocity criteria for carotid in-stent restenosis. Catheter Cardiovasc Interv. 2007;69(3): 349-354. 212. Furie DM, Tien RD. Fibromuscular dysplasia of arteries of the head and neck: imaging findings. Am J Roentgenol. 1994;162(5):1205-1209. 213. Kliewer MA, Carroll BA. Ultrasound case of the day. Internal carotid artery web (atypical fibromuscular dysplasia). Radiographics. 1991;11(3): 504-505. 214. Arning C, Grzyska U. Color Doppler imaging of cervicocephalic fibromuscular dysplasia. Cardiovasc Ultrasound. 2004;2:7. 215. Sethi SS, Lau JF, Godbold J, et al. The S curve: a novel morphological finding in the internal carotid artery in patients with fibromuscular dysplasia. Vasc Med. 2014;19(5):356-362. 216. Maeda H, Handa N, Matsumoto M, et al. Carotid lesions detected by B-mode ultrasonography in Takayasu’s arteritis: “macaroni sign” as an indicator of the disease. Ultrasound Med Biol. 1991;17(7):695-701. 217. Ralls PW. Takayasu arteritis. Ultrasound Q. 2010;26(3):133-134. 218. Sallustio F, Di Legge S, Rossi C, Stanzione P. Ultrasound evaluation of early changes in arterial dissection. J Stroke Cerebrovasc Dis. 2010;19(2): 167-168. 219. Sturzenegger M. Spontaneous internal carotid artery dissection: early diagnosis and management in 44 patients. J Neurol. 1995;242(4): 231-238. 220. Sturzenegger M, Mattle HP, Rivoir A, Baumgartner RW. Ultrasound findings in carotid artery dissection: analysis of 43 patients. Neurology. 1995;45(4):691-698. 221. Steinke W, Rautenberg W, Schwartz A, Hennerici M. Noninvasive monitoring of internal carotid artery dissection. Stroke. 1994;25(5):998-1005. 222. Lupetin AR, Davis DA, Beckman I, Dash N. Transcranial Doppler sonography. Part 1. Principles, technique, and normal appearances. Radiographics. 1995;15(1):179-191. 223. LaRovere KL, O’Brien NF. Transcranial Doppler sonography in pediatric neurocritical care: a review of clinical applications and case illustrations in the pediatric intensive care unit. J Ultrasound Med. 2015;34(12): 2121-2132. 224. Comerota AJ, Katz ML, Hosking JD, et al. Is transcranial Doppler a worthwhile addition to screening tests for cerebrovascular disease? J Vasc Surg. 1995;21(1):90-95. 225. Rorick MB, Nichols FT, Adams RJ. Transcranial Doppler correlation with angiography in detection of intracranial stenosis. Stroke. 1994;25(10): 1931-1934.

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CHAPTER

27

 

Peripheral Vessels Mark E. Lockhart, Heidi R. Umphrey, Therese M. Weber, and Michelle L. Robbin

SUMMARY OF KEY POINTS • Key aspects of vascular Doppler imaging include knowledge of anatomy and waveform morphology, scanning technique, and attention to detail. • Spectral Doppler velocity criteria can characterize stenosis detected by gray-scale and color Doppler. • Doppler evaluation of peripheral artery disease can provide diagnostic information and enable surgical planning and evaluation of bypass grafts. • Extremity aneurysm and pseudoaneurysm have typical Doppler findings similar to other areas of the arterial system. • Evaluation of the upper and lower extremity venous system is primarily performed with sonography.

• Differentiation of acute from residual or chronic deep venous thrombosis (DVT) with imaging and clinical parameters is often difficult. • Controversial venous issues include clinical criteria for treatment of DVT, when to recommend a follow-up examination, calf vein evaluation, and two-point or focused examination approach. • Preoperative sonographic mapping of upper extremity and thigh vessels assists surgical planning for placement of hemodialysis arteriovenous fistula (AVF) and grafts. • Postoperative evaluation of hemodialysis AVF and grafts with ultrasound aids the assessment of AVF maturation, as well as evaluation for access stenosis, steal, thrombus, and focal complications.

CHAPTER OUTLINE PERIPHERAL ARTERIES Sonographic Examination Technique Stenosis Evaluation Lower Extremity Arteries Normal Anatomy Ultrasound Examination and Imaging Protocol Peripheral Arterial Occlusion Peripheral Arterial Stenosis Aneurysm Pseudoaneurysm Arteriovenous Fistula Lower Extremity Vein Bypass Grafts Upper Extremity Arteries Normal Anatomy Ultrasound Examination and Imaging Protocol Arterial Occlusion, Aneurysm, and Pseudoaneurysm Arterial Stenosis Subclavian Stenosis Thoracic Outlet Syndrome Radial Artery Evaluation for Coronary Bypass Graft

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PERIPHERAL VEINS Sonographic Examination Technique Lower Extremity Veins Normal Anatomy Ultrasound Examination and Imaging Protocol Acute Deep Venous Thrombosis Residual (Chronic) Deep Venous Thrombosis Potential Pitfalls Complete Venous Doppler Versus More Limited Examinations Recommendations for Deep Venous Thrombosis Follow-Up Venous Insufficiency Venous Mapping Upper Extremity Veins Normal Anatomy Ultrasound Examination and Imaging Protocol Upper Extremity Acute Deep Venous Thrombosis Differentiation of Acute From Residual or Chronic Venous Thrombosis

Potential Pitfalls HEMODIALYSIS Sonographic Examination Technique Vascular Mapping Before Hemodialysis Access Upper Extremity Ultrasound Examination and Imaging Protocol Arteriovenous Fistula and Graft Arteriovenous Fistula Graft Palpable Focal Masses Near Arteriovenous Fistula and Graft Arteriovenous Fistula Maturation Evaluation Arteriovenous Fistula and Graft Stenosis Arterial Steal Arm and Leg Swelling With Arteriovenous Fistula or Graft Arteriovenous Fistula and Graft Occlusion CONCLUSION

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rior chapters have described details of physics of Doppler analysis and use of ultrasound in the assessment of the vasculature supplying the head and neck. In this chapter we describe assessment of the peripheral arteries and veins, as well as arteriovenous fistula (AVF) and grafts. In general, these areas are readily evaluated by Doppler ultrasound. Because they are usually located at depths of 6 cm or less, the extremity vessels are more consistently imaged than those in the abdomen or thorax. Availability of sufficient imaging windows allows the transducer to be placed over the vascular area of interest with overlying tissue containing bone or gas. Transducers with frequencies greater than 5 MHz can typically be used. Gray-scale sonography is useful for evaluating the presence of atherosclerotic plaque or confirming extravascular masses. Color flow Doppler imaging allows for a rapid survey of the area of interest, and then spectral Doppler can be used to characterize blood flow patterns. Standardized protocols, such as those provided by the American College of Radiology (ACR), American Institute of Ultrasound in Medicine, and Society of Radiologists in Ultrasound should be followed.1,2 It is recommended that examinations be performed in an accredited laboratory with participation in one of the vascular accreditation programs, such as the ACR or the Intersocietal Commission for the Accreditation of Vascular Laboratories, in order to achieve a national standard of excellence and to improve the chance of success of peripheral arterial and venous ultrasound examinations.3 In the setting of a dedicated staff and with physician support, ultrasound can be used to diagnose many peripheral vascular abnormalities definitively and avoid the need for ionizing radiation or intravenous contrasted cross-sectional studies.

PERIPHERAL ARTERIES A variety of symptoms and signs can be evaluated by arterial ultrasound. Sonographic examination is relatively rapid and has benefits over other modalities, such as real-time technique, lack of ionizing radiation, and relatively low expense. In the last two decades, the number of indications for peripheral artery ultrasound has expanded. The most recent ACR practice parameter on the topic lists indications for the examination, which include claudication and/or rest pain in the lower extremities to evaluate for arterial stenosis or occlusion.2 Patients with pain, discoloration, or ulcer formation in the extremities (most commonly lower) may have tissue ischemia or necrosis from arterial stenosis or occlusion. Additional symptoms of numbness or cold extremity may be noted. However, symptomatology may vary depending on the rapidity of onset and whether collaterals have developed to decrease the effects of stenosis on the tissues. In some patients, vascular abnormalities may be subclinical and found incidentally on imaging for other indications. Once an abnormality has been identified, ultrasound can monitor progression of disease, determine success or failure after intervention, and identify acceptable vessels for bypass graft creation. Other extremity abnormalities can be evaluated sonographically. Focal masses can be assessed to exclude vascular causes such as aneurysm or fistula with venous enlargement. When

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chronic positional upper extremity symptoms are present, ultrasound can evaluate for thoracic outlet syndrome. More peripherally, Doppler can document patency of the palmar arch in surgical planning for bypass graft harvesting, and it can assess the radial artery before and after vascular access. In the acute setting, traumatic injuries can be evaluated to determine adjacent arterial patency. Pseudoaneurysms and dissections are visible by ultrasound in these patients. Specific levels of embolic disease can also be depicted.

Sonographic Examination Technique Gray-scale evaluation of the peripheral arteries is important to determine the amount of atherosclerotic disease or thrombus present. The highest frequency transducer that allows good penetration and visualization should be applied, typically a 5- to 12-MHz linear array transducer, with a higher frequency transducer used in areas where the arteries are more superficial. Occasionally, a 3- to 5-MHz sector or curved array probe may be necessary in large patients or those with large amounts of edema. Occasionally, atherosclerotic plaque or thrombus is hypoechoic, and color Doppler is extremely useful to evaluate residual lumen, with the gain adjusted so color does not overlap into adjacent tissues. The spectral Doppler gate is adjusted within the lumen of the artery to allow adequate signal. The scale and gain should be optimized to show strong flow signals that use most of the scale to display the waveform. Normally, a medium or high wall filter is used in arterial evaluation. If there is slow flow, a low wall filter may be used to improve detection. In general, for detection of small channels of slow flow in areas of near-occlusion, power Doppler may be more sensitive than color Doppler.4 However, the advances in color Doppler may have reduced this difference in recent years. The components of the sonographic evaluation differ based on the indication. For example, imaging for suspected arterial stenosis or occlusion is very different from evaluation of a focal mass or aneurysm. The technical components of the examination have been recently described in the ACR practice parameters.2

Stenosis Evaluation Color and spectral Doppler imaging are key to stenosis evaluation, using a combination of waveform morphology and velocity characteristics. On gray-scale imaging, a focal stenosis or occlusion may be visible, but this should be confirmed by Doppler. Collaterals should also prompt additional attention with Doppler. Any areas of visible narrowing or turbulent color Doppler signal should be further characterized with spectral Doppler. A change in spectral waveform morphology from one arterial segment to the next should also be further evaluated with color and spectral Doppler to locate a point of transition (Fig. 27.1). Spectral Doppler should be performed in the longitudinal plane and should be angle corrected 60% or less from the center beam. If a jet at or downstream from a stenosis is seen, angle correction parallel to the orientation of the jet should be performed to more accurately measure peak systolic velocity (PSV). Using this technique, waveform morphology and peak velocity should be evaluated at any suspected area of stenosis, as well as the feeding vessel

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Triphasic Normal Biphasic, low velocity, high resistance Distal obstruction

Inflow obstruction

Monophasic, low velocity, lower resistance

Monophasic, high velocity, lower resistance Arteriovenous fistula

Biphasic, reciprocating Pseudoaneurysm FIG. 27.1  Diagrams of Doppler Flow Patterns in Normal and Abnormal Scenarios.  The normal Doppler spectrum of flowing blood in the lower extremity arteries typically has a triphasic pattern: (1) forward flow during systole, (2) a short period of flow reversal in early diastole, and (3) low-velocity flow during the remainder of diastole. Arterial Doppler signals are altered depending on the pathologic change. The four other patterns are examples of common arterial pathologies: distal obstruction, inflow obstruction, arteriovenous fistula, and pseudoaneurysm.

within 4 cm upstream, and the draining artery within 4 cm downstream. The inflow velocity is used as a reference to assess for increased peak velocity at the stenosis, and the downstream location is evaluated for peak velocity drop, decreased resistance, and tardus parvus morphology. The same concepts apply to bypass grafts, when looking for stenosis and occlusion, with additional evaluation at the anastomoses, which are common sites of abnormality. Ultrasound is the primary screening for bypass abnormalities but can be a time-consuming study if used to cover all areas of concern in a patient with diffuse atherosclerotic disease. If diffuse atherosclerotic disease is suspected, other imaging techniques such as computed tomography (CT) or magnetic resonance angiography may be able to survey large areas more effectively.

Lower Extremity Arteries Normal Anatomy Each lower extremity arterial system is primarily supplied from the common femoral artery, which originates from the external

iliac artery at the level of the inguinal ligament and extends caudally a few centimeters until it divides into the superficial femoral artery (SFA) and profunda femoris artery. The profunda femoris artery supplies the femoral head and the deep muscles of the thigh through perforators, as well as the medial circumflex artery and the lateral circumflex artery. The SFA continues along the medial thigh to the adductor canal in parallel with the femoral vein (FV). Below the adductor canal, it becomes the popliteal artery, coursing posterior to the knee and supplying branches of the calf. The popliteal artery branches into the anterior tibial artery and the tibioperoneal trunk. The anterior tibial artery courses laterally, perforating through the interosseous membrane between the tibia and fibula into the anterior compartment of the lower leg. The anterior tibial artery becomes the dorsalis pedis artery in the dorsum of the ankle and along the first intertarsal space of the foot. The tibioperoneal trunk divides after approximately 3 to 4 cm into the posterior tibial artery and the peroneal artery. The posterior tibial artery courses posterior to the medial malleolus of the ankle. The peroneal artery courses through the interosseous membrane above the ankle, and then supplies branches of the lateral ankle and foot.

Ultrasound Examination and Imaging Protocol Lower extremity arterial inflow from the external iliac artery is assessed by groin insonation in supine position, and then each major vessel in the leg is directly evaluated throughout its entire course. Normal arteries have thin smooth walls with anechoic lumens and lack of atherosclerotic plaques or stenosis on grayscale imaging (Fig. 27.2). After gray-scale evaluation, long arterial segments can be screened rapidly with color Doppler to find areas of suspected stenosis. Color Doppler is set to barely fill the lumen in a normal area of the artery. Color aliasing can alert the sonographer to areas of luminal narrowing that need to be evaluated further with spectral Doppler to determine significance. For evaluation of focal abnormalities other than stenosis, the examination may be limited to the general region of concern. The ACR-AIUM-SRU practice parameter for the performance of peripheral arterial ultrasound suggests that lower extremity ultrasound should examine the common femoral artery; the proximal, mid, and distal SFA; and the popliteal artery above and below the knee.2 Other arteries are examined as deemed clinically appropriate. The practice parameter states that these may include “iliac, deep femoral, tibioperoneal trunk, anterior tibial, posterior tibial, peroneal, and dorsalis pedis arteries.” The guideline further suggests that angle-corrected longitudinal Doppler and/or gray-scale imaging should be documented in each normal and at any abnormal segment. Angle-corrected spectral Doppler is recommended proximal to, at, and beyond any suspected stenosis.2 Supine position of the patient is acceptable for the thigh vessels, but a decubitus position may aid evaluation of the popliteal artery. Depending on the symptoms and findings of these arteries, imaging of the iliac arterial system may look for inflow disease, or imaging of the calf arteries may be indicated. Normal outer diameters of the common femoral artery, SFA, popliteal artery, posterior tibial artery, and anterior tibial artery

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FIG. 27.2  Normal Common Femoral Artery Bifurcation.  (A) Gray-scale imaging shows the normal appearance of arterial wall with lack of plaque. (B) Color and spectral Doppler normal triphasic spectral waveform in the profunda femoris artery.

are 8.1 mm, 6.1 mm, 6.0 mm, 2.1 mm, and 2.0 mm, respectively, and these vessels are slightly larger in males.5 The common femoral artery, SFA, and popliteal artery become slightly larger with age, whereas the calf arteries become smaller.5 Laminar flow is present without turbulence or aliasing on color Doppler. A high-resistance triphasic waveform with sharp upstroke and transient flow reversal is typically present in the normal lower extremity arteries on spectral Doppler. A monophasic waveform morphology that does not return to baseline can occur after exercise in normal patients, but can be also seen in lower extremity atherosclerotic disease. For differentiation, the PSV will decrease in the ischemic limb of a patient with peripheral artery disease after exercise, whereas it will increase in a patient with a healthy arterial system. For calf assessment, a posterior medial approach is used for the posterior tibial artery in the midcalf with longitudinal Doppler, and then the artery can be followed proximally and distally. Alternatively, it can be found at the medial malleolus at the ankle and followed cranially. An anterior transducer placement is applied for the anterior tibial artery with the patient lying supine. The anterior tibial artery is well seen along the interosseous membrane near the fibula. The peroneal artery can also be seen from this anterior probe placement; it is more deeply located posterior to the interosseous membrane. A posterior lateral approach may also be used to locate the peroneal artery.

Peripheral Arterial Occlusion Acute arterial occlusion is an emergent situation that can generate severe symptomatology and requires immediate attention. It is usually present in the setting of atherosclerotic disease, although traumatic dissection or embolic disease can occur (Fig. 27.3, Video 27.1). Use of Doppler allows for sensitive and specific demonstration of absent flow, and can differentiate occlusion from stenosis in the lower extremity with 98% accuracy.6 In another study, sensitivities for occlusion of the SFA and popliteal artery were 97% and 83%, respectively.7 In the lower leg, Doppler

FIG. 27.3  Acute Thrombus in the Superficial Femoral Artery.  Note the echogenic material within the arterial lumen. See also Video 27.1, which shows the thrombus to be slightly mobile.

performs better in the anterior and posterior tibial arteries than in the peroneal. Doppler sensitivity for patency of the tibial artery was 93% in a recent study, but with many false positives related to angiography.8 On gray-scale imaging, the anechoic lumen is typically filled with medium-echogenicity thrombus. Using a similar technique as generally performed for detection of deep venous thrombus, the artery can be externally compressed by the transducer to show focal thrombus that is noncompressible. However, if the artery walls completely coapt, then the findings are likely artifactual. On color and spectral Doppler of an occluded artery,

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no flow signal should be detectable (Fig. 27.4). Collaterals suggest chronic occlusion, but there may be a superimposed acute-onchronic thrombotic component (Fig. 27.5, Video 27.2).

Peripheral Arterial Stenosis Detection of stenosis in the setting of atherosclerotic disease is important owing to its role as a precursor to occlusion. Ultrasound is the primary screening tool for detection of stenosis, using a combination of gray-scale, color, and spectral Doppler. Duplex Doppler should be performed in these patients because of its superior performance relative to segmental Doppler pressures.9 In a study of 151 lower extremities, duplex Doppler demonstrated 78% to 95% sensitivity and 97% to 100% specificity for high-grade lower extremity arterial stenosis. Spectral broadening can be seen in nonflow-limiting stenoses less than 50%, with

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FIG. 27.4  Occluded Popliteal Artery.  (A) Spectral Doppler shows high-resistance flow pattern upstream to the occlusion. (B) Occluded portion of the popliteal artery without flow on spectral Doppler. (C) Tardus parvus pattern in the dorsalis pedis distal to the occluded popliteal artery indicates reconstitution of the artery by collaterals.

an otherwise normal waveform (Fig. 27.6). As regional measurements are made in the arteries of the lower extremity, there may be a change noted from normal triphasic arterial morphology to a pulsatile but monophasic waveform that does not return to baseline or demonstrate transient reversal (Fig. 27.7). When this transition is encountered, the artery between these two measurements should be more closely evaluated by color and spectral Doppler to locate a focal velocity elevation associated with visible narrowing of the artery. Gray-scale can characterize overall plaque burden, but calcifications may limit sonographic penetration into the artery lumen (Fig. 27.8, Video 27.3). In a patient with diffuse atherosclerotic disease and generalized calcifications, there may be numerous mild stenoses that have a combined effect to reduce flow pressures to the lower leg without a dominant stenosis. Gray-scale imaging is limited in its ability

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to measure narrowing of the vessel, and velocity and waveform criteria are more widely applied. Color Doppler improves the examination by rapidly depicting areas of turbulent or highvelocity flow that can be further sampled by spectral Doppler for velocity characterization. The main criteria for characterizing arterial stenosis involve waveform morphology, PSV, and end-diastolic velocity (EDV). For velocity criteria, the absolute values and the peak velocity ratio (defined as peak velocity at or in the downstream jet divided by peak velocity of the artery 2 cm upstream) have both been applied effectively. In a study of 338 arterial segments, focal increase in the PSV ratio at the stenosis relative to the

adjacent nonstenotic artery exceeding 2.0 is consistent with at least 50% diameter stenosis when combined with spectral broadening and loss of transient flow reversal in the artery10 (Fig. 27.9). The distal artery waveform will be abnormal with tardus parvus waveforms in the setting of stenosis greater than 50% (Fig. 27.10) but is typically normal if a lesser degree of stenosis is present.10 Direct measurement of PSVs can also be performed. For the femoral-popliteal region of native vessels, a combination of thresholds of PSV greater than 200 cm/sec and ratio above 2 : 1 have been suggested as criteria for greater than 70% stenosis with sensitivity of 79% and specificity of 99%11 (Fig. 27.11).

FIG. 27.5  Occlusion of the Superficial Femoral Artery With a Large Collateral Exiting Proximal to the Occlusion (Arrow).  The presence of a collateral suggests chronic occlusion. See also Video 27.2.

FIG. 27.6  Common Femoral Artery Stenosis.  Color and spectral Doppler shows normal biphasic waveform, with fill-in of the waveform spectral envelope, indicating some degree of stenosis but less than 50%.

A

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FIG. 27.7  Focal High-Grade Stenosis in the Proximal Superficial Femoral Artery (SFA).  (A) Elevated peak systolic velocity at a focal high-grade stenosis in the proximal SFA. (B) Tardus parvus pattern downstream.

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Velocity

FIG. 27.8  Calcification of the Superficial Femoral Artery (SFA).  (A) Severe calcification of the SFA limits ability to see within the artery lumen with gray-scale imaging. Color Doppler is useful to locate a place where spectral Doppler can be sampled. (B) Spectral Doppler of the artery has mild spectral broadening but otherwise normal triphasic waveform, without significant stenosis in this location. See also Video 27.3.

Time

Velocity

2 to 4 cm proximal

Time At the stenosis FIG. 27.9  Blood Flow Velocity Alterations Occur With Stenosis of at Least 50%.  Proximal to the lesion, the flow pattern is normal. At the stenosis, the peak systolic velocity increases in proportion to the degree of stenosis. Alterations in the diastolic portion of the Doppler waveform sampled at the lesion depend on the state of the distal arteries and the severity and geometry of the lesion; diastolic flow may increase dramatically or may be almost absent.

Ultrasound can direct intervention in these patients. Patients with nonacute conditions can benefit from ultrasound to characterize subacute occlusion or embolic disease versus chronic ischemic disease to help the surgeon decide among therapies such as thrombectomy or bypass procedure.12,13 Mapping with Doppler before bypass is very useful. Lesions are characterized by severity using the Trans-Atlantic Inter-Society Consensus (TASC) guidelines.14 Isolated and short category A and B lesions typically are directed to endovascular repair, whereas more

complex or longer lesions, C and D, in general require bypass. In one study of 622 TASC C or D lesions, Doppler mapping successfully identified lesions for intervention with sensitivity of 97% and specificity of 99%.15 Similar high accuracy has been shown in other studies as well.16,17 Doppler can also predict which lesions are suitable for percutaneous transluminal angioplasty with good success.18,19 However, duplex assessment may underestimate the length of stenosis. The lesions treated by angioplasty are generally short

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FIG. 27.10  Iliac Artery Stenosis With Tardus Parvus Waveform.  (A) Tardus parvus waveform in the right common femoral artery indicates severe upstream stenosis or occlusion. (B) Normal velocity biphasic waveform of the contralateral left common femoral artery indicates atherosclerotic disease is in right common or external iliac artery, and not in the aorta (unilateral abnormal waveform).

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FIG. 27.11  Superficial Femoral Artery (SFA) With >70% Stenosis.  (A) Moderately severe stenosis in the SFA with a peak systolic velocity (PSV) of 269 cm/sec. (B) At 4 cm upstream from the stenosis the PSV is 85.0 cm/sec, for a ratio exceeding 3 : 1, indicative of greater than 70% stenosis.

and isolated and have a diameter reduction of greater than 50%. In patients with endovascular intervention and stenting, Doppler can monitor success of the procedure and survey for recurrent stenosis at follow-up. In patients treated for critical limb ischemia, Doppler follow-up should occur every 3 months for the first year.20 Normal triphasic waveforms at the ankle help exclude stenosis, but spectral Doppler is still performed even in the absence of symptoms. For evaluation of stenosis within a stented artery, the best Doppler criteria to characterize SFA in-stent stenosis of 80% or greater include a combination of PSV above

275 cm/sec and PSV ratio (the ratio of the highest PSV within the stent to the PSV in a disease-free arterial segment 3 cm above the stented area) above 3.5.21 In patients with stent repair of SFA stenosis, Doppler and CT angiography have strong agreement.22

Aneurysm An aneurysm occurs when weakness of the arterial layers allows expansion of the arterial caliber beyond normal limits. Aneurysms of the peripheral arteries are uncommon, but most are found in

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FIG. 27.12  Popliteal Artery Aneurysms.  (A) Popliteal artery aneurysm measures 1.2 cm diameter (arrows). (B) In a different patient, a 3.7-cm popliteal artery aneurysm contains low-level echoes and is partially thrombosed (cursors).

the popliteal regions.23 Less commonly, aneurysms are present in the SFA. In more than half of patients with popliteal artery aneurysm, they are bilateral. An association exists between popliteal artery aneurysms and abdominal aortic aneurysm, and thus if a popliteal artery aneurysm is found, the abdominal aorta should be evaluated. There is also an association among peripheral artery aneurysm, tobacco use, and hypertension. Peripheral artery aneurysms may contain clot, which may result in distal emboli with or without soft tissue ischemia and infarction. In these cases, intervention is necessary regardless of aneurysm size. The walls of an aneurysm may calcify, and the presence of calcifications may have some protective effects against rupture. On gray-scale ultrasound, an aneurysm may appear as a fusiform anechoic or hypoechoic mass along the course of an artery. The Doppler signal depends on the amount of thrombus, the size of the neck of the aneurysm, and presence of calcification. Aneurysms may be saccular and commonly occur at branch points. The normal popliteal artery measures 4 to 6 mm in diameter.24 A bulge or focal enlargement of 20% of the vessel diameter constitutes a simple functional definition of an aneurysm (Fig. 27.12). Empirically, a 2-cm cutoff has been used to determine need for intervention.25 For popliteal artery aneurysm, surgical exclusion (ligation of the aneurysm) is the traditional treatment and has high rates of success.26 However, a recent meta-analysis showed that endovascular repair has similar success.27 Doppler ultrasound can be used to monitor the success of the intervention.28 Aneurysm exclusion with covered stents is an increasingly used therapy in place of surgical intervention. Doppler ultrasound can be used to monitor the patency of the stent and confirm the exclusion of the aneurysm from the circulation.29,30

Pseudoaneurysm Pseudoaneurysm describes disruption of an artery with flow in a space beyond the vessel wall. It may arise from any arterial structure and may occur with direct trauma or tumor or inflammatory erosion. Pseudoaneurysms are found in less than 1% of diagnostic angiography examinations and more commonly in coronary angiography.31 Pathologically, the arterial wall has been

at least partially breached. Outer arterial layers, perivascular tissues, clot, or reactive fibrosis contain the pseudoaneurysm sac.32 The mechanism of pseudoaneurysm formation has been well characterized. A hematoma forms adjacent to the artery at the point of injury. Eventual lysis of the clot results in pseudoaneurysm. A pseudoaneurysm is different from an aneurysm in that at least one layer of wall is disrupted. It differs from active extravasation in that blood within the pseudoaneurysm flows back into the feeding artery through a narrowed opening rather than into adjacent tissues. Arteriovenous communication, when present, is used to guide appropriate therapy. In patients with arteriovenous communication, thrombin repair is contraindicated owing to the potential for embolization of the thrombin into the venous system with resultant unintended regions of thrombosis. Gray-scale ultrasound is typically performed first to identify the abnormality. The pseudoaneurysm can appear as a round or oval anechoic structure with or without associated thrombus. When present, thrombus appears isoechoic or hypoechoic; it may be located along the edge of the pseudoaneurysm lumen. Attention should be directed to these areas of extraluminal hematoma or any anechoic collections to determine if there are areas of flow with color Doppler. If flow is detected, spectral Doppler is next performed to characterize arterial versus venous flow and to exclude a superimposed AVF. In the patent portion of a pseudoaneurysm, there may be turbulent or disorganized intraaneurysmal flow with a “yin-yang” appearance. Communication of the sac with the adjacent artery occurs through a neck with a typical “to-and-fro” biphasic flow on spectral Doppler33 (Fig. 27.13, Video 27.4). Measurement of the neck length and diameter of the neck off the artery is performed as part of the assessment before thrombin injection. A neck with larger diameter has clinical implications because these are less successfully treated by thrombin injection. If the sac is thrombosed, the neck may represent the only patent portion of the pseudoaneurysm. At least one-third of pseudoaneurysm require repair, but spontaneous closure is common for pseudoaneurysm smaller than 1.8 cm in diameter.34 If the sac is patent, ultrasound-guided thrombin

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FIG. 27.13  Common Femoral Artery Pseudoaneurysm.  (A) Common femoral artery pseudoaneurysm with “yin-yang” color flow pattern in the pseudoaneurysm (arrows). (B) Spectral Doppler of the pseudoaneurysm neck shows a high-velocity “to-and-fro” pattern. (C) Measurement of the length of the neck from the common femoral artery to the pseudoaneurysm (calipers). (D) Measurement of the diameter of the neck (calipers) off of the common femoral artery indicates size of hole in artery; a “rent” in the artery is less amenable to thrombin injection. It is preferable to measure the diameter in gray-scale because color may overestimate the diameter, but sometimes the neck cannot be seen without color (as in this case). See also Video 27.4.

injection into the pseudoaneurysm to thrombose is commonly performed, with a success rate of 94% to 97% without surgical intervention.35-37 Treatment with sonographically guided direct compression has been used in the past but is less successful (up to 85% pseudoaneurysm thrombosis).38

Arteriovenous Fistula The term “fistula” describes an abnormal communication between the arterial and venous circulations. There is disruption through all layers of the arterial wall as well as a focal disruption of a nearby venous structure, allowing communication from high– arterial pressure to low-pressure veins. This communication bypasses the capillary bed. It can be congenital, acquired, or

rarely spontaneous in nature. Fistulas may be seen after autologous vein bypass grafting39 and do not appear to affect patency of the graft.40 In the absence of bypass graft, most are acquired and usually associated with a history of trauma.41 A traumatic arteriovenous fistula may course from normal artery to normal vein in the setting of trauma, but congenital arteriovenous malformations (AVMs) may occur with associated abnormal vascular structures. Many are asymptomatic. However, symptomatic AVFs do not typically spontaneously resolve and often require surgery.42 Gray-scale imaging may show very little arterial abnormality in a traumatic fistula, but the cluster of dilated structures of an AVM can be identified. In either abnormality, there may be venous

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FIG. 27.14  Common Femoral Artery to Common Femoral Vein Arteriovenous Fistula (AVF).  (A) Color Doppler shows common femoral artery to common femoral vein AVF. Note the adjacent tissue vibration artifact (arrowheads). (B) Arterialized turbulent flow is seen within the vein just downstream to the AVF. See also Video 27.5.

dilation. Color Doppler ultrasound is the best noninvasive imaging modality to evaluate AVF or AVM and may show a large cluster of tortuous vessels with abnormal hyperemic flow. Spectral Doppler waveforms of the inflow arteries feeding the AVF may show low-resistance flow because they bypass the capillary bed. Doppler can show arterialized waveforms in the venous structures near the AVF. Tissue vibration artifact is commonly seen with AVFs, consisting of color pixels erroneously placed in the adjacent soft tissue by the ultrasound scanner because of the marked turbulence of the AVF. If the tissue vibration artifact is seen, a search should be made for an AVF. The arterialized waveform may be better seen during the Valsalva maneuver because with the increased thoracic pressure it causes, normal antegrade venous flow is decreased (Fig. 27.14, Video 27.5).

Lower Extremity Vein Bypass Grafts Bypass grafts may use arterial segments or veins for arterial revascularization. Like bypass conduits in other portions of the body, these have potential complications that can limit their functionality. Failures soon after surgery may result from poor bypass conduit selection or surgical technical factors such as poor selection of the sites for anastomosis. In addition, the valves of an autologous vein may not be fully lysed during surgical preparation. Although completion imaging is commonly performed at the time of surgery, a recent study showed no improvement in graft survival in patients with intraoperative completion angiography or ultrasound.43,44 In the longer term, fibrosis may occur at the site of a vein valve, or there may be intimal hyperplasia at an anastomotic region. If the bypass survives long enough, the underlying atherosclerotic disease may affect the bypass and inflow vessels to limit function. For synthetic grafts, the characterization of occlusion is similar to the native vessels, with

absence of flow on color or spectral Doppler. Echogenic thrombus may be identified within the graft on gray-scale technique. Ultrasound is a good technique to identify lesions that are likely to result in native vein bypass graft failure. Once the arterial bypass graft has been created, ultrasound is the primary screening modality; Doppler surveillance with revisions when needed is cost-effective.45 The diagnosis depends on visible identification of stenosis on gray-scale imaging in combination with characterization by color and spectral Doppler. Normal triphasic or biphasic waveforms in the ankle arteries distal to the bypass suggest patency of the bypass. Generalized reduced or monophasic flow velocities in a graft are concerning for disease, and further search for a focal abnormality should be performed. Color Doppler sonography can be used to search for areas of aliasing, and subsequent spectral Doppler evaluation for velocity changes is then performed. When a stenosis is detected in a nonbranching vessel, a velocity ratio can be applied to evaluate significance. The PSV ratio is calculated by dividing the PSV at the stenotic site by peak velocity in the graft 2 cm upstream. A PSV ratio of at least 2.0 corresponds to at least 50% diameter stenosis.46,47 Likewise, a PSV above 180 cm/sec has been associated with stenosis of greater than 50% diameter47 in lower extremity bypass vein grafts (Fig. 27.15, Video 27.6). Several ultrasound parameters, including PSV ratio, are associated with future bypass graft dysfunction. Once the PSV ratio measures at least 3.5 to 4.0, showing severe stenosis, treatment should be considered if it has not been performed at less severe degrees of stenosis, even in less symptomatic patients.46,47 A recent study of Doppler and CT showed that patients with PSV ratio above 3.5 were at high risk for graft failure, whereas high-grade stenosis on CT did not correlate as well with graft failure.48 Velocity criteria for severe stenosis used by Wixon and

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colleagues suggest that PSV above 300 cm/sec and PSV ratio above 3.5 should direct the patient to intervention of a vein graft stenosis. In patients who meet these criteria, the intervention should be immediate if flow velocity within the graft falls below 45 cm/sec.45 Decreased flow relative to a prior study is also a worrisome finding on spectral Doppler. In surveillance of vein grafts by Doppler with intervention on stenotic lesions, there is increased survival of the surveillance group. In patients with greater than 70% stenosis, 100% of grafts failed without revision, but only 10% failed with ultrasound detection and a subsequent revision pathway.49 Patients with venous bypass graft may form pseudoaneurysms or true aneurysms, but these are rare. When present, they occur most frequently in the anastomotic regions. In a study of saphenous vein grafts, only 10 of 260 (4%) developed true arterial aneurysm,50 with higher incidence in patients with preexisting aneurysm and in males. The average time to diagnosis was 7 years after graft placement.51

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FIG. 27.15  Superficial Femoral Artery Bypass Graft.  (A) Color and spectral Doppler show normal biphasic flow in the proximal bypass graft, with a peak systolic velocity of 83.5 cm/sec. (B) Grayscale imaging in the midcalf shows a focal area of narrowing or thrombosis (arrow). (C) Spectral Doppler at the stenosis with aliasing and a peak velocity of 253 cm/sec, consistent with at least 50% stenosis. See also Video 27.6.

Upper Extremity Arteries Normal Anatomy Each upper extremity arterial system is supplied from either the brachiocephalic artery (right) or the subclavian artery (left) in patients without normal anatomic variations. The artery is anterior to the vein when insonated from the supraclavicular fossa. The subclavian artery courses laterally and becomes the axillary artery once it is beyond the lateral margin of the first rib. The axillary artery courses medially over the proximal humeral head to the inferior margin of the pectoralis muscle, where it becomes the brachial artery. The brachial artery typically courses along the medial upper arm to the antecubital fossa and divides into the radial, ulnar, and smaller interosseous arteries. Occasionally, there is high brachial artery bifurcation above the antecubital fossa52 (Fig. 27.16). Regardless of the level of origin, the radial and ulnar branches extend to the wrist. On gray-scale imaging, normal upper extremity arteries have smooth

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FIG. 27.16  High Brachial Artery Bifurcation.  High brachial artery bifurcation, with two arteries (A) (radial and ulnar) and their paired accompanying veins (V), above the antecubital fossa.

walls with anechoic lumens and lack of atherosclerotic plaques or stenosis, similar to lower extremity arteries. Laminar flow is present without turbulence or aliasing on color Doppler. A similar high-resistance triphasic waveform with sharp upstroke and transient flow reversal is typically present in the upper extremity arteries on spectral Doppler.

Ultrasound Examination and Imaging Protocol Higher frequency imaging is usually possible owing to decreased size of the arm with respect to the leg. The subclavian artery, axillary artery, and brachial artery are evaluated to the level of the elbow. Both upper extremities should usually be insonated so that the symptomatic side can be compared with the asymptomatic. The ipsilateral innominate artery should be evaluated to determine an abnormal inflow etiology of the problem when the subclavian artery waveform is abnormal. In the forearm, imaging of the radial and ulnar arteries is the key to most diagnoses. The ACR-AIUM-SRU practice parameter for the performance of peripheral arterial ultrasound suggests that upper extremity ultrasound should examine the subclavian artery, axillary artery, and brachial artery.2 Other arteries are examined as deemed clinically appropriate. It states that these may include “innominate, radial, and ulnar arteries, and the palmar arch.” The guideline further suggests that angle-corrected longitudinal Doppler and/ or gray-scale imaging should be documented in each normal and at any abnormal segment. Angle-corrected spectral Doppler is recommended proximal to, at, and beyond any suspected stenosis.2 Arterial Occlusion, Aneurysm, and Pseudoaneurysm Upper arm arterial occlusion is usually the result of trauma, often iatrogenic. The rate of radial artery occlusion after artery access for coronary angiography may be as high as 30.5%, although lower rates are also reported in the literature.53 For surgical bypass harvest planning, documentation of patency of the palmar arch is an additional component. For detection and characterization of arterial aneurysm, the maximal outer diameters of the aneurysm should be measured in transverse (short axis) with gray-scale

technique. Doppler can differentiate the patent component from mural thrombus. In pseudoaneurysm characterization, the size and Doppler components are also measured, but the pseudoaneurysm neck is also evaluated with spectral Doppler as detailed earlier in the section on lower extremity arteries (Fig. 27.17, Video 27.7 and Video 27.8). If there is concern for AVF, both the arterial inflow portion and venous outflow should be characterized by duplex Doppler within several centimeters of the pseudoaneurysm, because the characteristic arterialization of the downstream venous waveform may be dampened farther away from the fistula. Turbulent flow through the fistula may affect surrounding tissues causing a tissue reverberation artifact, which may be the first clue that an AVF is present.

Arterial Stenosis Atherosclerotic disease can cause upper extremity stenosis but is a less common problem in the arm than encountered in the lower extremities. Gray-scale findings are similar to the lower extremities and include intimal plaques and/or visible irregularity of the vessel lumen. Color Doppler may show aliasing with turbulent flow similar to those findings seen in lower extremity arterial stenosis. On spectral Doppler, velocity criteria are not well defined for the upper extremity arteries. However, for a stenosis in most nonbranching arteries, a greater than 2 : 1 PSV ratio of the stenosis relative to the upstream artery within 2 to 4 cm is consistent with at least 50% diameter stenosis. Depending on the timing and whether collaterals have formed, this degree of stenosis may or may not be symptomatic or clinically significant (Fig. 27.18). Subclavian Stenosis Subclavian stenosis most commonly occurs proximal to the origin of the left vertebral artery. In a subset of patients, flow to the arm is provided by filling through the vertebral artery via retrograde flow. If this reversed flow is significant, there can be a steal phenomenon (“subclavian steal”) from the brain, leading to dizziness with certain arm movements as additional flow is diverted to the arm. In these patients, the vertebral artery waveform should be insonated (Fig. 27.19, Video 27.9). Transient early systolic deceleration with resultant transient cessation of antegrade flow or transient reversal of flow (Fig. 27.20) correlated with subclavian artery mean diameter stenosis of 72% and 78%, respectively.54 Similar stenosis can occur in the right subclavian artery, but less frequently. If these abnormal vertebral artery waveforms are seen, an attempt should be made to directly visualize a stenosis by gray-scale and duplex Doppler in the subclavian artery itself. Thoracic Outlet Syndrome In distal upper extremity ischemic symptoms, embolic or traumatic injury (commonly iatrogenic) to the artery should also be considered. If embolic phenomena are seen, evaluation for thoracic outlet syndrome should be considered. In patients with symptoms elicited by specific positioning of the arm, thoracic outlet syndrome is a form of arterial stenosis that should be considered. It occurs by external compression of the artery by adjacent muscles during abduction of the arm, and this narrowing

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can affect the waveform morphology of the downstream arteries.55 Bone and rib anomalies frequently contribute to the pathology.56 The velocities in the artery should be evaluated during adduction or neutral position then compared with velocities and waveforms in abduction. Over time, the artery may become injured, and this can lead to occlusion and formation of emboli, which may also be visible sonographically. These emboli can then migrate distally within the upper extremity to cause pain in regions such as the hand. For sonographic evaluation of thoracic outlet syndrome in the proper clinical presentation, it is important to begin by insonating the arteries with the arm in neutral position for baseline waveform characterization. Waveforms are acquired from the forearm arteries with the patient sitting comfortably in an upright, seated position. Once the baseline morphology is clearly defined, the arm is moved into the inciting position, usually with abduction and elevation of the arm with external rotation. A combination of inspiration, breath holding, neck extension, and neck turn to the affected side, known as the Adson maneuver, may elicit a positive finding on Doppler.57 The

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FIG. 27.17  Radial Artery Pseudoaneurysm.  (A) Large radial artery (*) pseudoaneurysm with rent in arterial wall (arrows). (B) Color Doppler shows typical “yin-yang” flow in pseudoaneurysm. (C) “To-and-fro” flow in pseudoaneurysm neck. See also Video 27.7 and Video 27.8.

waveform is monitored as the arm is moved into a variety of positions to elicit symptoms. If abnormal waveforms are not readily apparent, a variety of positions should be tested (Fig. 27.21). If positive, a diminished waveform should be apparent in the arteries of the forearm. Once this has been identified, it may be helpful to repeat the baseline and positive results to show reproducibility of the findings. Further support of the diagnosis includes visible narrowing identified in the subclavian artery, or the presence of an aneurysm in this region, if found.58 Pseudoaneurysms are frequently present in the setting of thoracic outlet syndrome and can lead to embolic events. Care must be taken in the diagnosis because hyperextension can produce arterial flow abnormality in up to 20% of normal volunteers.59

Radial Artery Evaluation for Coronary Bypass Graft Another use of Doppler in bypass patients is to determine suitability of the radial artery for coronary artery grafting. The ulnar artery typically provides the dominant source of blood

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flow to the hand. The ulnar artery supplies the superficial palmar arch, which is often incomplete. The radial artery supplies the deep palmar arch, which is more commonly complete, in communication with the ulnar artery. If the superficial palmar arch in the hand is patent, thus allowing flow to the entire hand through the ulnar artery, then the radial artery is harvested. Thus evaluation of palmar arch patency is necessary before harvest. Doppler evaluation of patency is more accurate than the modified Allen test on physical examination, because only about 5 of 43 (12%) patients with an abnormal modified Allen test result will have abnormal Doppler findings.60 A small linear array 12- to 15-MHz “hockey stick” transducer initially is used to determine antegrade flow of the ulnar artery and radial artery at the wrist. With duplex Doppler, arterial flow to the hand in the superficial palmar arch at the thenar eminence near the crease of the base of the thumb is characterized first with normal distal radial artery inflow. Subsequently, the radial artery is transiently occluded by direct compression of the radial

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FIG. 27.18  Subclavian Artery Stenosis Due to Atherosclerotic Disease.  (A) Focal hypoechoic approximately 50% stenosis (arrow) in the proximal subclavian artery, outlined by color Doppler. (B) Peak systolic velocity (PSV) elevation at 208 cm/sec at stenosis. (C) PSV 2 cm upstream (proximal) to stenosis is 89.1 cm/sec for a PSV ratio of greater than 2 : 1.

artery at the wrist, and the resultant spectral Doppler waveform is evaluated. Care should be taken during examination not to hyperextend the hand with regard to the wrist, because a falsenegative examination finding may incorrectly suggest lack of patency of the arch. In patients with a patent superficial palmar arch, there should be reversed flow of the radial artery in the hand, measured at the thenar eminence or in the region of the snuff box between the first metacarpal and second carpal bone.61,62 If there is no flow or absent reversed flow, then the radial artery of that upper extremity is not suitable for harvest owing to an incomplete arch (Fig. 27.22). Increased flow in the ulnar artery may also occur during radial artery compression if the arch is patent.63

PERIPHERAL VEINS Evaluation of the upper and lower extremity venous system is primarily performed with sonography. Useful applications

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FIG. 27.19  Subclavian Steal Phenomenon.  (A) Reversed flow in the right vertebral artery. Note that artery and vein are the same color, indicating abnormal flow direction in one of the vessels. (B) Magnetic resonance imaging confirms significant stenosis in the subclavian artery just distal to the vertebral artery (arrow). See also Video 27.9.

FIG. 27.20  Subclavian Steal With Transient Flow Reversal in the Vertebral Artery.

include evaluation for thrombus, localization for venous access procedures, preoperative venous mapping for hemodialysis AVF and graft placement, and postoperative hemodialysis AVF and graft assessment. Key aspects of venous Doppler imaging include knowledge of anatomy, scanning technique, and attention to detail. The most common indication for venous Doppler ultrasound is to identify deep venous thrombosis (DVT). Undiagnosed and untreated DVT can result in fatal pulmonary embolism (PE). Sudden death is the first symptom in about 25% of people who have PE64 (Fig. 27.23). Clinical evaluation of the peripheral venous system is frequently difficult, nonspecific, and often inaccurate. Clinical decision rules to improve pretest probability are recommended by the American College of Physicians and the American

Academy of Family Physicians.65-67 The Wells criteria generate a score for certain physical examination findings and pertinent clinical history.68 Clinical factors associated with increased probability of DVT include active cancer, immobilization, localized tenderness along the distribution of the deep venous system, swollen extremity, pitting edema localized to the symptomatic extremity, collateral superficial veins, and previously documented DVT. A modification of the Wells score creates two groups: DVT unlikely or DVT likely.69 Current guidelines recommend a D-dimer test for those with low risk.70,71 The D-dimer test measures a degradation product of fibrin and has a high negative predictive value that is sensitive, but not specific for DVT.72 If the D-dimer test result is positive, the patient should be evaluated with venous Doppler. As with patients without cancer, the combination of low probability and negative D-dimer result can exclude DVT in cancer patients.73,74 In practice, many patients do not undergo this workup.75 Going directly to sonography is frequently faster than waiting for workup results and may offer an alternative musculoskeletal diagnosis such as popliteal fossa cyst. Also, in cases of technically limited sonographic evaluation of the more central deep venous system (iliac veins and inferior vena cava [IVC]), magnetic resonance venography or CT venography may be more sensitive.76

Sonographic Examination Technique The superficial location of the upper and lower venous system allows the use of linear, higher frequency transducers. The highest frequency linear transducer that still gives adequate penetration should be used to optimize spatial resolution. Typically the examination is best performed using a 5- to 10-MHz linear array transducer, with application of the higher frequency range in upper arm, forearm, calf, and more superficial veins. A curved array or sector probe in the 3- to 5-MHz range may be necessary

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FIG. 27.21  Thoracic Outlet Syndrome.  (A) Normal baseline subclavian artery waveform. (B) Altered waveform during hyperextension, with compression against the clavicle causing stenosis.

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FIG. 27.22  Radial Artery Evaluation for Coronary Bypass Graft.  (A) Patent palmar arch, with reversal of flow in the superficial palmar arch on radial artery compression at the wrist. (B) Incomplete palmar arch, with lack of flow in the superficial palmar arch on radial artery compression at the wrist.

in very large patients or those with substantial extremity edema. Gray-scale imaging should include compression and should be performed in the transverse plane. Color flow and spectral analysis are the most common applications of Doppler sonography, with occasional use of power Doppler. Both techniques evaluate the disease process in the peripheral veins and give additional information regarding altered venous hemodynamics. Anatomic and functional detail makes sonography a valuable tool. Color Doppler sonography can be used to evaluate venous segments that cannot be directly assessed by compression, such as the subclavian veins. Power Doppler provides improved detection of very slow flow, especially in small veins. All spectral Doppler waveforms should be obtained in the longitudinal plane.

Lower Extremity Veins Normal Anatomy Deep Venous System. The venous anatomy of the leg is illustrated in Fig. 27.24. The common femoral vein (CFV) begins at the level of the inguinal ligament as the continuation of the external iliac vein and extends caudally to the bifurcation into the femoral vein (FV) and the profunda femoris vein, which lie medial to the adjacent artery. The FV courses medially to the adjacent artery through the adductor canal in the caudal thigh. The term “femoral vein,” previously called the “superficial femoral vein,” should be used to avoid clinical confusion regarding the deep versus superficial venous system.77 The popliteal vein (PV) represents the continuation of the FV after its exit from the adductor canal in the posterior caudal thigh. The PV is located superficial

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FIG. 27.23  Pulmonary Emboli.  (A) Axial CT with contrast shows a large saddle pulmonary embolus extending into the left and right pulmonary arteries (arrows). (B) Maximum-intensity projection coronal CT with contrast in the same patient shows extent of bilateral pulmonary emboli (arrows).

Common femoral vein

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Great saphenous vein

A Profunda femoris vein Femoral vein Adductor magnus muscle

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Anterior tibial veins Small saphenous vein

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Peroneal veins Posterior tibial veins

E FIG. 27.24  Venous Anatomy of the Lower Extremity.

to the artery and courses through the popliteal space into the proximal calf. Duplication of the FV can be seen in about 30% of patients.78 Duplication of the FV can also be segmental. It has been shown that these anatomic variants are associated with increased incidence of DVT.79,80 About 40% of patients with multiple vessels within the popliteal fossa arise from a high confluence of the posterior tibial and peroneal veins, rather than true PV duplication.78 Description of these anatomic variants assists in avoiding a missed diagnosis on follow-up examinations. The paired anterior tibial veins arise from the PV and course laterally along the anterior calf to the dorsum of the foot. The tibioperoneal trunk originates from the PV slightly caudal to the anterior tibial veins and bifurcates into the paired posterior tibial veins and peroneal veins. The peroneal veins course medial to the posterior aspect of the fibula, whereas the posterior tibial veins course through the posterior calf muscles posterior to the tibia and along the medial malleolus. Deep veins in the gastrocnemius and soleus calf muscles do not have an adjacent artery and are a common site of acute calf vein thrombus in postoperative or high-risk patients.81 Superficial Venous System. Anatomic terminology for the lower extremity superficial venous system was standardized in 2002. The great and small saphenous veins and their branches comprise the superficial venous system of the lower extremities.82 The great saphenous vein (GSV) empties into the medial aspect of the CFV in the proximal thigh superior to the bifurcation of the CFV. The GSV courses along the medial thigh and calf. The normal GSV typically is 1 to 3 mm in diameter at the level of the ankle and 3 to 5 mm in diameter at the saphenofemoral junction. These measurements are important when performing saphenous vein mapping for harvesting an autologous vein graft. The small saphenous vein has a variable insertion into the posterior aspect of the PV and courses along the dorsal calf to the ankle. Measurements for the small saphenous vein are typically

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1 to 2 mm in diameter inferiorly and 2 to 4 mm at the saphenopopliteal junction. In cases of superficial venous insufficiency, both the GSV and small saphenous vein can become abnormally enlarged and tortuous.

Ultrasound Examination and Imaging Protocol The choice of transducer depends on the patient’s body habitus and depth of the vessel to be studied. Typically a high-resolution 5- to 7.5-MHz linear array transducer will be used. For larger patients a lower-frequency (2.5- or 3.5-MHz) curvilinear transducer may be needed. Appropriate gain settings are needed to ensure that the vessels show no artifactual internal echoes and that thrombus is not mistaken for echoes caused by slow-flowing blood. Color Doppler imaging settings must be optimized for sensitivity to slow, low-volume flow. The lower extremity deep venous system should be evaluated from just above the inguinal ligament to the bifurcation of the PV in the upper calf, including compression, color, and spectral Doppler sonography with assessment of respiratory phasicity. The cranial profunda femoris vein and cranial GSV should also be examined. Ultrasound evaluation of the external iliac veins and IVC is helpful to determine extent of documented CFV when the top of the thrombus is not seen in the CFV. The patient is examined in the supine position with the leg abducted and externally rotated with slight flexion of the knee. The most important portion of the examination is venous grayscale compression. The veins of the deep system are compressed in the transverse plane and evaluated in a stepwise fashion every 1 to 2 cm through the level of the adductor canal (Fig. 27.25, Video 27.10). Pressure on the skin with the transducer should be applied to collapse the vein. If the adjacent artery is deforming, pressure application is adequate. Color Doppler is then performed in selected segments to evaluate for patency and any nonocclusive

or hypoechoic thrombus not seen on the gray-scale images. The spectral Doppler waveform obtained is assessed for respiratory phasicity and cardiac pulsatility. The PV is best evaluated with the patient’s leg bent in a frog leg position. Applying hand pressure to the posterior surface of the leg when imaging the adductor canal or creating simulated augmentation by asking the patient to “step on the gas” may aid in visualizing the vein if the veins are difficult to see because of slow flow, increased depth, or significant edema.83 Ultrasound evaluation of the calf veins remains controversial owing to uncertain clinical value and cost-effectiveness. The ACR practice guidelines do not require evaluation of the calf veins. At a minimum, all symptomatic areas should be evaluated, including the calf, to determine the source of symptoms such as superficial varicosities, and thrombophlebitis. Some institutions that routinely evaluate the calf veins start at the PV and track the paired anterior tibial veins, posterior tibial veins, and peroneal veins to the ankle. Calf imaging has become more common and is required for accreditation by the Intersocietal Accreditation Commission,84 but there is not a standard study protocol.85 The American College of Chest Physicians guideline for antithrombotic therapy does not favor routine venous Doppler of the calf veins.65 The more benign natural history of calf venous thrombosis favors management with serial sonographic examination with treatment only if proximal DVT is demonstrated. If calf venous thrombosis is detected, the interpreting physician may not know whether a patient with calf venous thrombosis will be treated. A suggested general statement may include, “If this calf venous thrombosis is not treated, a follow-up in 1 week is recommended to evaluate for progression.”85 Imaging Protocol. The lower extremity venous imaging protocol includes the following images for each deep venous segment:

FIG. 27.25  Normal Femoral Vein (FV) Compression.  Dual transverse image showing noncompressed (left) and compressed FV. (FV is completely compressed in right panel and thus not seen; location marked by arrow.) Accompanying Video 27.10 shows the compression maneuver. A, Superficial femoral artery; V, femoral vein.

CHAPTER 27  Peripheral Vessels 1. Transverse gray-scale image at rest and with compression, or a cine clip of the compression maneuver, of the saphenofemoral junction, CFV, FV (at minimum proximal and distal), and PV. 2. Longitudinal color Doppler with spectral waveform analysis. a. CFV at the level of the saphenofemoral junction and distal portions. If only a unilateral examination is requested, the contralateral CFV is also evaluated. b. PV at a minimum. Consider recording FV as well. c. A separate compression image of the profunda femoris vein at the bifurcation with the FV is not typically obtained, but patency is evaluated on the longitudinal color and spectral Doppler waveform of the CFV bifurcation into the proximal FV and profunda femoris vein. d. If a thrombus is seen in the CFV, the most proximal extent of thrombus should be demonstrated with inclusion of the external iliac veins and IVC in the evaluation.

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e. Document additional musculoskeletal findings (such as popliteal cyst, knee joint effusion, or hematoma if present in the region being evaluated).

Acute Deep Venous Thrombosis There are four findings of acute venous thrombosis: (1) intraluminal material that is deformable during compression, (2) dilation of the vein, (3) smooth intraluminal material, and (4) free tail floating proximally from the attachment of the clot on the vein wall.85 The classic gray-scale findings of acute DVT are noncompressibility of the vessel with direct visualization of the thrombus. With complete acute vein thrombosis, the vein will typically enlarge. Thrombi may completely or partially occlude the lumen, may be adherent to the wall, or may be free floating (Fig. 27.26, Video 27.11). Compression ultrasound for DVT has been shown to have 95% accuracy with 98% specificity.86

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FIG. 27.26  Acute Deep Venous Thrombosis (DVT).  (A) Acute common femoral vein (CFV) thrombus: Compression image in the transverse plane shows acute CFV thrombus. Note that the vein (arrows) is larger than the adjacent artery (A). (B) Longitudinal color Doppler image in the same patient shows acute nearly occlusive common femoral vein thrombus with little flow. See also Video 27.11. (C) Longitudinal image of acute DVT in the profunda femoris vein (*), with nonocclusive extension into the CFV (arrow), and a small amount of thrombus in the femoral vein as well. (D) Transverse color image of acute popliteal vein DVT, with expansion of the vein (arrow) relative to the popliteal artery (A).

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Thrombus within the proximal GSV may be treated as a DVT if within several centimeters of the insertion of the GSV, or more than 5 cm long, according to physician preference.65 If the thrombus within the GSV extends into the CFV, it should be treated as a DVT (Fig. 27.27, Video 27.12). If the top of the thrombus is not seen in the CFV or external iliac vein, an IVC and iliac vein examination should be considered to assess for more central thrombus (Fig. 27.28, Video 27.13).

Residual (Chronic) Deep Venous Thrombosis Differentiation of acute from residual or chronic DVT with imaging and clinical parameters is often difficult. With compression ultrasound, both acute and chronic DVT may show noncompressibility of the vessel. Wall thickening and smaller caliber vein suggest residual or chronic DVT (Fig. 27.29). Because vein noncompressibility can be seen in both acute and chronic DVT, an attempt to differentiate the two is important for the appropriate therapeutic decision. As the thrombus evolves, it loses bulk and the vein may return to normal size or may become smaller in caliber owing to scarring (Fig. 27.30, Video 27.14).

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Residual thrombus will become broadly adherent to the vein wall. Additional chronic findings that may assist in differentiating chronic from acute DVT are echogenic weblike filling defects within the vein (Fig. 27.31), collateral vessels (Fig. 27.32, Video 27.15), and valvular damage with reflux and subsequent chronic deep venous insufficiency.23 Differentiation of acute versus residual or chronic thrombus cannot be performed on thrombus echogenicity alone, although if calcifications are present, there is at least an element of chronic thrombus present87 (Fig. 27.33). If the thrombus is small (several centimeters or less), measurement may be helpful to aid the clinician in determining clinical importance, especially after catheter removal.

Potential Pitfalls Lower extremity potential pitfalls to avoid include the following: 1. Very slowly flowing blood may mimic the appearance of clot (Fig. 27.34, Video 27.16 and Video 27.17); however, compression will be normal.

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FIG. 27.27  Great Saphenous Vein (GSV) Thrombus.  Longitudinal gray-scale (A) and color Doppler (B) images show thrombus within the GSV (arrowheads) without extension into the common femoral vein (CFV) (arrow). (C) In a different patient, longitudinal image shows nonocclusive slightly mobile thrombus within the GSV (*) with extension into the CFV (arrow). See also Video 27.12.

CHAPTER 27  Peripheral Vessels

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FIG. 27.28  Acute Deep Venous Thrombosis (DVT).  (A) Transverse duplex Doppler image shows external iliac vein without demonstrable venous flow (*). The top of the thrombus is not seen, so sonographic evaluation continues to the common iliac vein and inferior vena cava (IVC). (B) Longitudinal image of occluded external iliac vein shows large amount of low-level echoes within the vein, without flow on spectral or color Doppler imaging. (C) Longitudinal image of caudal IVC shows no definite echoes on gray-scale imaging, confirmed with duplex Doppler imaging (not shown). (D) Duplex Doppler longitudinal image of the mid IVC shows no thrombus. (E) Longitudinal gray-scale image of the intrahepatic IVC shows no thrombus. (F) Duplex Doppler longitudinal image of the intrahepatic IVC without thrombus, with normal spectral Doppler waveform. Because the spectral waveform in the left common femoral vein was normal (not shown), thrombus in this patient extended into either the right external or common iliac vein, but not into the IVC. See also Video 27.13.

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FIG. 27.29  Chronic Deep Venous Thrombosis (DVT).  (A) Duplex Doppler longitudinal image of chronic femoral vein DVT, with small vein and peripheral nonocclusive flow. (B) Duplex Doppler longitudinal image of chronic DVT and scarring in a patent popliteal vein, with peripheral irregular residual thrombus.

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FIG. 27.30  Chronic Vein Occlusion With Collaterals.  (A) Transverse image of the popliteal fossa shows multiple small collateral veins (*) in the region of the popliteal vein, adjacent to the popliteal artery (A) in the setting of chronic popliteal vein deep venous thrombosis (DVT) and scarring. (B) Longitudinal image of chronic DVT and scarring in the popliteal vein shows mildly compressible nonocclusive thrombus with some portions adhering to the wall, in a small vein. See also Video 27.14.

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FIG. 27.31  Chronic Deep Venous Thrombosis (DVT) With Vein Web.  Longitudinal gray-scale (A) and color Doppler (B) images show linear weblike chronic DVT (cursors) with patent channels around the web.

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FIG. 27.32  Chronic Common Femoral Vein (CFV) Occlusion With Flow Reversal in the Profunda Femoris Vein (PFV).  Longitudinal gray-scale (A) and color Doppler (B) images show chronic CFV occlusion (arrows) and flow reversal in the PFV (*). The artery (A) is located anteriorly. See also Video 27.15.

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FIG. 27.33  Calcifications Indicating Chronic Thrombus.  (A) Longitudinal image of the femoral vein shows multiple shadowing calcifications (arrows). (B) Transverse image in another patient shows calcification in the popliteal vein (arrow). (C) Same patient as in (B) has new hypoechoic thrombus enlarging the popliteal vein (arrows)— acute-on-chronic deep venous thrombosis (DVT).

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2. Small nonocclusive thrombi in the profunda femoris vein may be missed if not carefully assessed. It is important to remember that DVT may initially be demonstrated in the profunda femoris vein only. 3. Thrombosis of a duplicated FV may be challenging to detect. It is useful to record the presence of this common anatomic variant in the report for comparison in a subsequent study, when only one of several FVs may be thrombosed (Fig. 27.35, Video 27.18).

4. Proximal iliac vein thrombosis may be difficult to demonstrate because of overlying bowel gas. Loss of respiratory phasicity should be recognized as a secondary sign suggesting more proximal thrombosis or obstructive compression by masses or fluid collections (Fig. 27.36). False-negative examination results may occur when the Valsalva maneuver is used while the pelvic veins are evaluated in patients with nonocclusive thrombus in the iliac veins who have well-developed pelvic venous collaterals.

FIG. 27.34  Slow Flow in Patent, Compressible Vein Without Deep Venous Thrombosis (DVT).  Accompanying Videos 27.16 and 27.17 show slow flow in longitudinal plane, and no DVT with compression.

FIG. 27.35  Thrombus in One of Paired Femoral Veins.  Transverse image of compressed paired femoral veins shows that one of the veins does not compress because of deep venous thrombosis (DVT). Arrow shows position of one femoral vein, which is completely compressed and thus not seen. See also Video 27.18. A, Superficial femoral artery; V, thrombus in other (paired) femoral vein.

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FIG. 27.36  (A) Patient with large pelvic mass compressing the left external iliac vein (not shown). Monophasic flow in left common femoral vein (CFV). (B) Normal phasic flow in right CFV.

CHAPTER 27  Peripheral Vessels 5. Occasionally only the actual coapting of the vein walls is seen during compression, the so-called vessel “wink.” The FV can sometimes be difficult to visualize throughout its entire extent. However, isolated FV thrombus is relatively uncommon, reported to occur in fewer than 1% to 4% of patients.83

Complete Venous Doppler Versus More Limited Examinations Complete compression venous Doppler from the inguinal area to the popliteal area is accurate, with less than 1% venous thromboembolic disease at 3-month follow-up in recent analyses.88,89 Limited, less detailed examinations have recently been proposed. A variety of specialties are performing this type of examination in office settings, intensive care units, and emergency departments. The two-point ultrasonography examination of the CFV and the PV using the compression technique has shown that most, but not all, proximal DVTs are detected.90,91 However, this approach requires a serial examination 1 week later to detect propagation of calf thrombus into proximal DVT. Two negative study results, 1 week apart, have shown a low likelihood of DVT in the months following the tests.89 The two-point technique has a 2% to 5.7% chance of detecting DVT on a repeat examination at 2 weeks.89,90 A carefully performed complete thigh venous ultrasound as detailed earlier remains the standard of care. Recommendations for Deep Venous Thrombosis Follow-Up If the patient’s clinical condition worsens, follow-up venous Doppler is warranted. In patients with documented DVT on therapy, a repeat venous Doppler during treatment is rarely warranted. Repeat Doppler should not be requested unless there is a clinical change.85,92 DVT typically lyses or fibroses over 6 to 18 months. Reevaluation near the anticipated end of anticoagulation should be encouraged to establish a new baseline for patients who return with new symptoms suggesting recurrent thrombus, especially those at high risk for recurrent DVT.85 In patients with isolated calf DVT, a follow-up Doppler examination at 1 week is warranted if the patient is not treated. In patients with scarring, pregnant women, patients with technically limited examinations, or patients with calf pain wherein DVT is not identified, it may be prudent to suggest follow-up in 1 week. It has been established that use of two limited examinations, 1 week apart, is a safe strategy.90 In an otherwise normal report, it may be prudent, as a helpful reminder, to state, “If there remains suspicion for DVT or the clinical condition worsens, a follow-up should be considered.”85 Venous Insufficiency The cause of deep venous insufficiency in many patients is venous valvular damage after DVT, which occurs in about 50% of patients with acute DVT.93 The physiology of venous insufficiency entails direct transmission of the hydrostatic pressure of the standing column of fluid in the venous system to the caudal lower extremity. Clinical manifestations include lower extremity swelling, chronic skin and pigmentation changes, woody induration, and eventually nonhealing venous stasis ulcers.

989

Superficial venous insufficiency has a much better prognosis than deep venous insufficiency and is associated with extensive varicosities. Perforating veins communicate between the superficial and deep system and may also become incompetent owing to chronic deep venous insufficiency. For assessment of venous insufficiency, the patient is placed in an upright or semi-upright position, with the body’s weight supported by the contralateral lower extremity. This positioning produces the hydrostatic pressure needed to reproduce venous insufficiency. Spectral analysis is obtained at several levels of the deep and superficial venous system during Valsalva and other provocative maneuvers in the CFV, proximal aspect of the GSV, PV, and saphenopopliteal junction. Distal augmentation is more reproducible and easier when performed by a single examiner.94 Normal veins after brisk distal augmentation will show antegrade flow, with a very short period of flow reversal as returning blood closes the first competent venous valve (Fig. 27.37, Video 27.19). Distal augmentation can be performed manually and more reproducibly with automated devices that inflate every 5 to 10 seconds. Insufficient veins show greater degree of reversed flow for a longer duration (Fig. 27.38). It is important that each vascular laboratory validate its protocol and quantification schemes.

Venous Mapping Vein mapping of superficial leg or arm veins is performed to determine patency, size, condition, and course of superficial veins to be used for vein grafts. Ultrasound mapping is also helpful when a vein is harvested as autologous graft material for a peripheral arterial bypass graft. Any superficial vein can be used, but the GSV is most often suitable for graft purposes. The examination is performed with the patient in the supine or reverse Trendelenburg position. The GSV is identified from the level of

FIG. 27.37  Normal Femoral Vein Valve.  Accompanying Video 27.19 shows normal coapting of valve, which prevents retrograde flow.

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A

Small Parts, Carotid Artery, and Peripheral Vessel Sonography

Augmentation

B

Augmentation

FIG. 27.38  Venous Insufficiency.  (A) Duplex spectral analysis of the popliteal vein shows a normal waveform with distal augmentation. Note no reversal of flow following distal augmentation. (B) Duplex spectral analysis of the great saphenous vein shows prolonged reflux after distal augmentation, consistent with severe superficial venous insufficiency.

Internal jugular vein Brachiocephalic vein Subclavian vein Pectoralis minor muscle Axillary vein Teres major muscle Cephalic vein Brachial veins Basilic vein

FIG. 27.39  Venous Anatomy of the Upper Extremity Veins.

the saphenofemoral junction to as far inferiorly as possible. A superficial vein typically needs to be larger than 3 mm in diameter, but not varicose, to be suitable graft material.95 The small saphenous vein and cephalic and basilic veins are secondary choices and can be used if the GSV has already been harvested or is inadequate.

Upper Extremity Veins Normal Anatomy The venous anatomy of the neck and arm is illustrated in (Fig. 27.39). The deep venous system includes the paired radial and ulnar veins in the forearm, which unite distal to the level of the

CHAPTER 27  Peripheral Vessels elbow to form the brachial veins. The brachial veins in the upper arm join with the basilic vein at a variable location, typically at the level of the teres major muscle. The confluence of the brachial and basilic veins continues as the axillary vein, which passes through the axilla from the teres major muscle to the first rib. As the axillary vein crosses the first rib, it becomes the lateral portion of the subclavian vein. The medial portion of the subclavian vein receives the smaller external jugular vein and the larger internal jugular vein (IJV) to form the brachiocephalic (innominate) vein. Most ultrasound laboratories define the central veins as the brachiocephalic veins and superior vena cava, which often are difficult to visualize sonographically. Because some angiographers include the subclavian vein when they describe the central veins, it is important to be very specific about the vein segment examined when describing sonographic findings. The presence or absence of clinically important central stenosis or thrombosis may be inferred by evaluating the transmitted cardiac pulsatility and respiratory phasicity in the medial subclavian vein and distal IJV.96 The cephalic and basilic veins comprise the most important superficial named veins of the upper extremity. The more laterally located cephalic vein traverses in the superficial soft tissues of the shoulder to drain into the axillary vein in the lateral chest. The basilic vein is located more medially, and typically joins the brachial veins to form the axillary vein.

Ultrasound Examination and Imaging Protocol Upper extremity Duplex evaluation consists of gray-scale compression and color and spectral Doppler assessment of all the visualized portions of the IJV and subclavian, axillary, and innominate veins, as well as compression gray-scale ultrasound of the brachial, basilic, and cephalic veins in the upper arm

A

991

to the elbow. A high-frequency, small-footprint transducer can be applied to the suprasternal notch to better demonstrate the brachiocephalic junction and IVC, often difficult to see because of overlying sternum and lung. Venous compression is applied to accessible veins in the transverse plane with adequate pressure on the skin to completely obliterate the normal vein lumen. The patient is scanned in a supine position with the examined arm abducted from the chest, with the patient’s head turned slightly away from the examined arm. Typically a 5- to 10-MHz linear array transducer will be used, with a higher frequency transducer chosen for more superficial veins. A curved array transducer or sector transducer may be more effective in larger patients, especially in the axillary area, because of its increased depth of penetration and larger field of view. All veins are examined with compression every 1 to 2 cm in the transverse plane. Gray-scale transverse images with and without compression or cine clips during compression are obtained from the cranial aspect of the IJV in the neck to the thoracic inlet caudally (Fig. 27.40, Video 27.20). Longitudinal color and spectral images are obtained. The subclavian vein is evaluated from its medial to lateral aspect with longitudinal color and spectral images, assessing for transmitted respiratory variability, cardiac pulsatility, and color fill-in. To demonstrate the superior brachiocephalic vein and the medial portion of the subclavian vein, an inferiorly angled, supraclavicular approach with color Doppler is necessary. A small-footprint sector probe in or near the suprasternal notch may improve visualization of the brachiocephalic veins and the cranial aspect of the superior vena cava (Fig. 27.41). The midportion of the subclavian vein, located deep to the clavicle, frequently is incompletely imaged. An infraclavicular, superiorly angled approach can be used to demonstrate the lateral aspect of the

B

FIG. 27.40  Normal Internal Jugular Vein (IJV) and Subclavian Vein (SCV) Spectral Doppler Waveforms.  (A) Normal IJV spectral Doppler waveform, with transmitted cardiac pulsatility and respiratory phasicity, with spectral waveform going to the baseline. Accompanying Video 27.20 shows normal IJV compression. (B) Normal medial SCV spectral Doppler, with transmitted cardiac pulsatility and respiratory phasicity, and spectral waveform going to the baseline.

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A

B

FIG. 27.41  Normal Brachiocephalic Veins.  Gray-scale (A), and color and spectral Doppler (B) of left and right brachiocephalic veins (arrows) and cranial superior vena cava (SVC; *).

subclavian vein. In many cases the subclavian vein can be compressed. Accurate spectral waveform evaluation is critical to this examination. Documentation of normal flow in the medial subclavian vein confirms patency of the brachiocephalic vein and superior vena cava, which cannot be examined directly. Each spectral image obtained in the longitudinal plane of the vessel with angle of insonation maintained at less than 60 degrees is evaluated for spontaneous, phasic, and pulsatile flow. Demonstration of transmitted cardiac pulsatility and respiratory phasicity is necessary in the spectral analysis of the caudal IJV and medial subclavian vein. A normal spectral tracing should return to baseline. Absence of pulsatility may be caused by a more central venous stenosis or obstruction (Fig. 27.42).97 Spectral tracings from the medial subclavian vein should be compared with tracings from the lateral subclavian vein. A change between these two tracings suggests midsubclavian vein stenosis. Response to a brisk inspiratory sniff or Valsalva maneuver may assist evaluation of venous patency. During a sniff, the normal IJV or subclavian vein normally decreases in diameter or collapses completely. The Valsalva maneuver will increase the vein diameter, demonstrating response to the increased thoracic pressure and documenting communication with the central vasculature. Patients with significant stenosis or obstruction of the central brachiocephalic vein of the superior vena cava will lose this response.97 The upper extremity venous imaging protocol includes the following images for each deep venous segment: 1. Transverse gray-scale image at rest and with compression, or a cine clip of the compression maneuver of the proximal and distal IJV, subclavian, axillary, and brachial veins. The basilic and cephalic veins are evaluated in the upper arm to the elbow. 2. Longitudinal color Doppler with spectral waveform analysis is performed of the IJV, both proximal and distal portions, as well as the subclavian vein, both medially and laterally,

and the axillary vein. If only a unilateral examination is requested, the contralateral subclavian vein is also evaluated. 3. Evaluation of focal symptomatic areas if present, including the forearm.

Upper Extremity Acute Deep Venous Thrombosis Current literature shows the sensitivity and specificity of venous Doppler ultrasound for upper extremity DVT to range from 78% to 100% and 82% to 100%, respectively.96,98-102 The classic ultrasound finding in acute upper extremity DVT is an enlarged, tubular structure filled with thrombus showing variable echogenicity and absence of color Doppler flow (Fig. 27.43, Video 27.21). Nonocclusive thrombus may show flow outlining the thrombus, with a variable appearance depending on whether the nonocclusive thrombus is acute or chronic. Nonocclusive thrombus usually does not result in enlargement of the vein (Fig. 27.44). When the obstruction is incomplete, nonphasic flow is demonstrated when the luminal narrowing is significant enough to affect the transmitted cardiac pulsatility and respiratory phasicity from the thorax. Attention to detail is important in the normally paired brachial veins to avoid overlooking thrombus in one of the veins (Fig. 27.45, Video 27.22). Evaluation of central thrombus relies on spectral analysis. The presence of a nonpulsatile waveform (similar to portal venous flow) that does not cross the baseline strongly suggests central venous thrombosis, stenosis, or extrinsic compression from an adjacent mass.96 A suspicious waveform should always be compared with the contralateral side to assess a unilateral versus bilateral process. Patel and colleagues103 found that absent or reduced cardiac pulsatility was a more sensitive parameter in patients who had unilateral venous thrombosis, even though respiratory phasicity often was asymmetric. In cases of bilateral subclavian vein or superior vena cava occlusion, a high level of suspicion must be maintained to detect central thrombus or stenosis. Of importance, because of high-volume flow, there may

CHAPTER 27  Peripheral Vessels

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D

E

993

FIG. 27.42  Superior Vena Cava (SVC) Stenosis With Right Peripherally Inserted Central Catheter (PICC) Line.  Abnormal caudal right internal jugular (A), right medial SCV (B), left caudal internal jugular (C), and left medial SCV (D) flow do not go to baseline. (E) Venogram performed during right PICC line replacement shows mild-moderate SVC stenosis (arrows), which was accentuated by indwelling catheter.

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FIG. 27.45  Nonocclusive Thrombus in Brachial Vein.  Transverse noncompressed image of nonocclusive thrombus (*) in one brachial vein in the paired brachial veins. A, Brachial artery. See also Video 27.22. FIG. 27.43  Acute Internal Jugular Thrombus.  Transverse image of a noncompressible internal jugular vein filled with thrombus (*). Arrowhead shows carotid artery. See also Video 27.21.

FIG. 27.44  Nonocclusive Chronic Internal Jugular Thrombus.  Longitudinal color Doppler image of the small-caliber proximal internal jugular vein with irregular thrombus adjacent to wall, with thickened valves (arrows).

be absence of phasicity without stenosis in the central veins if a hemodialysis graft or AVF is present in the upper arm. Unlike the lower extremity, most cases of upper extremity DVT are related to the presence of a central venous catheter or electrode leads from an implanted cardiac device. Approximately 35% to 75% of patients who have upper extremity venous catheters develop thrombosis, and approximately 75% are asymptomatic104-106 (Fig. 27.46, Video 27.23 and Video 27.24). Frequently a fibrin sheath is found adjacent to the catheter and may be seen after catheter removal. It is important to look carefully at the valves for adherent thrombus. Whether the catheter access site is the subclavian vein or the IJV affects the complication

rate. Trerotola and colleagues107 examined only patients who had symptomatic upper extremity DVT and found a greater incidence of DVT in patients who had subclavian venous access than in those who had internal jugular access. The placement of large-bore catheters into the subclavian vein should be avoided, especially in patients who have end-stage renal disease (ESRD) for whom dialysis access is being considered. Subsequent development of subclavian vein stenosis or thrombosis would limit dialysis access possibilities for that upper extremity. Only 12% to 16% of patients who have upper extremity DVT develop PE.108,109 In comparison, 44% of patients who developed proximal lower extremity DVT detected by sonography had a subsequent PE diagnosed clinically.110 Acute pulmonary emboli in patients who have upper extremity DVT tend to occur in untreated patients.111,112 As expected, there is greater risk of PE in catheter-related upper extremity DVT than in upper extremity DVT from other causes.113 Venous stasis and insufficiency caused by venous thrombosis, more commonly seen with LE DVT, are less common and less severe in the upper extremity. The deep venous system in the arm has less exposure to the physiologic hydrostatic high-pressure pump mechanism that is seen in the lower extremity.114,115 Development of extensive collateral venous pathways in the arm and chest after venous thrombosis or obstruction contributes to these differences and may cause greater technical challenge in performing the upper extremity venous Doppler examination, as compared with the lower extremity.

Differentiation of Acute From Residual or Chronic Venous Thrombosis Findings suggesting residual or chronic DVT in the upper extremity include fixed valve leaflets, synechiae, fibrin sheaths, small-caliber veins with noncompressible, thickened walls, and multiple serpiginous veins not paralleling the artery (Fig. 27.47). In some cases of residual or chronic thrombosis, the vein may not be seen in the expected location owing to fibrosis or scarring.

CHAPTER 27  Peripheral Vessels

995

A

B

C

A

FIG. 27.46  Thrombus Associated With Central Lines.  (A) Transverse image shows acute thrombus around peripherally inserted central catheter (PICC) line in the basilic vein. Thrombus completely occludes noncompressible vein. (B) Acute thrombus around PICC catheter in the basilic vein. No flow seen on duplex Doppler in the longitudinal plane. (C) Longitudinal image of the internal jugular vein shows a moderate amount of thrombus around a central line in another patient. See also Video 27.23 and Video 27.24.

B

FIG. 27.47  Collateral Formation in the Upper Extremity After Deep Venous Thrombosis (DVT).  (A) Transverse images of many serpiginous veins (*) in the region of the chronically occluded proximal internal jugular vein near the base of the neck. C, Carotid. (B) Longitudinal duplex Doppler image shows no spectral flow in the small, occluded distal internal jugular vein.

An excellent example is demonstration of only one brachial vein because of chronic scarring from prior DVT of the paired brachial veins116 (Fig. 27.48).

Potential Pitfalls Upper extremity pitfalls to avoid include the following117-119: 1. Axillary versus cephalic vein: The axillary vein of the deep venous system empties into the subclavian vein. The cephalic

vein of the superficial venous system empties into the axillary vein and will not have an adjacent artery along its course. Access to the axilla is generally improved by bending the patient’s elbow and placing the hand near the patient’s head, with an outstretched arm. Excessive abduction may alter the venous waveform, falsely suggesting a more central venous stenosis or obstruction; however, this will resolve with change in position.

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Small Parts, Carotid Artery, and Peripheral Vessel Sonography

FIG. 27.48  Chronic Clot in Brachial Vein.  One of the paired brachial veins is small and chronically occluded (arrow). A, Brachial artery; V, other, normal brachial vein.

2. Distal occlusion of IJV: The distal aspect of the IJV must be demonstrated flowing into the junction with the medial subclavian vein in the area of the brachiocephalic vein. If the vein being traced is located more than a few millimeters away from the carotid artery, it probably represents a collateral vessel, rather than the IJV. Well-developed collaterals may demonstrate normal respiratory phasicity, an additional pitfall. Collateral vessels tend to be multiple and serpiginous and to follow the occluded vein.

HEMODIALYSIS There were 661,648 patients being treated for ESRD by the end of 2013 in the United States, with 117,162 new cases that year.1 Approximately 64% of these patients were undergoing hemodialysis.120 A major cause of morbidity among ESRD patients is related to vascular access procedures and associated complications that increase health care costs in patients undergoing hemodialysis.121 There are two options for permanent access placement for ESRD patients requiring hemodialysis—an arteriovenous fistula (AVF) or a synthetic arteriovenous graft. Mature AVFs are the preferred access when appropriate, because of the lower rates of infection and thrombosis than with graft or catheter access.122-124 Several studies have shown that preoperative ultrasound evaluation of the upper extremity veins and arteries may increase the number of successful AVF placements through optimization of surgical planning125-127 as well as before graft placement in the thigh.128 Although sonographic postoperative hemodialysis access evaluation may be beneficial in assessing AVF maturation,129-131 the role of postoperative ultrasound evaluation for the detection of access pathology and early intervention to improve the longevity of a particular access is still being studied.132-139 Ultrasound is useful in evaluation of palpable masses adjacent to the vascular access to differentiate hematoma from pseudoaneurysm. It is also used in the evaluation of the swollen upper extremity in a patient with an AVF or graft, or a swollen lower extremity in a patient with a thigh graft, assessing for outflow

vein stenosis and DVT. Ultrasound is also used in the evaluation of patients with arm and hand pain after access placement to evaluate for symptomatic steal. The surgical creation of an AVF is preferred over a graft when surgically and clinically feasible. Placement of access in the nondominant upper extremity is preferred to allow continuance of daily activities of life while the access site heals; however, a dominant arm AVF is preferred to a graft in most patients. Possible sites of hemodialysis access in order of preference are as follows: (1) forearm AVF (radiocephalic AVF or transposed forearm basilic vein to radial artery AVF); (2) upper arm brachiocephalic AVF; (3) transposed brachiobasilic AVF; (4) forearm loop graft; (5) upper arm straight graft (brachial artery to upper basilic or axillary vein); (6) upper arm axillary artery to axillary vein loop graft; and (7) thigh graft (Fig. 27.49). The cephalic vein is preferred over a basilic vein transposition for fistula formation because the cephalic vein procedure involves less dissection and venous manipulation. Additional, less common access configurations may also be placed based on surgical experience.140

Sonographic Examination Technique Both gray-scale and color Doppler ultrasound techniques should be optimized for venous and arterial imaging as previously discussed in this chapter. A high-frequency linear array 12- to 15-MHz transducer provides optimal spatial resolution and adequate depth penetration to successfully evaluate superficial vascular structures. A lighter-weight transducer with a smaller footprint, such as a hockey stick configuration, can increase the speed and ease of the examination. A lower-frequency linear array 9- to 12-MHz transducer may be needed for adequate penetration in larger patients. A small-footprint curved array transducer may be useful for evaluation of the brachiocephalic vein and distal SVC. It is important to apply light pressure and use plenty of gel so as not to deform the circular shape of the vessels during the mapping examination for accurate vessel diameters. All diameter measurements are of the inner lumen measured in the anteroposterior dimension in the transverse plane. Color and spectral Doppler evaluation are performed in the longitudinal plane with angle correction of 60 degrees or less. Blood flow rate measurements are performed in the longitudinal plane in a straight area that is not curvy. In blood flow rate measurement, the Doppler gate is increased in size to encompass the entire vessel diameter, and is angle corrected to 60 degrees or less, parallel to the posterior vessel wall. Three to five spectral Doppler waveforms are analyzed, using the automatic blood flow rate calculation in most ultrasound scanners, using the formula of time-averaged mean velocity multiplied by the inner vessel diameter. Three measurements at the same location are performed and averaged, to ensure measurement reliability.

Vascular Mapping Before Hemodialysis Access Upper Extremity Attention to technical detail is necessary for optimum ultrasound evaluation for hemodialysis access planning.126,130,141-143 In general,

CHAPTER 27  Peripheral Vessels

Median cubital branch of cephalic vein

Basilic vein Brachial artery AVF anastomosis

997

Brachial artery AVF anastomosis

Cephalic vein Radial artery

Radial artery

AVF anastomosis

A

B

C

Axillary artery

Graft

Graft Brachial artery

Axillary vein

Brachial artery

Graft

D

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F

Great saphenous vein Common femoral artery

Graft

G FIG. 27.49  Most Common Arteriovenous Fistula (AVF) and Graft Placements.  (A) Forearm cephalic vein–radial artery AVF. (B) Upper arm cephalic vein–brachial artery AVF, using the median cubital branch of the cephalic vein for the anastomosis. (C) Upper arm basilic vein–brachial artery AVF. (D) Forearm loop graft. (E) Upper arm straight graft. (F) Upper arm loop graft. (G) Thigh loop graft. (Reproduced with permission from Robbin ML, Lockhart ME. Ultrasound evaluation before and after hemodialysis access. In: Zweibel WJ, Pellerito JS, editors. Introduction to vascular ultrasonography. 5th ed. Philadelphia: Elsevier; 2005. p. 325-340.158)

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Small Parts, Carotid Artery, and Peripheral Vessel Sonography

FIG. 27.51  Heavily Calcified Radial Artery at the Wrist.  Longitudinal image shows heavy arterial wall calcification (arrows).

FIG. 27.50  Sonographic Evaluation of the Forearm Veins With Patient’s Arm Comfortably Resting on a Surgical Stand.

it is easier to map all the upper extremity arteries and veins on the same side at one sitting so the surgeon has adequate information if vessel character at surgery is suboptimal and another access site needs to be chosen. If a suitable site for AVF creation is not found on the arm evaluated, the other arm is evaluated. The patient should be sitting upright for optimal evaluation of the upper extremity arteries and veins, with the forearm resting comfortably on a table or armrest. A tourniquet should be placed after arterial assessment, to assess vein caliber and distention144 (Fig. 27.50). Central venous evaluation to include the IJV and subclavian vein should then be performed with the patient supine, for easier and potentially more accurate waveform assessment. Sonographic assessment of the arterial wall should evaluate the amount of calcification and degree of stenosis or occlusion, if present. Vein walls should be described with as much detail as possible to assess for wall thickening and thrombus, which may limit future venous distention. The literature suggests that preoperative criteria include a minimum intraluminal arterial diameter of 2.0 mm and a minimal intraluminal venous diameter of 2.5 mm to allow successful AVF creation, and a minimum intraluminal venous diameter of 4.0 mm and a minimum arterial diameter threshold of 2.0 mm for grafts.145,146 At least the caudal third of the brachial artery and the entire radial artery are evaluated for intimal thickening, calcification, stenosis, or occlusion, with more extensive evaluation of the brachial and ulnar arteries as warranted, as well as the axillary artery. The severity of arterial calcification may be categorized, depending on surgeon preference, because it may be difficult to

suture into a heavily calcified artery, and the risk of emboli at surgery may be higher123 (Fig. 27.51). The arterial waveform is evaluated for a normal triphasic or biphasic high-resistance flow pattern, and PSV is measured in these regions (Fig. 27.52). A high brachial artery bifurcation is a common anatomic variant and should be suspected when two arteries with accompanying paired veins are seen in the upper arm52 (Fig. 27.53). The two arteries should be followed into the forearm to the wrist to confirm the presence of a high brachial artery bifurcation and to exclude a prominent arterial branch supplying the elbow, less commonly seen. For assessment of veins, the upright-seated position ensures venous distention owing to hydrostatic pressure. For optimal venous distention, the tourniquet should be placed on the arm cranial to the area of interrogation so that the veins are distended. Each vein should be inspected, with compression performed along the entire venous length to exclude thrombus (Fig. 27.54). The tourniquet is first placed in the midforearm. The region of the cephalic vein at the wrist is percussed for about 2 minutes for maximal venous distention, and the cephalic vein inner diameter is measured at multiple points in the forearm (Fig. 27.55, Video 27.25). Thereafter, the tourniquet is placed at the antecubital fossa, and then the proximal upper arm, after segmental vein diameter measurement. Cephalic vein anterior wall distance from the skin can be measured because if the cephalic vein is too deep for easy cannulation, it may need to be superficialized in a subsequent surgery (Fig. 27.56). It is not necessary to measure the distance of the basilic vein from the skin; the vein needs to be transposed for easier access. The median antecubital vein typically connects the cephalic vein to the basilic vein and is often part of the AVF draining vein. The median antecubital vein also can be used in creating an upper arm basilic or cephalic vein AVF and so is commonly evaluated at the mapping ultrasound procedure. The axillary vein, subclavian vein, and IJV should be assessed for compressibility (when possible) and normal waveforms (see Fig. 27.40).

CHAPTER 27  Peripheral Vessels

A

C

FIG. 27.53  High Brachial Artery Bifurcation.  Radial and ulnar arteries (A) and accompanying paired veins (V).

999

B

FIG. 27.52  Preoperative Mapping Ultrasound Meeting Criteria for Arteriovenous Fistula (AVF) Placement.  (A) Arterial evaluation: radial artery diameter of 0.28 cm (cursors). (B) Mild medial calcification in arterial wall (arrows) does not preclude AVF placement. (C) Normal triphasic radial artery spectral waveform.

FIG. 27.54  Preoperative Mapping Ultrasound Meeting Criteria for Arteriovenous Fistula (AVF) Placement.  Venous evaluation: cephalic vein in the midforearm is 0.27 cm (+ cursors). Anterior vein wall depth is 0.18 cm from skin (X cursor).

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FIG. 27.55  Thick-Walled Cephalic Vein With Chronic Thrombus.  This vein may not dilate normally after arteriovenous fistula (AVF) placement and should not be chosen for a potential AVF draining vein. See accompanying Video 27.25.

FIG. 27.56  Cephalic vein is quite deep from the skin surface (0.9 cm; X cursor), and may need to be superficialized after arteriovenous fistula creation.

Ultrasound Examination and Imaging Protocol Upper Extremity. After assessment of the brachial and radial arteries, the inner luminal diameter of the brachial artery 2 cm proximal to the antecubital fossa, and the radial artery at the wrist are measured, along with the axillary artery diameter. Using sequential tourniquet placement and after wrist percussion of the cephalic vein region, the cephalic vein inner diameter is measured at the wrist, midforearm, and proximal forearm (approximately 4 cm from the antecubital fossa). The proximal forearm measurement is used to evaluate the length of vein available to surgically move the vein from the forearm to the brachial artery in upper arm AVF creation. The cephalic and basilic vein diameters are measured at the antecubital fossa and mid and cranial upper arm. Distance of the anterior wall of the cephalic vein to the skin surface is measured. The axillary vein diameter is measured. The subclavian vein and IJV are assessed in the longitudinal plane with color and spectral Doppler assessment, and IJV compression is performed to assess for thrombus, stenosis, and occlusion.

Subclavian and internal jugular spectral Doppler waveforms are assessed for respiratory phasicity and transmitted cardiac pulsatility. Thigh. Once options to place AVF and grafts in the upper extremity are exhausted, the thigh graft becomes a viable option. Thigh grafts are similar to upper extremity grafts in length of time to permanent failure, with a trend toward increased loss because of infection.147 Thigh grafts are superior to dialysis via a catheter.148 If heavy arterial common femoral or superficial femoral arterial calcification is found at ultrasound, pelvic CT may be useful to determine the degree of atherosclerotic disease present. Careful sonographic assessment of atherosclerotic calcification and stenosis may limit immediate graft failure at surgical placement.128 Thigh graft creation has typically been at the common femoral artery and vein (Fig. 27.57). An alternate place to anastomose the venous end of the graft is the GSV, to preserve the CFV when graft revision is necessary. However, to preserve proximal vasculature for graft revision, and potentially because of fewer infectious complications, midthigh grafts are now being increasingly placed in the mid SFA and superficial femoral vein.149 Technical considerations for mapping the arteries and veins of the thigh for hemodialysis graft placement are similar to mapping the upper extremity as described earlier, although a lower-frequency linear transducer may be necessary because of greater thigh size. Evaluation of the degree of arterial calcification and the presence of thrombus is carefully performed in the thigh. More central stenosis or obstruction is assessed by spectral Doppler evaluation of the CFV and common femoral artery. Distance of the vein to the skin is not measured, because typically only thigh grafts are surgically created. A tourniquet is not used in sonographic thigh graft mapping. The common femoral artery and vein inner luminal diameters are measured, and evaluated for the degree of atherosclerotic calcification. Spectral and color Doppler evaluation of the common femoral artery and vein are performed to evaluate for more proximal stenosis or occlusion. SFA waveforms are also assessed for normalcy. The length of the GSV, which is at least 0.4 cm inner diameter, is measured from its insertion into the CFV extending distally. Inner diameter measurements of the proximal and mid superficial femoral artery and FV are obtained. Compressibility of the veins assessing for thrombus and wall thickening is performed.128

Arteriovenous Fistula and Graft A surgically created hemodialysis access can have a variety of complications, and most of these can be successfully evaluated by ultrasound. Operative notes and pertinent patient history should be reviewed before sonographic evaluation of hemodialysis access. An overall ultrasound scan is performed initially to obtain an overview of the access anatomy and anastomoses. When the general layout is known, sonographic assessment is performed with duplex Doppler sonography, typically in a seated patient with his or her arm resting comfortably on a table. The caudal third of the feeding artery is assessed for stenosis, and the intraluminal diameter is measured in the transverse plane using gray-scale techniques. The feeding artery is further assessed with

CHAPTER 27  Peripheral Vessels

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color and spectral Doppler in the longitudinal plane to document normal low-resistance flow (Fig. 27.58). Measurements of PSV and EDV can be obtained in the feeding artery, and at least at the anastomosis(es). There may be multiple anastomoses in the case of a graft. The draining vein of the AVF or graft is inspected for wall thickening, stenosis, and thrombosis along its entire length.143 If a stenosis is seen, the highest PSV either within the stenosis or in the jet downstream from the stenosis is measured, using angle correction parallel to the jet if different from the angle with the posterior vascular wall, keeping the angle to 60 degrees or less. The PSV 2 cm upstream to the stenosis is measured, and a PSV ratio of the PSV at the stenosis divided by the upstream PSV is calculated. A longitudinal gray-scale image is obtained to document any intraluminal thrombus identified within a draining vein or graft. Duplex Doppler should be performed to confirm absence of flow, with use of the more sensitive power Doppler as needed. Description of artery and vein location with regard to the AVF and graft can be difficult. Terminology including cranial and caudal location with regard to a particular anastomosis, and upstream or downstream position,

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FIG. 27.57  Thigh Graft Preoperative Mapping.  (A) Heavy arterial calcification is seen in the common femoral artery (CFA; *) with normal common femoral vein compression (compression not shown). (B) Longitudinal view of the mid superficial femoral artery (SFA) also shows heavy arterial calcification. (C) Spectral Doppler waveform of the mid SFA does not have a normal triphasic or biphasic waveform. These arteries may be too heavily calcified to sew into, and would likely prompt further evaluation of the patient’s arterial inflow to assess whether thigh graft placement is possible in this patient.

may be more useful than the conventional proximal and distal terminology.

Arteriovenous Fistula The feeding artery luminal diameter is measured. Spectral and color Doppler evaluations of the feeding artery are performed to evaluate for arterial stenosis or occlusion. The anastomosis is assessed for visible narrowing with subsequent spectral and color Doppler evaluation. The AVF draining vein diameter is evaluated at several levels from the anastomosis to 15 cm cranial to the anastomosis. The intraluminal draining vein diameter and the depth of the vein from the skin surface are measured at several points cranial to the arteriovenous anastomosis. Access challenges may result with a depth greater than 5 to 6 mm and require superficialization.131,150 The draining vein is interrogated for accessory branches (Fig. 27.59). Intraluminal diameter and distance from the anastomosis are recorded for each identified accessory vein within 10 to 15 cm of the anastomotic site. The flow volume rate measurements are obtained within the midportion of the draining vein of an AVF, typically at 10 cm cranial to the anastomosis. Optimal flow volume measurement is obtained

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E in an area with parallel vessel walls, minimal vessel tortuosity, and no stenosis (Fig. 27.60).

Graft Sonographic evaluation of the forearm or thigh graft is similar to that of the AVF. A normal graft is seen as two echogenic lines that represent strong specular reflection from polytetrafluoroethylene material. A low-resistance flow (arterialized flow) should be seen within a graft. Duplex Doppler evaluation of the feeding artery (including luminal diameter), arterial-graft anastomosis, graft (arterial side and venous side if loop graft), and venous

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FIG. 27.58  Normal Mature Forearm Arteriovenous Fistula (AVF) Ultrasound Evaluation (Radial Artery at the Wrist to Cephalic Vein).  (A) Normal feeding artery internal diameter (cursors). (B) Color and spectral Doppler 2 cm upstream to the anastomosis measures 2.62 m/sec. (C) peak systolic velocity (PSV) measures 3.97 m/sec for a PSV ratio at anastomosis of less than 3 : 1, normal. Visual assessment of anastomosis is also normal, without stenosis. (D) Normal cephalic vein cranial to the anastomosis (cursors show internal diameter measurement). (E) Mid AVF draining vein volume flow rate measurement (in midforearm) is 1000 mL/min.

anastomosis is performed, as well as draining vein and central vein evaluation. Flow volume is assessed within the midgraft (Fig. 27.61), and both arterial and venous limbs if a loop graft. Any points of visible narrowing are further assessed with spectral and color Doppler.

Palpable Focal Masses Near Arteriovenous Fistula and Graft Hematoma. Avascular, hypoechoic lesions adjacent to the AVF or graft often represent postaccess or postprocedure hematomas (Fig. 27.62, Video 27.26). These collections should

CHAPTER 27  Peripheral Vessels

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FIG. 27.59  Accessory Arteriovenous Fistula (AVF) Branch Measurement.  (A) Transverse image of the AVF draining vein (*) shows a branch of 0.24 cm (cursors). (B) Larger accessory AVF branch (cursors) of 0.44 cm may be large enough to sump blood away from the AVF draining vein (*).

FIG. 27.60  Volume Flow in a Fairly Straight Area of an Arteriovenous Fistula (AVF) Draining Vein.

be inspected for echogenic foci or gas. Fluid collections with echogenic foci associated with shadowing suspicious for gas may represent abscess in certain clinical settings. Aneurysm and Pseudoaneurysm. Focal or diffuse aneurysmal dilation of the AVF draining vein may occur as a result of repeated puncture (Fig. 27.63). Pseudoaneurysms may develop within a fistula or graft and often are related to suboptimal compression after cannulation. Color Doppler of a pseudoaneurysm reveals a circular flow pattern termed “yin-yang” (Fig. 27.64, Video 27.27). There may be “to-and-fro” flow identified in the pseudoaneurysm neck. Evaluation of the depth of the anterior wall of the pseudoaneurysm from the skin surface is important to evaluate those pseudoaneurysms in danger of imminent rupture. A unique complication of grafts is the degeneration of graft synthetic material. Irregularity of the graft wall is present, which may be associated with diffuse or focal pseudoaneurysms along the length of the graft wall (Fig. 27.65, Video 27.28).

Arteriovenous Fistula Maturation Evaluation A 6-week postoperative AVF ultrasound is used in some clinical centers for routine evaluation of the AVF to determine its

development toward usability.130 A functioning AVF has a volume flow of at least 300 to 800 mL/min.129,151 Robbin and colleagues showed that when an AVF had a minimum draining vein of 4 mm or larger or a blood flow rate of 500 mL/min or higher, approximately 70% of AVFs were able to be used for hemodialysis. The likelihood of fistula maturation was 95% if both criteria were met. If neither of these criteria was met, only 33% of fistulas were used for hemodialysis.129 Sonographic criteria published by the National Kidney Foundation Kidney Disease Outcomes Quality Initiative suggestive of maturation include a draining vein greater than 6 mm diameter, blood flow rate greater than 600 mL/min, and less than 6 mm skin depth. These criteria may exclude many fistulas that could subsequently provide hemodialysis access. Active investigation is underway with larger, multicenter trials to test these criteria. Etiology of failure to mature such as anastomotic or AVF draining vein stenosis, large accessory veins, or arterial inflow stenosis can be identified and ultrasound used to triage the AVF for intervention.131

Arteriovenous Fistula and Graft Stenosis AVF. Stenoses associated with AVFs are most frequently juxta-anastomotic, followed in frequency by AVF draining vein, with central venous and feeding artery stenosis less common but not infrequent. Stenoses may be clinically relevant owing to resultant flow decrease and can be associated with subsequent thrombosis. Potential sites for AVF stenosis include the feeding artery, juxta-anastomotic region, draining vein, and central veins. Early after placement, juxta-anastomotic stenoses are the most common. Later, AVF draining vein and central vein stenoses are more common, including a “cephalic arch” stenosis in which the cephalic vein enters the subclavian vein in the cephalic vein AVF. A careful directed search to common areas of stenosis is important during the sonographic examination, because stenoses may be short and therefore overlooked. Fistula stenosis is characterized by two criteria: (1) visual narrowing of greater than 50% as assessed on gray-scale imaging, and (2) an elevated PSV ratio of the PSV at or just distal to the stenosis as compared with the PSV measured 2 cm upstream from the site of stenosis. A juxta-anastomotic stenosis is defined by a location within 2 cm of the anastomosis, encompassing both the feeding artery and the draining

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FIG. 27.61  Assessment of Upper Arm Graft (Brachial Artery to Axillary Vein Graft) With Peak Systolic Velocity (PSV) Measurement.  (A) Normal color and spectral Doppler images show artery feeding the graft 2 cm cranial to the arterial anastomosis; PSV measures 3.7 m/sec. (B) Arterial anastomosis: PSV is 5.98 m/sec. PSV ratio is 3 : 1, concordant with visual assessment of a high-grade stenosis.

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FIG. 27.67  Graft or Arteriovenous Fistula (AVF) Draining Vein Stenosis Assessment Using Color and Spectral Doppler With Peak Systolic Velocity (PSV) Measurement.  (A) Visual narrowing in draining vein greater than 2 cm downstream from anastomotic stenosis (therefore draining vein stenosis, not juxta-anastomotic stenosis). (B) PSV measurement of area of greatest narrowing is 8.5 m/sec. (C) PSV 2 cm upstream from draining vein stenosis is 3.4 m/sec for a PSV gradient of >2 : 1, with visual narrowing, consistent with at least 50% stenosis.

B

FIG. 27.68  Graft Venous Anastomotic Stenosis.  (A) Gray-scale image shows significant narrowing at thigh graft– common femoral vein anastomosis. (B) Venous anastomosis peak systolic velocity (PSV) measures 6.1 m/sec in greatest jet. (C) PSV measurement within the graft 2 cm upstream from the venous anastomosis is 2.53 m/sec, for a PSV ratio >2 : 1, and concordant with visual narrowing, consistent with at least 50% stenosis. See also Video 27.29.

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FIG. 27.69  Arterial Steal in a Radial Artery to Cephalic Vein Arteriovenous Fistula (AVF) in the Proximal Forearm.  (A) Grayscale image of anastomosis shows no stenosis. A, Feeding artery; V, draining AVF vein. (B) Reversal of flow direction is seen in the radial artery just caudal (distal to the AVF anastomosis) in the radial artery—arterial steal. (C) Reversal of flow in the distal radial artery at the wrist confirms arterial steal.

B

FIG. 27.70  Severe Subclavian Vein Stenosis.  (A) Monophasic flow in the medial subclavian vein does not return to baseline. (B) Monophasic flow in the caudal internal jugular vein does not return to baseline. (C) Severe stenosis in proximal subclavian vein confirmed at venography before angioplasty.

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FIG. 27.71  Thrombosed Hemodialysis Graft.  (A) No flow seen on spectral Doppler (no flow on color Doppler; not shown). (B) Color and spectral Doppler of artery upstream (cranial) from graft takeoff shows high-resistance waveform expected in graft thrombosis.

mapping, and surveillance of the upper and lower extremity venous system. Preoperative ultrasound evaluation of the veins and arteries before both upper extremity and thigh hemodialysis access placement may decrease complications related to access procedures and improve overall access utility. After access placement, ultrasound is useful in the assessment of complications including stenosis, pseudoaneurysm, steal, and AVF nonmaturation. REFERENCES 1. American College of Radiology (ACR), American Institute of Ultrasound in Medicine (AIUM), Society of Pediatric Radiology (SPR), Society of Radiologists in Ultrasound (SRU). ACR-AIUM-SPR-SRU Practice parameter for the performance of peripheral venous ultrasound examinations 2015. Available from: http://www.acr.org/~/media/ACR/Documents/PGTS/ guidelines/US_Peripheral_Venous.pdf. 2. American College of Radiology (ACR), American Institute of Ultrasound in Medicine (AIUM), Society of Radiologists in Ultrasound (SRU). Practice parameter for the performance of peripheral arterial ultrasound using color and spectral Doppler. Peripheral arterial US. 2014. Available from: https:// www.acr.org/~/media/ACR/Documents/PGTS/guidelines/US_Peripheral _Arterial.pdf. 3. Sanyal R, Kraft B, Alexander LF, et al. Scanner-based protocol-driven ultrasound: an effective method to improve efficiency in an ultrasound department. AJR Am J Roentgenol. 2016;1-5. 4. AbuRahma AF, Jarrett K, Hayes DJ. Clinical implications of power Doppler three-dimensional ultrasonography. Vascular. 2004;12(5): 293-300. 5. Czyzewska D, Ustymowicz A, Krysiuk K, et al. Ultrasound assessment of the caliber of the arteries in the lower extremities in healthy persons—the dependency on age, sex and morphological parameters of the subjects. J Ultrason. 2012;12(51):420-427. 6. Moneta GL, Yeager RA, Antonovic R, et al. Accuracy of lower extremity arterial duplex mapping. J Vasc Surg. 1992;15(2):275-283. 7. Hatsukami TS, Primozich JF, Zierler RE, et al. Color Doppler imaging of infrainguinal arterial occlusive disease. J Vasc Surg. 1992;16(4):527531. 8. Mustapha JA, Saab F, Diaz-Sandoval L, et al. Comparison between angiographic and arterial duplex ultrasound assessment of tibial arteries in patients with peripheral arterial disease: on behalf of the Joint Endovascular and

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Small Parts, Carotid Artery, and Peripheral Vessel Sonography

69. Le Gal G, Carrier M, Rodger M. Clinical decision rules in venous thromboembolism. Best Pract Res Clin Haematol. 2012;25(3):303317. 70. Qaseem A, Snow V, Barry P, et al. Current diagnosis of venous thromboembolism in primary care: a clinical practice guideline from the American Academy of Family Physicians and the American College of Physicians. Ann Fam Med. 2007;5(1):57-62. 71. Segal JB, Eng J, Tamariz LJ, Bass EB. Review of the evidence on diagnosis of deep venous thrombosis and pulmonary embolism. Ann Fam Med. 2007;5(1):63-73. 72. Wells PS, Anderson DR, Rodger M, et al. Evaluation of D-dimer in the diagnosis of suspected deep-vein thrombosis. N Engl J Med. 2003;349(13): 1227-1235. 73. Carrier M, Lee AY, Bates SM, et al. Accuracy and usefulness of a clinical prediction rule and D-dimer testing in excluding deep vein thrombosis in cancer patients. Thromb Res. 2008;123(1):177-183. 74. Geersing GJ, Zuithoff NP, Kearon C, et al. Exclusion of deep vein thrombosis using the Wells rule in clinically important subgroups: individual patient data meta-analysis. BMJ. 2014;348:g1340. 75. Squizzato A, Micieli E, Galli M, et al. Diagnosis and management of venous thromboembolism: results of a survey on current clinical practice. Thromb Res. 2010;125(2):134-136. 76. Spritzer CE. Progress in MR imaging of the venous system. Perspect Vasc Surg Endovasc Ther. 2009;21(2):105-116. 77. Bundens WP, Bergan JJ, Halasz NA, et al. The superficial femoral vein. A potentially lethal misnomer. JAMA. 1995;274(16):12961298. 78. Quinlan DJ, Alikhan R, Gishen P, Sidhu PS. Variations in lower limb venous anatomy: implications for US diagnosis of deep vein thrombosis. Radiology. 2003;228(2):443-448. 79. Simpson WL, Krakowsi DM. Prevalence of lower extremity venous duplication. Indian J Radiol Imaging. 2010;20(3):230-234. 80. Dona E, Fletcher JP, Hughes TM, et al. Duplicated popliteal and superficial femoral veins: incidence and potential significance. Aust N Z J Surg. 2000;70(6):438-440. 81. Lautz TB, Abbas F, Walsh SJ, et al. Isolated gastrocnemius and soleal vein thrombosis: should these patients receive therapeutic anticoagulation? Ann Surg. 2010;251(4):735-742. 82. Caggiati A, Bergan JJ, Gloviczki P, et al. Nomenclature of the veins of the lower limbs: an international interdisciplinary consensus statement. J Vasc Surg. 2002;36(2):416-422. 83. Lockhart ME, Sheldon HI, Robbin ML. Augmentation in lower extremity sonography for the detection of deep venous thrombosis. AJR Am J Roentgenol. 2005;184(2):419-422. 84. Intersocietal Accreditation Commission (IAC). IAC standards and guidelines for vascular testing accreditation. IAC. Available from: http:// www.intersocietal.org/vascular/standards/IACVascularTestingStandards2016 .pdf. 85. Needleman L. Update on the lower extremity venous ultrasonography examination. Radiol Clin North Am. 2014;52(6):1359-1374. 86. Cronan JJ. Venous thromboembolic disease: the role of US. Radiology. 1993;186(3):619-630. 87. Rubin JM, Xie H, Kim K, et al. Sonographic elasticity imaging of acute and chronic deep venous thrombosis in humans. J Ultrasound Med. 2006;25(9): 1179-1186. 88. Johnson SA, Stevens SM, Woller SC, et al. Risk of deep vein thrombosis following a single negative whole-leg compression ultrasound: a systematic review and meta-analysis. JAMA. 2010;303(5):438-445. 89. Guanella R, Righini M. Serial limited versus single complete compression ultrasonography for the diagnosis of lower extremity deep vein thrombosis. Semin Respir Crit Care Med. 2012;33(2):144-150. 90. Birdwell BG, Raskob GE, Whitsett TL, et al. The clinical validity of normal compression ultrasonography in outpatients suspected of having deep venous thrombosis. Ann Intern Med. 1998;128(1):1-7. 91. Bernardi E, Camporese G, Buller HR, et al. Serial 2-point ultrasonography plus D-dimer vs whole-leg color-coded Doppler ultrasonography for diagnosing suspected symptomatic deep vein thrombosis: a randomized controlled trial. JAMA. 2008;300(14):1653-1659.

92. Society for Vascular Medicine. Five things physicians and patients should question. Choosing Wisely. 2014:1-2. Available from: http://www .choosingwisely.org/doctor-patient-lists/society-for-vascularmedicine/. 93. van Haarst EP, Liasis N, van Ramshorst B, Moll FL. The development of valvular incompetence after deep vein thrombosis: a 7 year follow-up study with duplex scanning. Eur J Vasc Endovasc Surg. 1996;12(3):295-299. 94. Thorisson HM, Pollak JS, Scoutt L. The role of ultrasound in the diagnosis and treatment of chronic venous insufficiency. Ultrasound Q. 2007;23(2): 137-150. 95. Human P, Franz T, Scherman J, et al. Dimensional analysis of human saphenous vein grafts: implications for external mesh support. J Thorac Cardiovasc Surg. 2009;137(5):1101-1108. 96. Chin EE, Zimmerman PT, Grant EG. Sonographic evaluation of upper extremity deep venous thrombosis. J Ultrasound Med. 2005;24(6): 829-838. 97. Gooding GA, Hightower DR, Moore EH, et al. Obstruction of the superior vena cava or subclavian veins: sonographic diagnosis. Radiology. 1986;159(3): 663-665. 98. Baarslag HJ, van Beek EJ, Koopman MM, Reekers JA. Prospective study of color duplex ultrasonography compared with contrast venography in patients suspected of having deep venous thrombosis of the upper extremities. Ann Intern Med. 2002;136(12):865-872. 99. Knudson GJ, Wiedmeyer DA, Erickson SJ, et al. Color Doppler sonographic imaging in the assessment of upper-extremity deep venous thrombosis. AJR Am J Roentgenol. 1990;154(2):399-403. 100. Baxter GM, Kincaid W, Jeffrey RF, et al. Comparison of colour Doppler ultrasound with venography in the diagnosis of axillary and subclavian vein thrombosis. Br J Radiol. 1991;64(765):777-781. 101. Bernardi E, Piccioli A, Marchiori A, et al. Upper extremity deep vein thrombosis: risk factors, diagnosis, and management. Semin Vasc Med. 2001;1(1):105-110. 102. Fraser JD, Anderson DR. Venous protocols, techniques, and interpretations of the upper and lower extremities. Radiol Clin North Am. 2004;42(2): 279-296. 103. Patel MC, Berman LH, Moss HA, McPherson SJ. Subclavian and internal jugular veins at Doppler US: abnormal cardiac pulsatility and respiratory phasicity as a predictor of complete central occlusion. Radiology. 1999;211(2): 579-583. 104. Bonnet F, Loriferne JF, Texier JP, et al. Evaluation of Doppler examination for diagnosis of catheter-related deep vein thrombosis. Intensive Care Med. 1989;15(4):238-240. 105. McDonough JJ, Altemeier WA. Subclavian venous thrombosis secondary to indwelling cathers. Surg Gynecol Obstet. 1971;133(3):397-400. 106. Luciani A, Clement O, Halimi P, et al. Catheter-related upper extremity deep venous thrombosis in cancer patients: a prospective study based on Doppler US. Radiology. 2001;220(3):655-660. 107. Trerotola SO, Kuhn-Fulton J, Johnson MS, et al. Tunneled infusion catheters: increased incidence of symptomatic venous thrombosis after subclavian versus internal jugular venous access. Radiology. 2000;217(1): 89-93. 108. Monreal M, Lafoz E, Ruiz J, et al. Upper-extremity deep venous thrombosis and pulmonary embolism. A prospective study. Chest. 1991;99(2):280283. 109. Becker DM, Philbrick JT, Walker FB. Axillary and subclavian venous thrombosis. Prognosis and treatment. Arch Intern Med. 1991;151(10): 1934-1943. 110. Kearon C. Natural history of venous thromboembolism. Circulation. 2003;107(23 Suppl. 1):I22-I30. 111. Horattas MC, Wright DJ, Fenton AH, et al. Changing concepts of deep venous thrombosis of the upper extremity—report of a series and review of the literature. Surgery. 1988;104(3):561-567. 112. Mustafa S, Stein PD, Patel KC, et al. Upper extremity deep venous thrombosis. Chest. 2003;123(6):1953-1956. 113. Kooij JD, van der Zant FM, van Beek EJ, Reekers JA. Pulmonary embolism in deep venous thrombosis of the upper extremity: more often in catheterrelated thrombosis. Neth J Med. 1997;50(6):238-242. 114. Meissner MH, Moneta G, Burnand K, et al. The hemodynamics and diagnosis of venous disease. J Vasc Surg. 2007;46(Suppl.S):4S-24S.

CHAPTER 27  Peripheral Vessels 115. Recek C. Calf pump activity influencing venous hemodynamics in the lower extremity. Int J Angiol. 2013;22(1):23-30. 116. Weber TM, Lockhart ME, Robbin ML. Upper extremity venous Doppler ultrasound. Radiol Clin North Am. 2007;45(3):513-524, viii-ix. 117. Kremkau FW, Taylor KJ. Artifacts in ultrasound imaging. J Ultrasound Med. 1986;5(4):227-237. 118. Reading CC, Charboneau JW, Allison JW, Cooperberg PL. Color and spectral Doppler mirror-image artifact of the subclavian artery. Radiology. 1990;174(1):41-42. 119. Pozniak MA, Zagzebski JA, Scanlan KA. Spectral and color Doppler artifacts. Radiographics. 1992;12(1):35-44. 120. U.S. Renal Data System (USRDS). 2015 USRDS annual data report: epidemiology of kidney disease in the United States. Bethesda, MD: National Institutes of Health; 2015. 121. Feldman HI, Kobrin S, Wasserstein A. Hemodialysis vascular access morbidity. J Am Soc Nephrol. 1996;7(4):523-535. 122. Vascular Access Work Group. Clinical practice guidelines for vascular access, pt 1. Am J Kidney Dis. 2006;48(Suppl. 1):S176-S247. 123. Hodges TC, Fillinger MF, Zwolak RM, et al. Longitudinal comparison of dialysis access methods: risk factors for failure. J Vasc Surg. 1997;26(6): 1009-1019. 124. Allon M, Robbin ML. Increasing arteriovenous fistulas in hemodialysis patients: problems and solutions. Kidney Int. 2002;62(4):1109-1124. 125. Allon M, Lockhart ME, Lilly RZ, et al. Effect of preoperative sonographic mapping on vascular access outcomes in hemodialysis patients. Kidney Int. 2001;60(5):2013-2020. 126. Robbin ML, Gallichio MH, Deierhoi MH, et al. US vascular mapping before hemodialysis access placement. Radiology. 2000;217(1):83-88. 127. Gibson KD, Caps MT, Kohler TR, et al. Assessment of a policy to reduce placement of prosthetic hemodialysis access. Kidney Int. 2001;59(6): 2335-2345. 128. Little MD, Allon M, McNamara MM, et al. Risk evaluation of immediate surgical failure during thigh hemodialysis graft placement by sonographic screening. J Ultrasound Med. 2015;34(9):1613-1619. 129. Robbin ML, Chamberlain NE, Lockhart ME, et al. Hemodialysis arteriovenous fistula maturity: US evaluation. Radiology. 2002;225(1):59-64. 130. Robbin ML, Greene T, Cheung AK, et al. Arteriovenous fistula development in the first 6 weeks after creation. Radiology. 2015;150385. 131. Singh P, Robbin ML, Lockhart ME, Allon M. Clinically immature arteriovenous hemodialysis fistulas: effect of US on salvage. Radiology. 2008; 246(1):299-305. 132. Allon M, Bailey R, Ballard R, et al. A multidisciplinary approach to hemodialysis access: prospective evaluation. Kidney Int. 1998;53(2): 473-479. 133. Robbin ML, Oser RF, Lee JY, et al. Randomized comparison of ultrasound surveillance and clinical monitoring on arteriovenous graft outcomes. Kidney Int. 2006;69(4):730-735. 134. Lumsden AB, MacDonald MJ, Kikeri D, et al. Prophylactic balloon angioplasty fails to prolong the patency of expanded polytetrafluoroethylene arteriovenous grafts: results of a prospective randomized study. J Vasc Surg. 1997;26(3): 382-390. 135. Ram SJ, Work J, Caldito GC, et al. A randomized controlled trial of blood flow and stenosis surveillance of hemodialysis grafts. Kidney Int. 2003;64(1):272-280. 136. Malik J, Slavikova M, Svobodova J, Tuka V. Regular ultrasonographic screening significantly prolongs patency of PTFE grafts. Kidney Int. 2005;67(4): 1554-1558. 137. Dember LM, Holmberg EF, Kaufman JS. Randomized controlled trial of prophylactic repair of hemodialysis arteriovenous graft stenosis. Kidney Int. 2004;66(1):390-398.

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138. Tonelli M, James M, Wiebe N, et al. Ultrasound monitoring to detect access stenosis in hemodialysis patients: a systematic review. Am J Kidney Dis. 2008;51(4):630-640. 139. Allon M, Robbin ML. Hemodialysis vascular access monitoring: current concepts. Hemodial Int. 2009;13(2):153-162. 140. Jennings WC, Sideman MJ, Taubman KE, Broughan TA. Brachial vein transposition arteriovenous fistulas for hemodialysis access. J Vasc Surg. 2009;50(5):1121-1126. 141. Robbin ML, Oser RF, Allon M, et al. Hemodialysis access graft stenosis: US detection. Radiology. 1998;208(3):655-661. 142. Lockhart ME, Robbin ML. Hemodialysis access ultrasound. Ultrasound Q. 2001;17(3):157-167. 143. Umphrey HR, Abts CA, Robbin ML. Dialysis grafts and fistulae: planning and assessment. Ultrasound Clin. 2011;6(4):477-490. 144. Lockhart ME, Robbin ML, Fineberg NS, et al. Cephalic vein measurement before forearm fistula creation: does use of a tourniquet to meet the venous diameter threshold increase the number of usable fistulas? J Ultrasound Med. 2006;25(12):1541-1545. 145. Glass CJM, DiGragio W, Illig KA. A meta-analysis of preoperative duplex ultrasound vessel diameters for successful radiocephalic fistula placement. J Vasc Ultrasound. 2009;65-68(4). 146. Sidawy AN, Spergel LM, Besarab A, et al. The Society for Vascular Surgery: clinical practice guidelines for the surgical placement and maintenance of arteriovenous hemodialysis access. J Vasc Surg. 2008;48(5 Suppl.):2S-25S. 147. Miller CD, Robbin ML, Barker J, Allon M. Comparison of arteriovenous grafts in the thigh and upper extremities in hemodialysis patients. J Am Soc Nephrol. 2003;14(11):2942-2947. 148. Ong S, Barker-Finkel J, Allon M. Long-term outcomes of arteriovenous thigh grafts in hemodialysis patients: a comparison with tunneled dialysis catheters. Clin J Am Soc Nephrol. 2013;8(5):804-809. 149. Scott JD, Cull DL, Kalbaugh CA, et al. The mid-thigh loop arteriovenous graft: patient selection, technique, and results. Am Surg. 2006; 72(9):825-828. 150. National Kidney Foundation. KDOQI clinical practice guidelines and clinical practice recommendations for vascular access 2006. Am J Kidney Dis. 2006;48(Suppl. 1):S176-S322. 151. Falk A. Maintenance and salvage of arteriovenous fistulas. J Vasc Interv Radiol. 2006;17(5):807-813. 152. Clark TW, Hirsch DA, Jindal KJ, et al. Outcome and prognostic factors of restenosis after percutaneous treatment of native hemodialysis fistulas. J Vasc Interv Radiol. 2002;13(1):51-59. 153. Beathard GA, Arnold P, Jackson J, et al. Aggressive treatment of early fistula failure. Kidney Int. 2003;64(4):1487-1494. 154. May RE, Himmelfarb J, Yenicesu M, et al. Predictive measures of vascular access thrombosis: a prospective study. Kidney Int. 1997;52(6): 1656-1662. 155. Shackleton CR, Taylor DC, Buckley AR, et al. Predicting failure in polytetrafluoroethylene vascular access grafts for hemodialysis: a pilot study. Can J Surg. 1987;30(6):442-444. 156. Leake AE, Winger DG, Leers SA, et al. Management and outcomes of dialysis access-associated steal syndrome. J Vasc Surg. 2015;61(3):754-760. 157. Valji K, Hye RJ, Roberts AC, et al. Hand ischemia in patients with hemodialysis access grafts: angiographic diagnosis and treatment. Radiology. 1995;196(3):697-701. 158. Robbin ML, Lockhart ME. Ultrasound evaluation before and after hemodialysis access. In: Zweibel WJ, Pellerito JS, editors. Introduction to vascular ultrasonography. 5th ed. Philadelphia: Elsevier; 2005. p. 325-340.

PART FOUR: Obstetric and Fetal Sonography CHAPTER

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Overview of Obstetric Imaging Deborah Levine

SUMMARY OF KEY POINTS • Ultrasound allows for accurate prediction of gestational age. • The appropriate training and skills are necessary for safely performing and accurately interpreting obstetric ultrasound • There are many options for screening pregnant women, most of which include ultrasound.

• Routine obstetric ultrasound has specific recommended views that allow for depiction of many, but not all, fetal anomalies. • Three-dimensional ultrasound, fetal Doppler examinations, and fetal magnetic resonance imaging may be used when additional information is needed beyond that available with routine gray-scale ultrasound.

CHAPTER OUTLINE TRAINING, PERSONNEL, AND EQUIPMENT ULTRASOUND GUIDELINES First Trimester Second and Third Trimesters ROUTINE ULTRASOUND SCREENING

T

Estimation of Gestational Age Identification of Twin/Multiple Pregnancies Screening and Perinatal Outcomes Fetal Malformations: Diagnostic Accuracy

here were more than 3.9 million live births in the United States in 2013.1 Ultrasound is the most frequently used imaging modality for assessment of pregnancy. With care being taken to keep exposure to ultrasound limited to medically needed information, and with imaging performed at the appropriate power settings, ultrasound is safe for use in pregnancy. Indications for ultrasound during the first trimester include pregnancy dating, assessment of women with bleeding or pain, and assessment of nuchal translucency in screening for aneuploidy. In the second trimester, ultrasound is used for pregnancy dating, assessment of interval growth, assessment of patients with abnormal pain or bleeding, assessment of size-to-dates discrepancy, routine survey of fetal anatomy, and assessment of maternal complications due to conditions such as age, drug use, or history of previous abnormalities. In cases of multiple gestations, ultrasound is used to assess growth and complications of twinning. In women with history of cervical incompetence, ultrasound is used to screen for cervical changes that put a patient at risk for preterm delivery. In the third trimester, ultrasound is predominantly used to assess fetal growth and well-being. Ultrasound is increasingly used for fetal procedures such as testing for aneuploidy, drainage of abnormal fetal fluid collections, and guidance for fetal surgery. Ultrasound is well recognized as the screening modality of choice, but

Three-Dimensional Ultrasound Prudent Use of Ultrasound MAGNETIC RESONANCE IMAGING CONCLUSION

additional information may be needed beyond that available with ultrasound. In many of these cases, especially those with fetal central nervous system abnormalities, fetal magnetic resonance imaging (MRI) can help clarify the diagnosis. Part IV of this textbook focuses on obstetric ultrasound and reviews specific fetal organ system anatomy and pathology, with chapters also on safety of ultrasound in pregnancy, assessment of twins, and growth. Fetal magnetic resonance (MR) and threedimensional (3D) ultrasound images are added throughout to illustrate the benefit of these techniques in select cases.

TRAINING, PERSONNEL, AND EQUIPMENT Obstetric ultrasound diagnosis is critically dependent on examiner training and experience.2,3 Physicians and sonographers performing obstetric ultrasound examinations should have completed appropriate training and should be appropriately credentialed and/or boarded. Accreditation of ultrasound laboratories improves compliance with published minimum standards and guidelines.4 Ultrasound practitioners should be knowledgeable regarding the basic physical principles of ultrasound, equipment, record-keeping requirements, indications, and safety of using ultrasound in pregnancy. Studies should be conducted with real-time scanners

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Indications for First-Trimester Ultrasound Confirmation of the presence of an intrauterine pregnancy Suspected ectopic pregnancy Vaginal bleeding Pelvic pain Estimation of gestational age Diagnosis or evaluation of multiple gestations Confirmation of cardiac activity Adjunct to chorionic villus sampling, embryo transfer, and localization, and removal of an intrauterine device Assessment for certain fetal anomalies, such as anencephaly, in high-risk patients Measurement of nuchal translucency when part of a screening program for fetal aneuploidy Suspected ectopic pregnancy Suspected hydatidiform mole Maternal pelvic masses and/or uterine abnormalities Modified from Collaborative Subcommittee. ACR–ACOG–AIUM–SRU practice parameter for the performance of obstetrical ultrasound. American College of Radiology; 2014.5

using a transabdominal and/or transvaginal approach, depending on the gestational age and the region of interest. The choice of transducer frequency is a trade-off between beam penetration and resolution. In general, a 3- to 5-MHz transducer frequency provides sufficient resolution with adequate depth penetration in all but the extremely obese patient. During early pregnancy, a 4- to 7-MHz abdominal transducer or a 5- to 10-MHz vaginal transducer can provide superior resolution while still allowing adequate penetration. Higher-frequency transducers are most useful in achieving high-resolution scans of anatomy close to the probe, and lower-frequency transducers are useful when increased penetration of the sound beam is necessary and when a wider field of view is needed. Use of Doppler ultrasound and 3D imaging depends on the specific indication. As in all imaging studies, complete documentation of the images and a formal written interpretation are essential for quality assurance, accreditation, and medicolegal issues.

ULTRASOUND GUIDELINES First Trimester The current guidelines of the American College of Radiology (ACR) and American Institute of Ultrasound in Medicine (AIUM) for the performance of first-trimester obstetric ultrasound examination include documentation of the location of the pregnancy (intrauterine vs. extrauterine), documentation of the appearance of the maternal uterus and ovaries (Fig. 28.1), and assessment of gestational age, either by measurement of mean sac diameter (before visualization of embryonic pole; Fig. 28.2) or by embryonic/fetal pole crown-rump length5 (Fig. 28.3). Another important structure to assess is the yolk sac. An image of the heart rate is taken using M-mode ultrasound. It is important to use M-mode rather than spectral Doppler ultrasound on the embryo to limit power deposition. Late in the first trimester,

Indications for Second- and Third-Trimester Ultrasound Estimation of gestational (menstrual) age Evaluation of fetal growth Evaluation of fetal anatomy and fetal well-being Vaginal bleeding Abdominal or pelvic pain Cervical insufficiency Determination of fetal presentation Suspected multiple gestation Adjunct to amniocentesis or other procedure Evaluation of discrepancy between uterine size (as measured by fundal height) and clinical dates Pelvic mass Suspected hydatidiform mole Adjunct to cervical cerclage placement Suspected ectopic pregnancy Suspected fetal death Suspected uterine abnormality Suspected amniotic fluid abnormalities Suspected placental abruption Adjunct to external cephalic version Premature rupture of membranes and/or premature labor Previous abnormal screening exams Follow-up evaluation of placental location for suspected placenta previa or accreta Previous congenital anomaly Screening for or follow-up of fetal anomalies Modified from Collaborative Subcommittee. ACR–ACOG–AIUM–SRU practice parameter for the performance of obstetrical ultrasound. American College of Radiology; 2014.5

dating can be performed with measurement of the biparietal diameter and head circumference rather than crown-rump length. Videos 28.1 and 28.2 show normal first-trimester findings of an early embryo with cardiac activity (Video 28.1) and normal findings of rhombencephalon (Video 28.2). In the first trimester it is important to not only establish the location of the pregnancy (intrauterine versus extrauteruine) but when intrauterine, to carefully determine if it is a potentially viable pregnancy or if it is a nonviable pregnancy.6-9 Due to the

General Survey Guidelines for First-Trimester Ultrasound Gestational sac Location of pregnancy: intrauterine vs. extrauterine Gestational age (as appropriate) Mean sac diameter Embryonic pole length or crown rump length Yolk sac Cardiac activity on M-mode ultrasound Embryo/fetal number (amnionicity/chorionicity) Maternal anatomy: uterus and adnexa Modified from Collaborative Subcommittee. ACR–ACOG–AIUM–SRU practice parameter for the performance of obstetrical ultrasound. American College of Radiology; 2014.5

CHAPTER 28  Overview of Obstetric Imaging

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FIG. 28.1  Normal First-Trimester Ultrasound Images: Pregnancy Location and Adnexa.  (A) Transabdominal sagittal sonogram shows an intrauterine gestational sac. (B) Transverse image to the left of uterus shows normal appearance for the ovary (arrow). (C) Transvaginal color Doppler image shows normal hypervascular rim around corpus luteum.

FIG. 28.2  Normal First-Trimester Measurement of Sac Diameter.  Transvaginal sagittal image shows sagittal measurement of sac diameter (calipers). Measurements in three orthogonal planes are averaged to calculate the mean sac diameter. Note yolk sac within the gestational sac.

variety of medical professionals performing and interpreting ultrasound in a variety of clinical settings, thresholds for the diagnosis of a failed pregnancy have been increased in order to not misdiagnose a potentially viable pregnancy. These issues are discussed in detail in Chapter 30. In cases of multiple gestation, first-trimester scans should document the fetal number as well as the amnionicity and chorionicity (Fig. 28.4). Chapter 32 discusses the assessment of multifetal pregnancies. In addition, the American College of Obstetricians and Gynecologists (ACOG) recommends that prenatal testing for aneuploidy be offered to all pregnant women.10 Clinicians must understand current screening options (and the tradeoffs between them), including traditional serum analysis (with or without nuchal translucency ultrasonography) or cell-free DNA so that they can discuss these options appropriately with the patient. Cell-free DNA testing uses DNA from the placenta to assess the risk of the fetus having a chromosomal abnormality; it does not assess risk for fetal anomalies such as neural tube defects or ventral wall defects. Management decisions, including termination of the pregnancy, should not be based on the results of the cell-free

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D

G

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FIG. 28.3  First-Trimester Ultrasound Images: Embryo and Fetus.  (A) Normal embryo at 6.5 weeks’ gestation. Note embryonic pole (calipers) adjacent to yolk sac. (B) Normal embryo at 8 weeks’ gestation. Note embryo (calipers) and adjacent yolk sac (arrow). (C) M-mode ultrasound from same embryo as in B. Note normal heart rate of 160 beats/min. (D) Normal embryo at 9 weeks’ gestational age. Note embryo within amnion (arrow) and umbilical cord (arrowhead). (E) Just lateral to image in D, note yolk sac (arrowhead) is located outside the amnion (arrow). (F) Sagittal ultrasound at 10.5 weeks’ gestation. (G) Sagittal ultrasound at 11.5 weeks’ gestation. (H) Coronal view of face at 13 weeks’ gestation. (I) Sagittal ultrasound of nuchal translucency (calipers) at 13 weeks’ gestation. See also Videos 28.1 and 28.2.

DNA screening alone.10 Patients should be counseled that a negative cell-free DNA test result does not ensure an unaffected pregnancy. According to a 2015 ACOG committee opinion, “Given the performance of conventional screening methods, the limitations of cell-free DNA screening performance, and the limited data on cost-effectiveness in the low-risk obstetric population, conventional screening methods remain the most appropriate choice for first-line screening for most women in the general obstetric population.”10 Thus despite increased use of cell-free DNA testing, ultrasound screening is still being performed by measuring nuchal translucency between 11 and 14 weeks of gestation (see Fig. 28.3I). This measurement, in conjunction with maternal age

and serology, can be used to determine an individualized risk of fetal aneuploidy (see Chapter 31). Increased use of maternal serum screening, as well as first- and second-trimester ultrasound have reduced the number of interventional procedures to detect aneuploidy while increasing the number of prenatal diagnoses of aneuploidy.11 Given the increased scanning late in the first trimester, it is also increasingly common for a limited anatomic survey to be conducted in the late first trimester. Anomalies that should be detected this early include anencephaly (Fig. 28.5) and omphalocele (Fig. 28.6). Although substantial information can be obtained at this time, the firsttrimester anatomic survey is unlikely to replace the secondtrimester anatomic survey, since many structures are difficult

CHAPTER 28  Overview of Obstetric Imaging

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FIG. 28.4  Multiple Gestations.  The entire gestational sac should be examined to identify multiple gestations. (A) Transabdominal image of diamniotic dichorionic twins. Note the thick, dividing membrane that separates twin A (A), the presenting twin, from twin B (B). (B) Transvaginal image of diamniotic monochorionic twins at 8 weeks’ gestational age (calipers denote crown rump length [CRL]) with two thin membranes (arrows, amnion) still close to embryonic poles.

A

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FIG. 28.5  Anencephaly.  (A) Sagittal ultrasound at 10 weeks’ gestation. (B) Sagittal ultrasound in a different fetus at 12 weeks’ gestation. Note the orbits (arrow) with absent ossified cranium above this level with angiomatous stroma. The calipers mark the estimate of the crown rump length, made difficult due to angiomatous stroma above the orbits.

to visualize completely early in the second trimester, particularly the heart, cardiac outflow tracts, posterior fossa, and distal spine.

Second and Third Trimesters The current ACR/AIUM guidelines for the performance of the second- and third-trimester obstetric ultrasound examinations

describe the standard sonographic examination.5 It is important to understand that the guidelines were written to maximize detection of many fetal abnormalities but are not expected to allow for detection of all structural abnormalities. The terminology level I and level II examinations refer to “standard” or “routine” (level I) and “high risk,” “specialized,” or “detailed” (level II) obstetric ultrasound. The concept of these

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FIG. 28.6  Omphalocele at 11 Weeks’ Gestational Age.  Sagittal view of fetus (calipers) shows a large, abdominal wall defect (arrow).

two levels of scanning is that the standard, basic, routine, or level I examination is performed routinely on pregnant patients (Figs. 28.7 to 28.15, Videos 28.3) to 28.9. The methods to obtain all the required images are described in detail in subsequent chapters. This chapter provides a collage of figures as a guide for the anatomic survey and common additional views obtained during a fetal survey. In general, the “standard fetal anatomic survey” refers to the second-trimester scan, typically performed between 16

and 22 weeks of gestation. When anatomic surveys are performed at 20 to 22 weeks’ gestational age, there is less need for repeat scans to document normal anatomy compared to studies performed earlier in pregnancy.12 However, there are practical considerations when determining the optimal timing of studies. In well-dated pregnancies in women who are unlikely to want amniocentesis, a survey at 20 to 22 weeks’ gestation is optimal. However, if a pregnancy is not well-dated, an earlier scan may be needed both to establish accurate dates for the pregnancy and to assess the anatomy. Some centers offer the scan at 16 weeks’ gestation to coincide with performance of genetic amniocentesis and/or midtrimester quadruple serum screening. The level I examination consists of investigation of the maternal uterus and ovaries, the cervix, and placenta (Fig. 28.7, Video 28.3), as well as a systematic review of fetal anatomy. Adnexal cysts are common in pregnant women. In early pregnancy a cyst is most likely the corpus luteum. If a cyst appears atypical or enlarges beyond the middle second trimester, it should be further assessed. Leiomyoma position and size should be documented. If the myometrium appears thin in the lower uterine segment (e.g., 1000) populations. Often, however, these studies describe no anomalies in the study group or in the control population; in a survey of more than 121,000 patients among 68 examiners, combining 292 institute-years of experience, 3000 to 5000 anomalies would be expected as background rate, but none were reported.121 In fact, rigorous epidemiologic studies of the adverse bioeffects of ultrasound are scarce. Several biologic end points have been analyzed in the human fetus or neonate to determine whether prenatal exposure to diagnostic ultrasound had observable effects: intrauterine growth restriction and low birth weight,122 delayed speech,123 vision and hearing,124 dyslexia,125 neurologic and mental development or behavioral issues,126,127 malignancies,128 and nonright-handedness.129,130 Most findings have never been duplicated, and the majority of studies have been negative for any association, with the possible exception of low birth weight. There are no epidemiologic studies related to the output display standard (thermal and mechanical indices) and clinical

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outcomes. Only a few clinical studies describe routine scan,131 first-trimester scan,132 particularly, nuchal translucency screening,133 as well as Doppler132 and three-dimensional (3D)/fourdimensional (4D) ultrasound.134 Furthermore, although some studies address the issue of repeat scans,135,136 it was not as an analysis of potential cumulative effects for which no information is available.

Birth Weight In one often-quoted study of more than 2000 infants, a small (116 g at term) but statistically significant lower mean birth weight was found in the half exposed to ultrasound compared with the nonexposed group.137 However, information was collected several years after exposure, with no indications known and no exposure information available. Moreover, in a later study, the authors concluded that the relationship of ultrasound exposure to reduced birth weight may be caused by shared common risk factors, which lead to both exposure and a reduction in birth weight,138 an association but not a causal relationship. A twice-greater risk of low birth weight was reported in another retrospective study after four or more exposures to diagnostic ultrasound.14 These results were not reproduced in another retrospective study with a large population, originally of 10,000 pregnancies exposed to ultrasound matched with 500 controls and with 6-year follow-up.139 No increased congenital malformations, chromosomal abnormalities, infant neoplasms, speech or hearing impairment, or developmental problems were observed in this latter study. In a randomized controlled trial of more than 2800 pregnant women, about half received five ultrasound imaging and Doppler flow studies at 18, 24, 28, 34, and 38 weeks of gestation, and half received a single ultrasound imaging at 18 weeks.122 An increased risk of intrauterine growth restriction was detected in those exposed to frequent Doppler ultrasound examinations, possibly through effects on bone growth. However, when children were examined at 1 year of age, there were no differences between the study and control groups. In addition, after examining their original subjects after 8 years, the investigators found no evidence of adverse neurologic outcome.136 Similarly, other randomized studies found no harmful effect of one or two prenatal scans on growth.140,141 Curiously, in some studies, birth weight was slightly higher in the scanned group, but not significantly, except in one group of newborns exposed to ultrasound in utero who weighed on average 42 g (75 g in reported smokers) more than the control group.141 Thus ultrasound exposure in utero does not appear to be associated with reduced birth weight, although Doppler ultrasound exposure may have some risks.114 Delayed Speech To determine if an association exists between prenatal ultrasound exposure and delayed speech in children, Campbell et al.123 studied 72 children with delayed speech and found a higher rate of ultrasound exposure in utero compared with the 144 control subjects. However, this retrospective study used records more than 5 years old, with neither a dose-response effect nor any relationship to time of exposure. A much larger study of more than 1100 children exposed in utero and 1000 controls found

no significant differences in delayed speech, limited vocabulary, or stuttering.142

Dyslexia Dyslexia has been extensively studied. Stark et al.125 compared more than 4000 children (ages 7-12 years) exposed to ultrasound in utero to matched controls, analyzing outcome measures at birth (Apgar scores, gestational age, head circumference, birth weight, length, congenital abnormalities, neonatal/congenital infection) or in early infancy (hearing, visual acuity/color vision, cognitive function, behavior). No significant differences were found, except for a significantly greater proportion of dyslexia in children exposed to ultrasound. Given the design of the study and the presence of several possible confounding factors, the authors indicated that dyslexia could be incidental. Subsequently, long-term follow-up studies of more than 600 children with various tests for dyslexia (e.g., spelling, reading) were performed.143-147 End points included evaluation for dyslexia along with examination of nonright-handedness, said to be associated with dyslexia. No statistically significant differences were found between ultrasound-exposed children and controls for reading, spelling, arithmetic, or overall performance, as reported by teachers. Specific dyslexia tests showed similar incidence rates among scanned children and controls in reading, spelling, and intelligence scores and no discrepancy between intelligence and reading or spelling. Therefore the original finding of dyslexia was not confirmed in subsequent randomized controlled trials. It is considered unlikely that routine ultrasound screening can cause dyslexia. Nonright-Handedness A possible link between prenatal exposure to ultrasound and subsequent nonright-handedness at age 8 to 9 years in children exposed to ultrasound in utero was first reported in 1993 from Norway.146 According to the authors, however, the difference was “only barely significant at the 5% level” and was restricted to boys.148 A second group of researchers (including Salvesen, main author of the first study), studying a new population of more than 3000 children from Sweden, reported similar findings of a statistically significant association between ultrasound exposure in utero and nonright-handedness in males.129 An intriguing recent study showed that fetuses self-touched their faces more often with the left hand than the right, as observed by ultrasound, in correlation to stress levels of the mother.149 Furthermore, laterality is, mostly, genetically determined150 but could, naturally, be modified by external factors. Evidence is insufficient to infer a direct effect on brain structure or function, or even that nonright-handedness is an adverse effect. Neurologic Development and Behavioral Issues Neurons of the cerebral neocortex in mammals, including humans, are generated during fetal life in the brain proliferative zones and then migrate to their final destination by following an inside-to-outside sequence. This neuronal migration occurs in the human fetal brain mainly from 6 to 11 weeks of gestation151 but continues until 32 weeks. It has long been theorized that

CHAPTER 29  Bioeffects and Safety of Ultrasound in Obstetrics external factors such as ultrasound could affect this process.152 In another study, only 2 of 123 variables were found to be disturbed at birth, but not at 1 year of age, in children exposed in utero; these variables are grasp reflex and tonic neck reflex.153 The significance was not elaborated, and some doubts exist regarding statistical validity. Stark et al.125 reported that vision and intelligence scores were identical among 425 exposed infants and 381 controls. A large report found no association between routine exposure to prenatal ultrasound and school performance (deficits in attention, motor control, perception, vision, and hearing).154 In more than 4900 children age 15 to 16 years, no differences were found in school performance between exposed and nonexposed children, except for a lower score for exposed boys in physical education.155 Behavioral changes may be a more sensitive marker of subtle brain damage than obvious structural alterations.156 Such changes have been described in animals,84,105 although often transient.97 An interesting study in mice was recently published.157 As detailed earlier, there may be male preponderance of nonright-handedness after in utero ultrasound exposure. Furthermore, an increased prevalence of autism exists in males and there are reports of excess nonright-handedness in this population. Pregnant mice were exposed to 30 minutes of diagnostic ultrasound at embryonic day 14.5. Social behavior of their male pups was analyzed 3 weeks after birth. Ultrasound-exposed pups were significantly (P < .01) less interested in social interaction than sham-exposed pups and demonstrated significantly (P < .05) more activity relative to the sham-exposed pups (only in the presence of an unfamiliar mouse). These results suggest that social behavior in young mice was altered by in utero exposure to diagnostic ultrasound. The authors’ conclusions are that this may be relevant for autism but that major differences between the exposure of diagnostic ultrasound of mice and humans preclude conclusions regarding human exposure and require further studies. Indeed, no such changes have been reported in humans. In particular, schizophrenia and other psychoses have not been found to be associated with prenatal ultrasound exposure.158 The question has been raised about the increased rate of autism observed over the past few years and its relation to the greatly increased use of ultrasound in obstetrics. Although a major upsurge in both have occurred, there is no cause and effect demonstrable between the two.159

Congenital Malformations In humans, prenatal ultrasound has not been shown to result in an increased incidence of congenital anomalies, as found in animals. Childhood Malignancies No association has been found between ultrasound exposure in utero and the later development of leukemia160,161 or solid tumors in children.128,162-166 Again, although some of these studies were published in 2007 or 2008, the populations studied were exposed to ultrasound in utero 20 to 30 years ago, that is, with instruments generating lower outputs and with minimal or no information available on exposure conditions.

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IS DOPPLER DIFFERENT? Spectral (pulsed) Doppler uses high pulse repetition frequencies, generating greater temporal average intensities and powers than B- or M-mode, and hence greater heating potential (see “Thermal Effects”).75 Adequate diagnostic information may be obtained with low output levels (as documented by values of the TI), as demonstrated in Fig. 29.1. This has been reported in the literature, specifically for Doppler, the mode with the highest output, both in early and later pregnancy.167,168 In fact, under pressure from bioeffects and safety committees of various professional organizations (American Institute of Ultrasound in Medicine [AIUM], European Federation of Societies of Ultrasound in Medicine and Biology [EFSUMB], International Society for Ultrasound in Obstetrics and Gynecology [ISUOG], and World Federation for Ultrasound in Medicine and Biology [WFUMB]), several manufacturers have changed their default settings, specifically for pulsed Doppler in fetal mode, from very high (as it was originally, presumably in an attempt to obtain better images) to very low, with the end user capable of raising the output, if desired. Because acoustic output is high in Doppler, special precaution is recommended, particularly in early gestation.169

SAFETY GUIDELINES It is difficult to issue precise safety recommendations because of the multitude of ultrasound instruments, each with a selection of transducers and used in a variety of applications. Patient characteristics further complicate the task.170 Safety guidelines are very important, however, given the very low level of knowledge about bioeffects and safety of ultrasound among clinical end users. In a questionnaire distributed to ultrasound active end users (of which 82% were obstetricians), only 17.7% gave the correct answer of the definition of the TI. Approximately 96% did not know the proper definition for MI. Almost 80% of respondents did not know the correct answer to the multiple choice question of where to find the acoustic indices; answer options were the machine documentation, a textbook, a complicated calculation or in real time on the ultrasound monitor (the correct answer).171 Similar results were recorded in surveys abroad, performed in Europe, Asia, or the Middle East,172-174 indicating that clinical end users worldwide show poor knowledge regarding safety issues of ultrasound during pregnancy.30 More recently, knowledge among residents in obstetrics and gynecology was also found to be grossly lacking.175 Similar results were obtained in a survey of sonographers, and years of experience made no difference.176 In another study, compliance with the ALARA (as low as reasonably achievable) principle by practitioners seeking credentialing for nuchal translucency (NT) measurement between 11 and 14 weeks’ gestation was evaluated. Only 5% of the providers used the correct TI type (TIB) at lower than 0.5 for all submitted images, 6% at lower than 0.7, and 12% at 1.0 or lower. A TI (TIB or TIS) higher than 1.0 was used by almost 20% of the providers. Proficiency in NT measurement and educational background (physician or sonographer) did not influence compliance with ALARA. The authors concluded that clinicians seeking

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credentialing in NT do not demonstrate compliance with the recommended use of the TI in monitoring acoustic output.177 An easy way to reduce exposure is to reduce the TI and MI, using the appropriate controls, and/or reduce the dwell time. The 1999 statement of the British Medical Ultrasound Society, reconfirmed in 2009, declares178: For equipment for which the safety indices are displayed over their full range of values, the TI should always be less than 0.5 and the MI should always be less than 0.3. When the safety indices are not displayed, Tmax should be less than 1°C and MImax should be less than 0.3. Frequent exposure of the same subject is to be avoided. The British Medical Ultrasound Society has strict recommendations for maximum allowed exposure time (Tmax), depending on the TI (Table 29.1). Miller and Ziskin57 demonstrated a logarithmic relationship between exposure duration and temperature elevation in producing harmful bioeffects in animal fetuses. For temperatures below 43°C, the exposure time necessary for every 1°C increase in temperature was decreased by a factor of 4. Using a maximum “safe” exposure time of 4 minutes for a temperature elevation of 4°C, based on these calculations, the following maximal exposure times are allowable with no apparent obvious risks: 128 minutes at 1°C, 64 at 2°C, 16 at 3°C, and only 4 minutes at 4°C. Precautions are, naturally, of particular importance in early gestation179,180 and for Doppler exposure.181 General recommendations from major professional organizations follow. It is strongly recommended to consult various safety statements published on these organizations’ websites.182-192 1. A diagnostic ultrasound exposure that produces a maximum in situ temperature rise of no more than 1.5°C above normal physiologic levels (37°C) may be used clinically without reservation on thermal grounds.193 2. A diagnostic ultrasound exposure that elevates embryonic and fetal in situ temperature above 41°C (4°C above normal temperature) for 5 minutes or more should be considered potentially hazardous.193,194 In this regard, maternal temperature elevation (e.g., from viral disease) should be considered because body temperature of the fetus will also be increased above normal.48

TABLE 29.1  Duration of Obstetric Ultrasound as a Function of Thermal Index Thermal Index (TI) 0.7 1 1.5 2 2.5

Recommended Upper Limit 60 min 30 min 15 min 4 min 1 min

Modified from British Medical Ultrasound Society (BMUS) Safety Group. Guidelines for the safe use of diagnostic ultrasound equipment. Ultrasound. 2010;18:52-59.178

3. The risk of adverse effects is increased with the duration of exposure (dwell time).195 4. Based on available information, there is no reason to withhold scanning in B-mode for medical indications. The risk of thermal damage secondary to heating appears to be negligible.193 5. M-mode ultrasound appears to be safe and not to cause thermal damage (Fig. 29.5).48 6. Spectral Doppler ultrasound may produce high intensities, and routine Doppler examination during the embryonic period is rarely indicated.196 7. Three-dimensional (3D) and four-dimensional (4D) ultrasound are based on two-dimensional (2D) B-mode imaging with multiple 2D planes obtained and assembled (reconstructed) into a volume. Hence the exposure is really to B-mode and is, most likely, safe. Time of exposure has to be watched to avoid long episodes of scanning to obtain the “ideal” 3D volume (Fig. 29.6). 8. Education of ultrasound operators is crucial; the responsibility for the safe use of ultrasound devices is shared between the users and the manufacturers, who should ensure the accuracy of the output display.196 9. The AIUM advocates the responsible use of diagnostic ultrasound and strongly discourages the nonmedical use of ultrasound for “entertainment” purposes. The use of ultrasound without a medical indication to view the fetus, obtain a picture of the fetus, or determine the fetal gender is inappropriate and contrary to responsible medical practice. Ultrasound should be used by qualified health professionals to provide medical benefit to the patient.28 10. Examinations should be kept as short as possible and with as low MI and TI outputs as possible, but without sacrificing diagnostic accuracy. Follow the as low as reasonably achievable (ALARA) principle.197

CONCLUSION Diagnostic ultrasound has been used in medicine in general and obstetrics and gynecology in particular for more than half a century. No confirmed biologic effects have been described in patients as a result of exposure to diagnostic ultrasound. Such effects, however, have been described in animals, often at exposure levels higher than, but also occasionally equivalent to, those used in clinical practice. Epidemiologic information available is from studies performed on instruments with acoustic output much lower than current machines. Often, exposure data are insufficient and number of subjects too small. Furthermore, “no reported effects” does not mean “no effects,” and such biologic effects may be identified in the future. Prudent use of ultrasound in fetal scanning, following the ALARA principle, is therefore recommended. Based on known mechanisms, there is no contraindication to the use of B-mode, M-mode, 3D/4D, and color Doppler ultrasound, when clinically indicated. However, special precaution is necessary when applying pulsed Doppler ultrasound, particularly in the first trimester.

CHAPTER 29  Bioeffects and Safety of Ultrasound in Obstetrics

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FIG. 29.5  M-Mode Tracing, Obtained With Low TI (0.3) and MI (0.8).

FIG. 29.6  Multiplanar Images and Three-Dimensional Reconstructed Volume With Low TI (0.1) and MI (0.9).

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44. Dombrowski SC, Martin RP, Huttunen MO. Association between maternal fever and psychological/behavior outcomes: a hypothesis. Birth Defects Res A Clin Mol Teratol. 2003;67(11):905-910. 45. Edwards MJ, Saunders RD, Shiota K. Effects of heat on embryos and foetuses. Int J Hyperthermia. 2003;19(3):295-324. 46. Miller MW, Nyborg WL, Dewey WC, et al. Hyperthermic teratogenicity, thermal dose and diagnostic ultrasound during pregnancy: implications of new standards on tissue heating. Int J Hyperthermia. 2002;18(5): 361-384. 47. Moretti ME, Bar-Oz B, Fried S, Koren G. Maternal hyperthermia and the risk for neural tube defects in offspring: systematic review and meta-analysis. Epidemiology. 2005;16(2):216-219. 48. European Committee for Medical Ultrasound Safety (ECMUS). Thermal teratology. Eur J Ultrasound. 1999;9(3):281-283. 49. National Council on Radiation Protection and Measurements. Exposure criteria for medical diagnostic ultrasound. II. Criteria based on all known mechanisms. NCRP Report No. 140. Bethesda, Md: NCRP; 2002. 50. Acs N, Banhidy F, Puho E, Czeizel AE. Maternal influenza during pregnancy and risk of congenital abnormalities in offspring. Birth Defects Res A Clin Mol Teratol. 2005;73(12):989-996. 51. Cleves MA, Malik S, Yang S, et al. Maternal urinary tract infections and selected cardiovascular malformations. Birth Defects Res A Clin Mol Teratol. 2008;82(6):464-473. 52. Miller MW, Church CC, Miller RK, Edwards MJ. Fetal thermal dose considerations during the obstetrician’s watch: implications for the pediatrician’s observations. Birth Defects Res C Embryo Today. 2007;81(3): 135-143. 53. Peterka M, Tvrdek M, Likovsky Z, et al. Maternal hyperthermia and infection as one of possible causes of orofacial clefts. Acta Chir Plast. 1994;36(4): 114-118. 54. Superneau DW, Wertelecki W. Similarity of effects—experimental hyperthermia as a teratogen and maternal febrile illness associated with oromandibular and limb defects. Am J Med Genet. 1985;21(3):575-580. 55. Dreier JW, Andersen AM, Berg-Beckhoff G. Systematic review and metaanalyses: fever in pregnancy and health impacts in the offspring. Pediatrics. 2014;133(3):e674-e688. 56. Luteijn JM, Brown MJ, Dolk H. Influenza and congenital anomalies: a systematic review and meta-analysis. Hum Reprod. 2014;29(4):809-823. 57. Miller MW, Ziskin MC. Biological consequences of hyperthermia. Ultrasound Med Biol. 1989;15(8):707-722. 58. Miller MW, Miller HE, Church CC. A new perspective on hyperthermiainduced birth defects: the role of activation energy and its relation to obstetric ultrasound. J Therm Biol. 2005;30:400-409. 59. Brent RL. Is hyperthermia a direct or indirect teratogen? Teratology. 1986;33(3):373-374. 60. Barnett SB. Can diagnostic ultrasound heat tissue and cause biological effects? In: Barnett SB, Kossoff G, editors. Safety of diagnostic ultrasound. New York: Parthenon; 1998. p. 30. 61. Nyborg WL, Steele RB. Temperature elevation in a beam of ultrasound. Ultrasound Med Biol. 1983;9(6):611-620. 62. Nyborg WL, O’Brien Jr WD. An alternative simple formula for temperature estimates. J Ultrasound Med. 1989;8(11):653-654. 63. Martínez-Frías ML, García Mazario MJ, Caldas CF, et al. High maternal fever during gestation and severe congenital limb disruptions. Am J Med Genet. 2001;98(2):201-203. 64. Horder MM, Barnett SB, Vella GJ, et al. Ultrasound-induced temperature increase in guinea-pig fetal brain in utero: third-trimester gestation. Ultrasound Med Biol. 1998;24(9):1501-1510. 65. Jauniaux E, Gulbis B, Burton GJ. The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus—a review. Placenta. 2003;24(Suppl. A):S86-S93. 66. Carbillon L, Perrot N, Uzan M, Uzan S. Doppler ultrasonography and implantation: a critical review. Fetal Diagn Ther. 2001;16(6):327-332. 67. Kurjak A, Kupesic S. Doppler proof of the presence of intervillous circulation. Ultrasound Obstet Gynecol. 1996;7(6):463-464. 68. Jauniaux E. Intervillous circulation in the first trimester: the phantom of the color Doppler obstetric opera. Ultrasound Obstet Gynecol. 1996;8(2):73-76.

CHAPTER 29  Bioeffects and Safety of Ultrasound in Obstetrics 69. Makikallio K, Tekay A, Jouppila P. Uteroplacental hemodynamics during early human pregnancy: a longitudinal study. Gynecol Obstet Invest. 2004;58(1):49-54. 70. Wloch A, Rozmus-Warcholinska W, Czuba B, et al. Doppler study of the embryonic heart in normal pregnant women. J Matern Fetal Neonatal Med. 2007;20(7):533-539. 71. Russell NE, McAuliffe FM. First-trimester fetal cardiac function. J Ultrasound Med. 2008;27(3):379-383. 72. Duck FA. Is it safe to use diagnostic ultrasound during the first trimester? Ultrasound Obstet Gynecol. 1999;13(6):385-388. 73. Smythe GE, MacRae DJ. Letter: doppler ultrasound and fetal hazard. Lancet. 1975;2(7925):134. 74. Calvert J, Duck F, Clift S, Azaime H. Surface heating by transvaginal transducers. Ultrasound Obstet Gynecol. 2007;29(4):427-432. 75. Ziskin MC. Intrauterine effects of ultrasound: human epidemiology. Teratology. 1999;59(4):252-260. 76. O’Brien WD, Siddiqi TA. Obstetric sonography: the output display standard and ultrasound bioeffects. In: Fleischer AC, Manning FA, Jeanty P, Romero R, editors. Sonography in obstetrics and gynecology: principles and practice. 6th ed. New York: McGraw-Hill; 2001. p. 29-48. 77. Bly SH, Vlahovich S, Mabee PR, Hussey RG. Computed estimates of maximum temperature elevations in fetal tissues during transabdominal pulsed Doppler examinations. Ultrasound Med Biol. 1992;18(4):389397. 78. Carstensen EL, Gates AH. The effects of pulsed ultrasound on the fetus. J Ultrasound Med. 1984;3(4):145-147. 79. Dalecki D, Raeman CH, Child SZ, et al. Hemolysis in vivo from exposure to pulsed ultrasound. Ultrasound Med Biol. 1997;23(2):307-313. 80. Abramowicz JS. Ultrasonographic contrast media: has the time come in obstetrics and gynecology? J Ultrasound Med. 2005;24(4):517-531. 81. Miller MW, Brayman AA, Sherman TA, et al. Comparative sensitivity of human fetal and adult erythrocytes to hemolysis by pulsed 1 MHz ultrasound. Ultrasound Med Biol. 2001;27(3):419-425. 82. Fatemi M, Ogburn Jr PL, Greenleaf JF. Fetal stimulation by pulsed diagnostic ultrasound. J Ultrasound Med. 2001;20(8):883-889. 83. Duck FA. Acoustic streaming and radiation pressure in diagnostic applications: what are the implications? In: Barnett SB, Kossoff G, editors. Safety of diagnostic ultrasound. New York: Parthenon; 1998. p. 8798. 84. Jensh RP, Brent RL. Intrauterine effects of ultrasound: animal studies. Teratology. 1999;59(4):240-251. 85. Harvey EN, Loomis AL. High-frequency sound waves of small intensity and their biological effects. Nature. 1928;121:622-624. 86. Sikov MR. Effect of ultrasound on development. Part 1: introduction and studies in inframammalian species. Report of the Bioeffects Committee of the American Institute of Ultrasound in Medicine. J Ultrasound Med. 1986;5(10):577-583. 87. Sikov MR. Effect of ultrasound on development. Part 2: studies in mammalian species and overview. J Ultrasound Med. 1986;5(11):651-661. 88. Fry FJ, Kossoff G, Eggleton RC, Dunn F. Threshold ultrasonic dosages for structural changes in the mammalian brain. J Acoust Soc Am. 1970;48(6):Suppl 2:1413. 89. Frizzell LA, Carstensen EL, Davis JD. Ultrasonic absorption in liver tissue. J Acoust Soc Am. 1979;65(5):1309-1312. 90. Frizzell LA, Lee CS, Aschenbach PD, et al. Involvement of ultrasonically induced cavitation in the production of hind limb paralysis of the mouse neonate. J Acoust Soc Am. 1983;74(3):1062-1065. 91. Borrelli MJ, Frizzell LA, Dunn F. Ultrasonically induced morphological changes in the mammalian neonatal spinal cord. Ultrasound Med Biol. 1986;12(4):285-295. 92. Frizzell LA, Linke CA, Carstensen EL, Fridd CW. Thresholds for focal ultrasonic lesions in rabbit kidney, liver, and testicle. IEEE Trans Biomed Eng. 1977;24(4):393-396. 93. Carnes KI, Hess RA, Dunn F. The effect of ultrasound exposure in utero on the development of the fetal mouse testis: adult consequences. Ultrasound Med Biol. 1995;21(9):1247-1257. 94. Hynynen K. The threshold for thermally significant cavitation in dog’s thigh muscle in vivo. Ultrasound Med Biol. 1991;17(2):157-169.

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95. Dalecki D, Raeman CH, Child SZ, Carstensen EL. Intestinal hemorrhage from exposure to pulsed ultrasound. Ultrasound Med Biol. 1995;21(8): 1067-1072. 96. Dalecki D, Child SZ, Raeman CH, et al. Ultrasonically induced lung hemorrhage in young swine. Ultrasound Med Biol. 1997;23(5):777-781. 97. Tarantal AF, Hendrickx AG. Evaluation of the bioeffects of prenatal ultrasound exposure in the cynomolgus macaque (Macaca fascicularis): II. Growth and behavior during the first year. Teratology. 1989;39(2):149-162. 98. Hande MP, Devi PU. Effect of in utero exposure to diagnostic ultrasound on the postnatal survival and growth of mouse. Teratology. 1993; 48(5):405-411. 99. O’Brien WD. Dose-dependent effects of ultrasound on fetal weight in mice. J Ultrasound Med. 1983;2:1-8. 100. Vorhees CV, Acuff-Smith KD, Schilling MA, et al. Behavioral teratologic effects of prenatal exposure to continuous-wave ultrasound in unanesthetized rats. Teratology. 1994;50(3):238-249. 101. O’Brien Jr WD, Januzik SJ, Dunn F. Ultrasound biologic effects: a suggestion of strain specificity. J Ultrasound Med. 1982;1(9):367-370. 102. Hande MP, Devi PU. Effect of prenatal exposure to diagnostic ultrasound on the development of mice. Radiat Res. 1992;130(1):125-128. 103. Rao S, Ovchinnikov N, McRae A. Gestational stage sensitivity to ultrasound effect on postnatal growth and development of mice. Birth Defects Res A Clin Mol Teratol. 2006;76(8):602-608. 104. Borrelli MJ, Bailey KI, Dunn F. Early ultrasonic effects upon mammalian CNS structures (chemical synapses). J Acoust Soc Am. 1981;69(5):1514-1516. 105. Norton S, Kimler BF, Cytacki EP, Rosenthal SJ. Prenatal and postnatal consequences in the brain and behavior of rats exposed to ultrasound in utero. J Ultrasound Med. 1991;10(2):69-75. 106. Devi PU, Suresh R, Hande MP. Effect of fetal exposure to ultrasound on the behavior of the adult mouse. Radiat Res. 1995;141(3):314-317. 107. Hande MP, Devi PU, Karanth KS. Effect of prenatal ultrasound exposure on adult behavior in mice. Neurotoxicol Teratol. 1993;15(6):433-438. 108. Schneider-Kolsky ME, Ayobi Z, Lombardo P, et al. Ultrasound exposure of the foetal chick brain: effects on learning and memory. Int J Dev Neurosci. 2009;27(7):677-683. 109. Milunsky A, Ulcickas M, Rothman KJ, et al. Maternal heat exposure and neural tube defects. JAMA. 1992;268(7):882-885. 110. Ang Jr ES, Gluncic V, Duque A, et al. Prenatal exposure to ultrasound waves impacts neuronal migration in mice. Proc Natl Acad Sci USA. 2006;103(34):12903-12910. 111. Abramowicz JS. Prenatal exposure to ultrasound waves: is there a risk? Ultrasound Obstet Gynecol. 2007;29(4):363-367. 112. Kieler H. Epidemiological studies on adverse effects of prenatal ultrasound— which are the challenges? Prog Biophys Mol Biol. 2007;93(1-3):301-308. 113. Newman PG. Studies of ultrasound safety in humans: clinical benefit vs. risk. In: Barnett SB, Kossoff G, editors. Safety of diagnostic ultrasound. New York: Parthenon; 1998. 114. Salvesen KA. Epidemiological prenatal ultrasound studies. Prog Biophys Mol Biol. 2007;93(1-3):295-300. 115. Ziskin MC, Petitti DB. Epidemiology of human exposure to ultrasound: a critical review. Ultrasound Med Biol. 1988;14(2):91-96. 116. Edmonds PD, Abramowicz JS, Carson PL, et al. Guidelines for Journal of Ultrasound in Medicine authors and reviewers on measurement and reporting of acoustic output and exposure. J Ultrasound Med. 2005;24:1171-1179. 117. Carvalho JS. Fetal heart scanning in the first trimester. Prenat Diagn. 2004;24(13):1060-1067. 118. Makikallio K, Jouppila P, Rasanen J. Human fetal cardiac function during the first trimester of pregnancy. Heart. 2005;91(3):334-338. 119. Becker R, Wegner RD. Detailed screening for fetal anomalies and cardiac defects at the 11-13-week scan. Ultrasound Obstet Gynecol. 2006;27(6):613-618. 120. Vinals F, Ascenzo R, Naveas R, et al. Fetal echocardiography at 11 + 0 to 13 + 6 weeks using four-dimensional spatiotemporal image correlation telemedicine via an Internet link: a pilot study. Ultrasound Obstet Gynecol. 2008;31(6):633-638. 121. Ziskin MC. Survey of patients exposed to diagnostic ultrasound. In: Reid JM, Sikov MR, editors. Interactions of ultrasound and biological tissues.

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PART IV

Obstetric and Fetal Sonography

Proceedings of a workshop, Battelle Seattle Research Center, Seattle, 1971. Rockville, Md: Bureau of Radiological Health, U.S. Department of Health, Education and Welfare; 1973. pp. 203-206. 122. Newnham JP, Evans SF, Michael CA, et al. Effects of frequent ultrasound during pregnancy: a randomised controlled trial. Lancet. 1993;342(8876): 887-891. 123. Campbell JD, Elford RW, Brant RF. Case-control study of prenatal ultrasonography exposure in children with delayed speech. CMAJ. 1993;149(10): 1435-1440. 124. Kieler H, Haglund B, Waldenstrom U, Axelsson O. Routine ultrasound screening in pregnancy and the children’s subsequent growth, vision and hearing. Br J Obstet Gynaecol. 1997;104(11):1267-1272. 125. Stark CR, Orleans M, Haverkamp AD, Murphy J. Short- and long-term risks after exposure to diagnostic ultrasound in utero. Obstet Gynecol. 1984;63(2):194-200. 126. Bricker L, Neilson JP, Dowswell T. Routine ultrasound in late pregnancy (after 24 weeks’ gestation). Cochrane Database Syst Rev. 2008;(4): CD001451. 127. Kieler H, Haglund B, Cnattingius S, et al. Does prenatal sonography affect intellectual performance? Epidemiology. 2005;16(3):304-310. 128. Cartwright RA, McKinney PA, Hopton PA, et al. Ultrasound examinations in pregnancy and childhood cancer. Lancet. 1984;2(8410):999-1000. 129. Kieler H, Axelsson O, Haglund B, et al. Routine ultrasound screening in pregnancy and the children’s subsequent handedness. Early Hum Dev. 1998;50(2):233-245. 130. Salvesen KA. Ultrasound and left-handedness: a sinister association? Ultrasound Obstet Gynecol. 2002;19(3):217-221. 131. Sheiner E, Freeman J, Abramowicz JS. Acoustic output as measured by mechanical and thermal indices during routine obstetric ultrasound examinations. J Ultrasound Med. 2005;24(12):1665-1670. 132. Sheiner E, Shoham-Vardi I, Pombar X, et al. An increased thermal index can be achieved when performing Doppler studies in obstetric sonography. J Ultrasound Med. 2007;26(1):71-76. 133. Sheiner E, Abramowicz JS. Acoustic output as measured by thermal and mechanical indices during fetal nuchal translucency ultrasound examinations. Fetal Diagn Ther. 2009;25(1):8-10. 134. Sheiner E, Hackmon R, Shoham-Vardi I, et al. A comparison between acoustic output indices in 2D and 3D/4D ultrasound in obstetrics. Ultrasound Obstet Gynecol. 2007;29(3):326-328. 135. Bellieni CV, Buonocore G, Bagnoli F, et al. Is an excessive number of prenatal echographies a risk for fetal growth? Early Hum Dev. 2005;81(8): 689-693. 136. Newnham JP, Doherty DA, Kendall GE, et al. Effects of repeated prenatal ultrasound examinations on childhood outcome up to 8 years of age: follow-up of a randomised controlled trial. Lancet. 2004;364(9450): 2038-2044. 137. Moore Jr RM, Barrick MK, Hamilton TM. Effect of sonic radiation on growth and development. Am J Epidemiol. 1982;116:571. 138. Moore Jr RM, Diamond EL, Cavalieri RL. The relationship of birth weight and intrauterine diagnostic ultrasound exposure. Obstet Gynecol. 1988;71(4): 513-517. 139. Lyons EA, Dyke C, Toms M, Cheang M. In utero exposure to diagnostic ultrasound: a 6-year follow-up. Radiology. 1988;166(3):687-690. 140. Saari-Kemppainen A, Karjalainen O, Ylostalo P, Heinonen OP. Ultrasound screening and perinatal mortality: controlled trial of systematic one-stage screening in pregnancy. The Helsinki Ultrasound Trial. Lancet. 1990; 336(8712):387-391. 141. Waldenstrom U, Axelsson O, Nilsson S, et al. Effects of routine one-stage ultrasound screening in pregnancy: a randomised controlled trial. Lancet. 1988;2(8611):585-588. 142. Salvesen KA, Vatten LJ, Bakketeig LS, Eik-Nes SH. Routine ultrasonography in utero and speech development. Ultrasound Obstet Gynecol. 1994;4(2): 101-103. 143. Bakketeig LS, Eik-Nes SH, Jacobsen G, et al. Randomised controlled trial of ultrasonographic screening in pregnancy. Lancet. 1984;2(8396): 207-211. 144. Eik-Nes SH, Okland O, Aure JC, Ulstein M. Ultrasound screening in pregnancy: a randomised controlled trial. Lancet. 1984;1(8390):1347.

145. Salvesen KA, Bakketeig LS, Eik-nes SH, et al. Routine ultrasonography in utero and school performance at age 8-9 years. Lancet. 1992;339(8785): 85-89. 146. Salvesen KA, Vatten LJ, Eik-Nes SH, et al. Routine ultrasonography in utero and subsequent handedness and neurological development. BMJ. 1993;307(6897):159-164. 147. Salvesen KA, Vatten LJ, Jacobsen G, et al. Routine ultrasonography in utero and subsequent vision and hearing at primary school age. Ultrasound Obstet Gynecol. 1992;2(4):243-244, 245-247. 148. Salvesen KA, Eik-Ness SH, Vatten LJ, et al. Routine ultrasound scanning in pregnancy [authors’ reply]. BMJ. 1993;307:1562. 149. Reissland N, Aydin E, Francis B, Exley K. Laterality of foetal self-touch in relation to maternal stress. Laterality. 2015;20(1):82-94. 150. Hepper PG. The developmental origins of laterality: fetal handedness. Dev Psychobiol. 2013;55(6):588-595. 151. Sidman RL, Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973;62(1):1-35. 152. Mole R. Possible hazards of imaging and Doppler ultrasound in obstetrics. Birth. 1986;13:Suppl:23-33 suppl. 153. Scheidt PC, Stanley F, Bryla DA. One-year follow-up of infants exposed to ultrasound in utero. Am J Obstet Gynecol. 1978;131(7): 743-748. 154. Salvesen K. Routine ultrasonography in utero and development in childhood. In: Tejani N, editor. Obstetrical events and developmental sequelae. 2nd ed. Boca Raton, Fla: CRC Press; 1994. 155. Stalberg K. Prenatal ultrasound and x-ray-potentially adverse effects on the CNS. Upsalla, Sweden: Upsalla Universitet; 2008. 156. Coyle I, Wayner MJ, Singer G. Behavioral teratogenesis: a critical evaluation. Pharmacol Biochem Behav. 1976;4(2):191-200. 157. McClintic AM, King BH, Webb SJ, Mourad PD. Mice exposed to diagnostic ultrasound in utero are less social and more active in social situations relative to controls. Autism Res. 2014;7(3):295-304. 158. Stalberg K, Haglund B, Axelsson O, et al. Prenatal ultrasound scanning and the risk of schizophrenia and other psychoses. Epidemiology. 2007;18(5):577-582. 159. Abramowicz JS. Ultrasound and autism: association, link, or coincidence? J Ultrasound Med. 2012;31(8):1261-1269. 160. Shu XO, Potter JD, Linet MS, et al. Diagnostic X-rays and ultrasound exposure and risk of childhood acute lymphoblastic leukemia by immunophenotype. Cancer Epidemiol Biomarkers Prev. 2002;11(2):177-185. 161. Naumburg E, Bellocco R, Cnattingius S, et al. Prenatal ultrasound examinations and risk of childhood leukaemia: case-control study. BMJ. 2000;320(7230):282-283. 162. Kinnier Wilson LM, Waterhouse JA. Obstetric ultrasound and childhood malignancies. Lancet. 1984;2(8410):997-999. 163. Bunin GR, Buckley JD, Boesel CP, et al. Risk factors for astrocytic glioma and primitive neuroectodermal tumor of the brain in young children: a report from the Children’s Cancer Group. Cancer Epidemiol Biomarkers Prev. 1994;3(3):197-204. 164. Sorahan T, Lancashire R, Stewart A, Peck I. Pregnancy ultrasound and childhood cancer: a second report from the Oxford Survey of Childhood Cancers. Br J Obstet Gynaecol. 1995;102(10):831-832. 165. Salvesen KA, Eik-Nes SH. Ultrasound during pregnancy and birthweight, childhood malignancies and neurological development. Ultrasound Med Biol. 1999;25(7):1025-1031. 166. Stalberg K, Haglund B, Axelsson O, et al. Prenatal ultrasound and the risk of childhood brain tumour and its subtypes. Br J Cancer. 2008;98(7): 1285-1287. 167. Sande RK, Matre K, Eide GE, Kiserud T. Ultrasound safety in early pregnancy: reduced energy setting does not compromise obstetric Doppler measurements. Ultrasound Obstet Gynecol. 2012;39(4):438-443. 168. Sande RK, Matre K, Eide GE, Kiserud T. The effects of reducing the thermal index for bone from 1.0 to 0.5 and 0.1 on common obstetric pulsed wave Doppler measurements in the second half of pregnancy. Acta Obstet Gynecol Scand. 2013;92(7):790-796. 169. ter Haar GR, Abramowicz JS, Akiyama I, et al. Do we need to restrict the use of Doppler ultrasound in the first trimester of pregnancy? Ultrasound Med Biol. 2013;39(3):374-380.

CHAPTER 29  Bioeffects and Safety of Ultrasound in Obstetrics 170. Kossoff G, Griffiths KA, Garrett WJ, et al. Thickness of tissues intervening between the transducer and fetus and models for fetal exposure calculations in transvaginal sonography. Ultrasound Med Biol. 1993;19(1):59-65. 171. Sheiner E, Shoham-Vardi I, Abramowicz JS. What do clinical users know regarding safety of ultrasound during pregnancy? J Ultrasound Med. 2007;26(3):319-325. 172. Marsal K. The output display standard: has it missed its target? Ultrasound Obstet Gynecol. 2005;25(3):211-214. 173. Piscaglia F, Tewelde AG, Righini R, et al. Knowledge of the bio-effects of ultrasound among physicians performing clinical ultrasonography: results of a survey conducted by the Italian Society for Ultrasound in Medicine and Biology (SIUMB). J Ultrasound. 2009;12:6-11. 174. Akhtar W, Arain MA, Ali A, et al. Ultrasound biosafety during pregnancy: what do operators know in the developing world? National survey findings from Pakistan. J Ultrasound Med. 2011;30(7):981-985. 175. Houston LE, Allsworth J, Macones GA. Ultrasound is safe… right? Resident and maternal-fetal medicine fellow knowledge regarding obstetric ultrasound safety. J Ultrasound Med. 2011;30(1):21-27. 176. Bagley J, Thomas K, DiGiacinto D. Safety practices of sonographers and their knowledge of the biologic effects of sonography. J Diag Med Sonography. 2011;27:252-261. 177. Bromley B, Spitz J, Fuchs K, Thornburg LL. Do clinical practitioners seeking credentialing for nuchal translucency measurement demonstrate compliance with biosafety recommendations? Experience of the Nuchal Translucency Quality Review Program. J Ultrasound Med. 2014;33(7):1209-1214. 178. British Medical Ultrasound Society (BMUS) Safety Group. Guidelines for the safe use of diagnostic ultrasound equipment. Ultrasound. 2010;18: 52-59. 179. Lees C, Abramowicz JS, Brezinka C, et al. Ultrasound from conception to 10+0 weeks of gestation. London: Royal College of Obstetricians and Gynaecologists; 2015. Scientific Impact Paper No. 49. 180. Abramowicz JS. Ultrasound in the first trimester and earlier: how to keep it safe. In: Abramowicz JS, editor. First trimester ultrasound: a comprehensive guide. Cham. Switzerland: Springer; 2015. p. 1-19. 181. Abramowicz JS. Fetal Doppler: how to keep it safe? Clin Obstet Gynecol. 2010;53(4):842-850. 182. American Institute of Ultrasound in Medicine. AIUM official statement: Prudent use in pregnancy. 2012. Available from: http://www.aium.org/ officialStatements/33. Accessed 26 December 2015. 183. American Institute of Ultrasound in Medicine. AIUM official statement: Keepsake fetal imaging. 2012. Available from: http://www.aium.org/ officialStatements/31. Accessed 26 December 2015. 184. American Institute of Ultrasound in Medicine. AIUM official statement: As low as reasonably achievable (ALARA) principle. 2014. Available from: http://www.aium.org/officialStatements/39. Accessed 26 December 2015. 185. American Institute of Ultrasound in Medicine. AIUM Statement on mammalian biological effects of heat. 2015. Available from: http://www.aium.org/ officialStatements/17. Accessed 26 December 2015.

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186. British Medical Ultrasound Society. BMUS Statement on the safe use and potential hazards of diagnostic ultrasound. 2000, reconfirmed 2012. Available from: https://www.bmus.org/static/uploads/resources/statement_on_the_ safe_use_and_potential_hazards_of_diagnostic_ultrasound.pdf. Accessed 26 December 2015. 187. BMUS. Guidelines for the safe use of diagnostic ultrasound equipment. Ultrasound. 2010;18:52-59. 188. British Medical Ultrasound Society Safety Group. BMUS Statement for the general public on the safety of medical ultrasound imaging. 2012. Available from: https://www.bmus.org/static/uploads/resources/Statement_for_the_ General_Public_on_the_Safety_of_Medical_Ultrasound_Imaging.pdf. Accessed 26 December 2015. 189. European Committee for Medical Ultrasound Safety of the European Federation of Societies for Ultrasound in Medicine and Biology. ECMUS Statement on the use of diagnostic ultrasound for producing souvenir images or recordings in pregnancy. 2012. Available from: https://www.bmus.org/ static/uploads/resources/ECMUS_Souvenir_Scanning.pdf. Accessed 26 December 2015. 190. European Committee for Medical Ultrasound Safety of the European Federation of Societies for Ultrasound in Medicine and Biology. ECMUS Guidelines for the safe use of Doppler ultrasound for clinical application. 2013. Available from: http://www.efsumb-portal.org/ep/article.php?id=50. Accessed 26 December 2015. 191. International Society for Ultrasound in Obstetrics and Gynecology. ISUOG safety statements, 2000-2015. Available from: http://www.isuog.org/ StandardsAndGuidelines/Statements+and+Guidelines/Safety+Statements/. Accessed 26 December 2015. 192. World Federation of Ultrasound in Medicine and Biology. WFUMB/ISUOG Statement on the safe use of Doppler ultrasound during 11-14 week scans (or earlier in pregnancy). 2011, reaffirmed 2015. Available from: http://www.wfumb.org/safety-statements/. Accessed 26 December 2015. 193. World Federation for Ultrasound in Medicine and Biology. WFUMB Symposium on Safety and Standardisation in Medical Ultrasound. Issues and recommendations regarding thermal mechanisms for biological effects of ultrasound. Hornbaek, Denmark, 30 August-1 September 1991. Ultrasound Med Biol. 1992;18(9):731-810. 194. Barnett SB. WFUMB Symposium on Safety of Ultrasound in Medicine. Conclusions and recommendations on thermal and non-thermal mechanisms for biological effects of ultrasound. Kloster-Banz, Germany, 14-19 April 1996. World Federation for Ultrasound in Medicine and Biology. Ultrasound Med Biol. 1998;24(Suppl. 1):i-xvi, S1-S58. 195. Health Canada. Guidelines for the safe use of diagnostic ultrasound: Canada Minister of Public Works and Government Services; 2001. 196. Abramowicz JS, Kossoff G, Marsal K, Ter Haar G. Safety statement, 2000 (reconfirmed 2003). International Society of Ultrasound in Obstetrics and Gynecology (ISUOG). Ultrasound Obstet Gynecol. 2003;21(1):100. 197. Barnett SB, Ter Haar GR, Ziskin MC, et al. International recommendations and guidelines for the safe use of diagnostic ultrasound in medicine. Ultrasound Med Biol. 2000;26(3):355-366.

CHAPTER

30

 

The First Trimester Elizabeth Lazarus and Deborah Levine

SUMMARY OF KEY POINTS • First-trimester development follows a predictable pattern on first-trimester ultrasound. • Some ultrasound findings are definitive for early pregnancy failure, whereas others are suggestive and require follow-up.

• Ultrasound is vital in the diagnosis of ectopic pregnancy in typical and atypical locations. • Gestational trophoblastic disease is composed of four entities, and ultrasound is helpful in their diagnosis and management.

CHAPTER OUTLINE MATERNAL PHYSIOLOGY AND EMBRYOLOGY SONOGRAPHIC APPEARANCE OF NORMAL INTRAUTERINE PREGNANCY Gestational Sac β-hCG and Early Pregnancy Ultrasound Yolk Sac Embryo and Amnion Embryonic Cardiac Activity Umbilical Cord and Cord Cyst ESTIMATION OF GESTATIONAL AGE Gestational Sac Size Crown-Rump Length EARLY PREGNANCY FAILURE Diagnostic Findings of Early Pregnancy Failure Crown-Rump Length 7 mm or Greater and No Heartbeat Gestational Sac Mean Sac Diameter 25 mm or Greater and No Embryo Worrisome Findings of Early Pregnancy Failure

T

Embryos With Crown-Rump Length Less Than 7 mm and No Heartbeat Gestational Sac With Mean Sac Diameter 16 to 24 mm and No Embryo Gestational Sac Appearance Small Mean Sac Diameter in Relationship to Crown-Rump Length Abnormally Large Amnion With Respect to Embryo Size Yolk Sac Size and Shape Embryonic Bradycardia Subchorionic Hemorrhage ECTOPIC PREGNANCY Clinical Presentation Sonographic Diagnosis Heterotopic Gestation Serum β-hCG Levels Specific Sonographic Findings Nonspecific Sonographic Findings Adnexal Mass Free Fluid Endometrium

he first trimester of pregnancy is a period of rapid change that spans fertilization, formation of the blastocyst, implantation, gastrulation, neurulation, the embryonic period (weeks 6-10), and early fetal life.1 First-trimester sonographic diagnosis traditionally focused on evaluation of growth by serial examination to differentiate normal from abnormal gestations. This has changed since the advent of transvaginal sonography (TVS), which affords enhanced resolution over transabdominal sonography (TAS), with earlier visualization of the gestational sac and its contents,2

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Implantation Sites Pregnancy of Unknown Location Management EVALUATION OF THE EMBRYO Normal Embryologic Findings Mimicking Pathology Rhombencephalon Physiologic Anterior Abdominal Wall Herniation Abnormal Embryos GESTATIONAL TROPHOBLASTIC DISEASE Hydatidiform Molar Pregnancy Complete Molar Pregnancy Partial Molar Pregnancy Coexistent Hydatidiform Mole and Normal Fetus Persistent Trophoblastic Neoplasia Invasive Mole Choriocarcinoma Placental-Site Trophoblastic Tumor Sonographic Features of Persistent Trophoblastic Neoplasia Diagnosis and Treatment CONCLUSION

earlier identification of embryonic cardiac activity,3 and improved visualization of embryonic and fetal structures. Despite these technologic improvements, it is important to set clinically relevant and realistic goals for first-trimester sonographic diagnosis. Most examinations are requested because the patient has vaginal bleeding or pain, or a palpable mass has been identified on physical examination. Ultrasound in the first trimester is often requested to diagnose early pregnancy failure or an ectopic pregnancy.

CHAPTER 30  The First Trimester The goals of first-trimester sonography include (1) visualization and localization of the gestational sac (intrauterine or ectopic pregnancy) and (2) early identification of embryonic demise and other forms of nonviable gestation. It also seeks to identify those pregnancies that are at increased risk for early pregnancy failure. First-trimester ultrasound accurately dates the duration or menstrual/gestational age of the pregnancy and assists in early diagnosis of fetal abnormalities, including identification of embryos more likely to be abnormal, based on secondary criteria (e.g., abnormal yolk sac). In multifetal pregnancies, first-trimester ultrasound can be used to determine the number of embryos and the chorionicity and amnionicity. Current trends in ultrasound late in the first trimester focus on nuchal translucency screening combined with maternal age and maternal serum screening to determine the risk of chromosomal abnormalities and structural anomalies. Associated with the increased emphasis on late first-trimester ultrasound and first-trimester screening, there is an opportunity to visualize fetal anomalies earlier than at the time of the standard 18- to 20-week scan. First-trimester diagnosis of specific anomalies is discussed in the chapters covering those organ systems. As experience with early first-trimester ultrasound evolves, reliable sonographic indicators of ectopic pregnancy and embryonic demise have been established.4-6 The accuracy of some sonographic signs used as indicators of the presence of a live embryo or of embryonic demise depends on the use of modern, high-resolution ultrasound equipment and the operator’s expertise. Published values in the literature based on data using highfrequency transducers cannot be applied to lower-resolution 5.0-MHz transducers.7,8 The TVS signs listed in this chapter assume the use of modern equipment with a transducer frequency of at least 7 to 8 MHz, with meticulous scanning technique. Transducers with frequencies of 10 MHz or higher can provide improved spatial resolution, identifying abnormal and normal features at even earlier points in pregnancy.9 Nyberg and Filly6 emphasize that experienced physicians who interpret ultrasound rarely rely on a single parameter and simultaneously consider multiple variables to create a diagnostic impression.

MATERNAL PHYSIOLOGY AND EMBRYOLOGY All dates presented in this chapter are in menstrual age or gestational age, in keeping with the radiologic and obstetric literature, rather than in embryologic age, as used by embryologists. This can be counted as follows: Gestational age = Conceptual age + 2 weeks Early in the menstrual cycle, the pituitary secretes rising levels of follicle-stimulating hormone (FSH) and luteinizing hormone (LH), which cause the growth of 4 to 12 primordial follicles into primary ovarian follicles10 (Fig. 30.1). When a fluid-filled cavity or antrum forms in the follicle, it is referred to as a secondary follicle. The primary oocyte is off to one side of the follicle and surrounded by follicular cells or the cumulus oophorus. One follicle becomes dominant, bulges on the surface of the ovary,

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and becomes a “mature follicle” or graafian follicle. It continues to enlarge until ovulation, with the remainder of the follicles becoming atretic. The developing follicles produce estrogen. The estrogen level remains relatively low until 4 days before ovulation, when the dominant or active follicle produces an estrogen surge, after which an LH and prostaglandin surge results in ovulation. Ovulation follows the LH peak within 12 to 24 hours. Actual expulsion of the oocyte from the mature follicle is aided by several factors, including the intrafollicular pressure, possibly contraction of the smooth muscle in the theca externa stimulated by prostaglandins, and enzymatic digestion of the follicular wall.11 Ovulation occurs on approximately day 14 of the menstrual cycle with expulsion of the secondary oocyte from the surface of the ovary. In women with a menstrual cycle longer than 28 days, this ovulation occurs later, so that the secretory phase of the menstrual cycle remains at about 14 days. After ovulation, the follicle collapses to form the corpus luteum, which secretes progesterone and, to a lesser degree, estrogen. If a pregnancy does not occur, the corpus luteum involutes. In pregnancy, involution of the corpus luteum is prevented by human chorionic gonadotropin (hCG), which is produced by the outer layer of cells of the gestational or chorionic sac (syncytiotrophoblast). Before ovulation, endometrial proliferation occurs in response to estrogen secretion (Fig. 30.1). After ovulation, the endometrium becomes thickened, soft, and edematous under the influence of progesterone.12 The glandular epithelium secretes a glycogen-rich fluid. If pregnancy occurs, continued production of progesterone results in more marked hypertrophic changes in the endometrial cells and glands to provide nourishment to the blastocyst. These hypertrophic changes are referred to as the decidual reaction and occur as a hormonal response regardless of the site of implantation, intrauterine or ectopic. Oocyte transport into the fimbriated end of the fallopian tube occurs at ovulation as the secondary oocyte is expelled with the follicular fluid and is “picked up” by the fimbria. The sweeping movement of the fimbria, the currents produced by the action of the cilia of the mucosal cells, and the gentle peristaltic waves from contractions of the fallopian musculature all draw the oocyte into the tube.13 The mechanism of sperm transport is regulated to maximize the chance of fertilization and ensure the most rigorous sperm will be available.14 From 200 to 600 million sperm and the ejaculate fluid are deposited in the vaginal fornix during intercourse. Sperm must move through the cervical canal and its mucous plug, up the endometrial cavity, and down the fallopian tube to meet the awaiting oocyte within the distal third or ampullary portion of the fallopian tube. Sperm were thought to move primarily using their tails, although they travel at 2 to 3 mm per minute, which would take about 50 minutes to travel the 20 cm to their destination. Settlage et al.13 found motile sperm within the ampulla between 5 and 10 minutes after deposition near the external cervical os. If inert particles such as radioactive macroaggregates or carbon particles are placed near the external os, they too will be picked up and transported up the uterus and down the tubes. Contractions of the inner layer of myometrium are believed to create a negative pressure strong enough to suck up particles and move them up the endometrial canal. These contractions

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FIG. 30.1  Schematic Drawing of Interrelationships Among the Hypothalamus, Pituitary Gland, Ovaries, and Endometrial Lining.  FSH, Follicle-stimulating hormone; LH, luteinizing hormone. (With permission from Moore KL. The developing human: clinically oriented embryology. 10th ed. Philadelphia: Elsevier; 2016.1)

CHAPTER 30  The First Trimester Posterior wall of uterus

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Blastocysts Morula

Eight-cell stage

Four-cell stage

Two-cell stage Zygote

Follicle approaching maturity Secondary follicle Mature Growing follicle follicle Early primary Oocyte follicle

Fertilization

Oocyte in tube

Blood vessels Epithelium Corpus albicans Mature corpus luteum

Endometrium

Atretic (degenerating) follicle Atretic (degenerating) follicle

Released oocyte Ruptured follicle Connective tissue Developing corpus Coagulated blood luteum

FIG. 30.2  Diagram of Ovarian Cycle, Fertilization, and Human Development to the Blastocyst Stage. (With permission from Moore KL. The developing human: clinically oriented embryology. 10th ed. Philadelphia: Elsevier; 2016.1)

have been demonstrated in nonpregnant women and increase in strength and frequency to peak at 3.5 contractions per minute at ovulation.15 Fertilization occurs on or about day 14 as the mature ovum and sperm unite to form the zygote in the outer third of the fallopian tube (Fig. 30.2). Cellular division of the zygote occurs during transit through the fallopian tube. By the time the conceptus enters the uterus, about day 17, it is at the 12- to 15-cell stage (morula). By day 20, the conceptus has matured to the blastocyst stage. The blastocyst is a fluid-filled cyst lined with trophoblastic cells that contain a cluster of cells at one side called the inner cell mass. On day 20, the blastocyst at the site of the inner cell mass burrows through the endometrial membrane into the hyperplastic endometrium, and implantation begins16 (Fig. 30.3A). Implantation is completed by day 23 as the endometrial membrane re-forms over the blastocyst (Fig. 30.3B). During implantation, the amniotic cavity forms in the inner cell mass. A bilaminar embryonic disk separates the amniotic cavity from the exocoelomic cavity. The primary (primitive) yolk sac forms

at about 23 days of gestational age as the blastocyst cavity becomes lined by the exocoelomic membrane and hypoblast. As the extraembryonic coelom forms, the primary yolk sac is pinched off and extruded, resulting in the formation of the secondary yolk sac (Fig. 30.4). Standard embryology texts indicate that the secondary yolk sac forms at approximately 27 to 28 days of menstrual age, when the mean diameter of the gestational sac is approximately 3 mm. It is the secondary yolk sac, rather than the primary yolk sac, that is visible with ultrasound. For the remainder of this chapter, the term yolk sac is used to refer to the secondary yolk sac. The extraembryonic coelom becomes the chorionic cavity. Later, because of differential growth, the yolk sac comes to lie between the amnion and chorion. During week 4, there is rapid proliferation and differentiation of the syncytiotrophoblast, forming primary chorionic villi. Traditional thinking that the syncytiotrophoblastic cells invade the maternal endometrial vessels, leaving maternal blood to bathe the trophoblastic ring, has been challenged. Hustin16 compared TVS to hysteroscopy of the placenta, chorionic villous sampling tissue, and

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A

B FIG. 30.3  Implantation of the Blastocyst Into Endometrium.  Entire conceptus is approximately 0.1 mm at this stage. (A) Partially implanted blastocyst at approximately 22 days. (B) Almost completely implanted blastocyst at about 23 days. (With permission from Moore KL. The developing human: clinically oriented embryology. 10th ed. Philadelphia: Elsevier; 2016.1)

hysterectomy specimens with an early pregnancy in situ. Before 12 weeks, the intervillous space contains no blood, only clear fluid, and on histologic examination, the villous tissue is separated from the maternal circulation by a continuous layer of trophoblastic cells. Only after the third month does the trophoblastic shell become broken and the maternal circulation become continuous with the intervillous space. Furthermore, at weeks 8 and 9 of gestation, the trophoblastic shell forms plugs within the spiral arteries, allowing only filtered plasma to permeate the placenta.17 In two-thirds of abnormal pregnancies, the

trophoblastic shell is thinner and fragmented, and the trophoblastic invasion of the spiral arteries is reduced or absent.18 Vascularization of the placenta occurs at the beginning of the fifth week. Oh et al.19 showed significant increases in sac size from 5 weeks onward in normal intrauterine pregnancy (IUP) versus pregnancy failure. The rationale for placental vascularization was based on early work by Folkman,20 who showed that tumors can grow to a size of 3 mm being nourished only by diffusion. To exceed this size, cells must recruit host blood vessels, or the cells at the center will receive inadequate nutrition.

CHAPTER 30  The First Trimester

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A

B

C

FIG. 30.4  Formation of Secondary Yolk Sac.  (A) Approximately 26 days: formation of cavities within extraembryonic mesoderm. These cavities will enlarge to form extraembryonic coelom. (B) About 27 days and (C) 28 days: formation of secondary yolk sac with extrusion of primary yolk sac. Extraembryonic coelom will become chorionic cavity. (With permission from Moore KL. The developing human: clinically oriented embryology. 10th ed. Philadelphia: Elsevier; 2016.1)

Similarly, the rapidly growing embryonic implantation must be vascularized by the 3-mm stage that occurs at 5 weeks’ gestation. During the fifth week, the embryo is converted by the process of gastrulation from a bilaminar disk to a trilaminar disk with the three primary germ cell layers: ectoderm, mesoderm, and endoderm. During gastrulation, the primitive streak and notochord form. The primitive streak gives rise to the mesenchyme, which forms the connective tissue of the embryo and stromal components of all glands. The formation of the neural plate and its closure to form the neural tube is referred to as neurulation. This process begins

in the fifth week in the thoracic region and extends caudally and cranially, resulting in complete closure by the end of the sixth week (day 42). Failure of closure of the neural tube results in neural tube defects. During the fifth week, two cardiac tubes (the primitive heart) develop from splanchnic mesodermal cells. By the end of the fifth week, these tubes begin to pump into a primitive paired vascular system. By the end of the fifth week, a vascular network develops in the chorionic villi that connect through the umbilical arteries and vein to the primitive embryonic vascular network. Essentially all internal and external structures appear in the adult form during the embryonic period, which ends at 10

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menstrual weeks. By the end of the sixth week, blood flow is unidirectional, and by the end of the eighth week, the heart attains its definitive form. The peripheral vascular system develops slightly later and is completed by the end of the tenth week. The primitive gut forms during week 6. The midgut herniates into the umbilical cord from week 8 through the end of week 12. The rectum separates from the urogenital sinus by the end of week 8, and the anal membrane perforates by the end of week 10. The metanephros, or primitive kidneys, ascend from the pelvis, starting at approximately week 8, but do not reach their adult position until week 11. Limbs are formed with separate fingers and toes. Almost all congenital malformations except abnormalities of the genitalia originate before or during the embryonic period. External genitalia are still in a sexless state at the end of week 10 and do not reach mature fetal form until the end of week 14. Early in the fetal period, body growth is rapid and head growth relatively slower, with the crown-rump length (CRL) doubling between weeks 11 and 14.

SONOGRAPHIC APPEARANCE OF NORMAL INTRAUTERINE PREGNANCY Gestational Sac Implantation usually occurs in the fundal region of the uterus between day 20 and day 23.21 In a study of early implantation sites in 21 patients, it was found that implantation occurs most frequently on the uterine wall ipsilateral to the ovulating ovary and least often on the contralateral wall.21 In addition, in a study of predominant sleeping positions in the peri-implantation period, Magann et al.22 found that the 33% of women who slept prone were most likely to have a high or fundal implantation than those who slept on their back or side. The latter groups predominantly had implantations corresponding to their resting posture. At 23 days, the entire conceptus measures approximately 0.1 mm in diameter and cannot be imaged by TAS or TVS techniques. The earliest sonographic sign of an IUP was described by Yeh et al.,23 who identified a focal echogenic zone of decidual thickening at the site of implantation at about 3 1 2 to 4 weeks of gestational age. This sign is nonspecific and of limited diagnostic value. The first reliable gray-scale evidence of an IUP is visualization of a small (1-2 mm fluid collection surrounded by an echogenic rim) gestational sac within the thickened decidua. Yeh et al.23 originally identified this sign, referred to as the intradecidual sign, which is seen at about 4.5 weeks’ gestation. An intradecidual gestational sac should be eccentrically located within the endometrium. It is important to ensure that the sac abuts the endometrial canal to distinguish an intrauterine gestational sac from a decidual cyst. The intradecidual sign was originally described on TAS,23 with a sensitivity of 92%, specificity 100%, and overall accuracy of 93% for distinguishing between early IUP and ectopic pregnancy. Chiang et al.24 looked at this sign using TVS and found overall sensitivity of 60% to 68%, specificity of 97% to 100%,

and overall accuracy of 67% to 73%, indicating that the sign, when present, is useful for diagnosing an IUP. When absent, it does not reliably exclude an IUP. It is usually possible to demonstrate an early IUP as a small intradecidual sac between 4 1 2 and 5 weeks’ gestational age using TVS (Figs. 30.5 and 30.6). Using a high-frequency (7.5-10 MHz) TVS, Oh et al.19 were able to identify a gestational sac in all 67 patients scanned between 28 and 42 days’ gestational age (mean sac diameter [MSD] between 28 and 35 days was 2.6 mm). The double-decidual sign (also called double decidual sac sign) was described by Bradley et al.25 and Nyberg et al.26 as a method for distinguishing between an early IUP and an endometrial fluid collection of other origin, such as the pseudosac of an ectopic pregnancy. A well-defined double-decidual sign is an accurate predictor of the presence of an IUP. A vague or absent double-decidual sign should be considered nondiagnostic because it does not reliably exclude an IUP.27 The endometrium in the pregnant state is called the decidua capsularis, decidua vera, and decidua basalis. The doubledecidual sign is based on visualization of the gestational sac as an echogenic ring formed by the decidua capsularis and chorion laeve eccentrically located within the decidua vera (Fig. 30.6), forming two echogenic rings. The outer ring is formed by the echogenic endometrium of the lining of the uterus. The decidua basalis–chorion frondosum (future placenta) may also be visualized as an area of eccentric echogenic thickening. The double-decidual sign was initially described, and is considered most useful, on TAS. It can usually be identified by about 5.5 to 6 weeks’ gestational age and is useful in establishing an intrauterine gestation prior to TAS ability to visualize the yolk sac. It is almost always resolvable by the time the gestational sac reaches 10 mm, at which point the yolk sac is typically visible by TVS, thus diminishing the usefulness of this finding.28 Parvey et al.29 found a double-decidual sign in only 53% of early pregnancies with no yolk sac or embryo present. They also assessed visualization of the echogenic chorionic rim alone as a sign of IUP and found its presence in 64% of cases. It was more clearly defined in later pregnancies with a higher β-hCG level (mean, 16,082 mIU/mL) and thin, less clearly defined, or even absent in the earliest pregnancies. Using a higher-frequency 10-MHz transvaginal transducer to scan patients who had a positive pregnancy test and only a small (5.6 mm), and one yolk sac was irregular in contour. Therefore in MCMA twins, a single, large, or normal-sized yolk sac with two live embryos can result in a normal twin delivery.

Embryo and Amnion Visualization of the amnion in the absence of an embryo usually occurs in intrauterine embryonic death as a result of resorption of the embryo45 (Fig. 30.12). Amniotic fluid is a colorless, fetal dermal transudate; as the skin cornifies and the kidneys begin to function, at about 11 weeks, it becomes pale yellow. The amnion becomes visible when the embryo has a CRL of 2 mm at 6 weeks. The cavity becomes almost spherical by about 7 weeks, likely a result of the more rapid increase in fluid volume relative to the growth of the sac membrane to accommodate it. The actual rate of fluid increase is more rapid after about 9 weeks (Fig. 30.13), when urine is produced. Fluid accumulates at about 5 mL per day at 12 weeks. The amniotic cavity expands to fill the chorionic cavity completely by week 16. It is therefore normal to identify the amnion as a separate membrane or sac within the chorionic cavity before 16 weeks (Fig. 30.14). Occasionally, the amnion and chorionic membranes may fail to be juxtaposed at week 16 (so-called unfused amnion), and separation of these membranes may persist for a short time.46 Iatrogenic or spontaneous rupture of the amniotic membrane in the first trimester is a rare occurrence and even more rarely results in the amniotic band sequence. This rupture may result in retraction of the amnion in part or in whole, up to the base of the umbilical cord where the amnion and chorion are adherent. More often, the floating amniotic membranes do not adhere to the fetus, and no fetal anomalies occur.

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PART IV

A

B

C

D

FIG. 30.9  Normal Yolk Sac.  (A) Sagittal and (B) transverse TVS of the early IUP demonstrates the yolk sac at 5 weeks 5 days. (C) Yolk sac is seen separate from embryo (calipers) at 9 weeks. (D) At 11 weeks, yolk sac lies at edge of chorionic sac outside of early amnion.

ys

e

FIG. 30.10  Normal Embryo at 8 Weeks.  TVS shows vitelline duct (thick arrow), yolk sac (ys), and embryo (e).

Embryonic Cardiac Activity Using TVS, an embryo with a CRL as small as 1 to 2 mm may be identified immediately adjacent to the yolk sac (Fig. 30.15). In normal pregnancies the embryo can be identified in gestational sacs as small as 10 mm and should always be identified when

FIG. 30.11  Early Monochorionic Diamniotic (MCDA) Twins.  Two separate yolk sacs are seen within a single chorion at 5 weeks 5 days. It is too early to visualize the two amnions.

the MSD is equal to or greater than 25 mm with optimal scanning parameters and high-resolution TVS.4,5 Embryologic data suggest the tubular heart begins to beat at 36 to 37 days’ gestational age.10 Cadkin and McAlpin47 described cardiac activity adjacent to the yolk sac before the embryo can

CHAPTER 30  The First Trimester

A

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B

FIG. 30.12  Abnormal Amnion.  (A) TVS at 9 weeks demonstrates an empty amnion within the gestational sac. This pregnancy eventually failed. (B) Expanded amnion at 7 weeks. Note how the amnion is much larger than would be expected for an embryo (calipers) of this size. This pregnancy did not progress.

Umbilical Cord and Cord Cyst

FIG. 30.13  Normal 9-Week 4-Day Gestation.  TVS shows the embryo (calipers) and the amnion (arrow) separate from the surrounding chorion.

be fully visualized at the end of the fifth week. Ragavendra et al.48 placed a 12.5-MHz endoluminal catheter transducer into the endometrial canal adjacent to the gestational sac. They identified cardiac activity in an embryo with a CRL of 1.5 mm and resolved the two walls of the heart, seen only as a tube. Using TVS, cardiac activity is typically seen by the time an embryo is 2 mm in size, and is almost always seen by 5-mm CRL. However, for strict diagnosis of nonviable pregnancy the threshold is set at 7 mm CRL.4,5 Normal embryonic cardiac activity is greater than 100 beats per minute (bpm) (Video 30.1) when the embryo is less than 6.3 weeks and 120 bpm at or beyond 6.3 weeks.49 When embryonic cardiac activity is visualized and the rate is less than 100 bpm, then follow-up should be obtained. We have seen pregnancies with small embryos of 1–2 mm in size with heart rates of 80–99 bpm with normal follow-up (see Fig. 30.15).

The umbilical cord is formed at the end of the sixth week (CRL = 4.0 mm) as the amnion expands and envelops the connecting stalk, the yolk stalk, and the allantois. The cord contains two umbilical arteries, a single umbilical vein, the allantois, and yolk stalk (also called the omphalomesenteric duct or vitelline duct), all of which are embedded in Wharton jelly. The umbilical arteries arise from the internal iliac arteries and in the newborn become the superior vesical arteries and the medial umbilical ligaments. The umbilical vein carries oxygenated blood from the placenta to the fetus. The oxygenated blood is shunted through the ductus venosus into the inferior vena cava and the heart. The single left umbilical vein in the newborn becomes the ligamentum teres, which attaches to the left branch of the portal vein. The ductus venosus becomes the ligamentum venosum. The allantois is associated with bladder development and becomes the urachus and the median umbilical ligament. It extends into the proximal portion of the umbilical cord. The yolk stalk connects the primitive gut to the yolk sac. The paired vitelline arteries and veins accompany the stalk to provide blood supply to the yolk sac. The arteries arise from the dorsal aorta to supply initially the yolk sac, then the primitive gut. The arteries remain as the celiac axis, superior and inferior mesenteric arteries supplying the foregut, midgut, and hindgut, respectively. The vitelline veins drain directly into the sinus venosus of the heart. The right vein is later incorporated into the right hepatic vein. The portal vein is also formed by an anastomotic network of vitelline veins. The length of the umbilical cord has a close linear relationship with gestational age in normal pregnancies. Hill et al.50 found they could reliably measure the cord lengths in 53 embryos at 6 to 11 weeks’ gestational age. Also, the cord lengths in 60% of dead embryos were more than two standard deviations (2 SD) below the value for that expected gestational age. The width of the umbilical cord has also been measured sonographically, and Ghezzi et al.51 found a steady increase from 8 to 15 weeks. There was a significant correlation between cord

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FIG. 30.14  Normal 12-Week Gestation.  (A) Surface rendering image from three-dimensional TVS shows the embryo within the amnion. (B) Two-dimensional TVS shows the amnion (arrow) approaching, but not fused with, the chorionic sac.

A

B

C

D

FIG. 30.15  Normal Embryo With Early Cardiac Activity.  (A) Image shows 5-week 6-day embryo (calipers) adjacent to the yolk sac. (B) M-mode ultrasound shows a heart rate of 96 beats/min. (C) Two days later, the embryonic pole (calipers) has grown and (D) the heart rate has increased to 111 beats/min. See also Video 30.1.

CHAPTER 30  The First Trimester diameter and gestational age (r = 0.78; P < .001), CRL (r = 0.75; P < .001), and biparietal diameter (r = 0.81; P < .001) but no correlation with birth weight or placental weight. The cord diameter was significantly smaller by at least 2 SD in patients who developed preeclampsia or had a miscarriage. Cysts and pseudocysts within the cord have been described in the first trimester.52 Cysts are usually seen in the eighth week and usually resolve by the 12th week. They are singular, closer to the embryo/fetus than the placenta, with a mean size of 5.2 mm (Fig. 30.16). Cysts may originate from remnants of the allantois or omphalomesenteric duct and characteristically have an epithelial lining.53 It is hypothesized that the cyst is an amnion

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inclusion cyst that occurs as the amnion was enveloping the umbilical cord. In a series of 1159 consecutive patients scanned between 7 and 14 weeks, Ghezzi et al.54 found 24 cord cysts at a prevalence of 2.1%. Single cysts in the first trimester were associated with a normal outcome and a healthy infant, whereas multiple or complex cysts were associated with an increased risk of miscarriage or aneuploidy. Thus although umbilical cord cysts have been associated with chromosomal abnormalities if seen in the second and third trimesters, those seen in the first trimester typically resolve and are not associated with poor outcome.

ESTIMATION OF GESTATIONAL AGE During the first trimester, gestational age can be estimated sonographically with greater accuracy than at any other stage of pregnancy. As pregnancy progresses, biologic variation results in wider variation around the mean for all sonographic parameters at a given gestational age.

Gestational Sac Size

FIG. 30.16  Umbilical Cord Cyst at 10 Weeks.  TVS shows a cyst (small arrow) arising from the cord (large arrow). On subsequent examination (not shown) the cyst was no longer seen.

The MSD offers an opportunity to date an early pregnancy before the embryo can be visualized. The MSD is an average of the diameter of the sac, obtained by adding the anteroposterior and craniocaudad diameters on the sagittal view of the uterus to the transverse diameter obtained on the transverse view and dividing by three (Fig. 30.17). The gestational age can be predicted by MSD using the following formula: menstrual age in days = MSD in mm + 30.55 The MSD increases in size at a rate of 1.1 mm per day.56 If MSD is very small, about 2 mm, gestational age is 4 to 4 1 2 weeks, and MSD of about 5 mm is 5 weeks. At 5 1 2 weeks, a yolk sac appears (see Fig. 30.9A and B). At 6 weeks, an embryo first appears adjacent to the yolk sac (see Fig. 30.15A). When the embryo is first seen, cardiac activity is appreciated as a consistent flicker40 (Fig. 30.15B and Video 30.1).

FIG. 30.17  Gestational Age Established by Mean Sac Diameter (MSD).  Gestational age can be estimated measuring the sac in three dimensions. Average of three measurements is used to correlate with gestational age prior to visualization of the embryonic pole. MSD of 12 mm is consistent with gestational age of 6 weeks 0 days. However, these data are not used to formally establish pregnancy dating. Sonographic dating of the pregnancy is done with the crown-rump length when cardiac activity is present.

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Crown-Rump Length Once the embryonic pole is visualized (just before 6 weeks), measurement of the CRL of the embryo is considered the most accurate method to date the pregnancy.57,58

EARLY PREGNANCY FAILURE One of the most important roles of ultrasound in the first trimester is to identify early pregnancies that have failed or that are more likely to fail. Studies have demonstrated a 20% to 31% rate of early pregnancy loss after implantation in normal healthy volunteers.59,60 Many pregnancies abort before the pregnancy is confirmed by either ultrasound or a chemical pregnancy test. Approximately 50% of miscarriage is caused by chromosomal abnormalities.61 Early pathologic studies of Hertig and Rock,60 also showed a high frequency of morphologic abnormalities in preimplantation embryos. Loss rates are increased with increased maternal age and prior history of early pregnancy failure.62 Although the etiology of first-trimester pregnancy loss is still not fully understood, there are many known and suspected causes. In a study of 232 first-trimester patients (normal, healthy women, positive urinary pregnancy test, and no vaginal bleeding) with TVS at the first visit, Goldstein57 determined the incidence of subsequent pregnancy loss by following all to delivery or spontaneous abortion. This group had an overall pregnancy loss rate of 11.5% in the embryonic period, (i.e., 35) and low serum β-hCG ( 6 mm Calcified yolk sac Embryonic bradycardia Large subchorionic hemorrhage

Expanded amnion or empty amnion as evaluated by an experienced sonologist is diagnostic of miscarriage. If any uncertainty is present, then follow-up should be obtained. Findings are associated with miscarriage, but the size of the embryo and presence or absence of cardiac activity guides the diagnosis. Heart rate (HR) < 100 may be seen with 1- to 2-mm embryo and be a normal finding. In general, when HR is 10 mm) on prenatal sonography. J Ultrasound Med. 1997;16(11):731-734. 48. Ghai S, Fong KW, Toi A, et al. Prenatal US and MR imaging findings of lissencephaly: review of fetal cerebral sulcal development. Radiographics. 2006;26(2):389-405. 49. Quarello E, Stirnemann J, Ville Y, Guibaud L. Assessment of fetal sylvian fissure operculization between 22 and 32 weeks: a subjective approach. Ultrasound Obstet Gynecol. 2008;32(1):44-49. 50. Toi A, Lister WS, Fong KW. How early are fetal cerebral sulci visible at prenatal ultrasound and what is the normal pattern of early fetal sulcal development? Ultrasound Obstet Gynecol. 2004;24(7):706-715. 51. Pashaj S, Merz E, Wellek S. Biometry of the fetal corpus callosum by threedimensional ultrasound. Ultrasound Obstet Gynecol. 2013;42(6): 691-698. 52. Rizzo G, Capponi A, Pietrolucci ME, et al. An algorithm based on OmniView technology to reconstruct sagittal and coronal planes of the fetal brain from volume datasets acquired by three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2011;38(2):158-164. 53. Tonni G, Grisolia G, Sepulveda W. Second trimester fetal neurosonography: reconstructing cerebral midline anatomy and anomalies using a novel three-dimensional ultrasound technique. Prenat Diagn. 2014;34(1): 75-83. 54. Levine D, Barnes PD, Madsen JR, et al. Central nervous system abnormalities assessed with prenatal magnetic resonance imaging. Obstet Gynecol. 1999;94(6):1011-1019. 55. Pooh RK, Nagao Y, Pooh K. Fetal neuroimaging by transvaginal 3D ultrasound and MRI. Ultrasound Rev Obstet Gynecol. 2006;6:123-134. 56. Fong K, Chong K, Toi A, et al. Fetal ventriculomegaly secondary to isolated large choroid plexus cysts: prenatal findings and postnatal outcome. Prenat Diagn. 2011;31(4):395-400. 57. Van den Hof MC, Wilson RD. Fetal soft markers in obstetric ultrasound. J Obstet Gynaecol Can. 2005;27(6):592-636. 58. Ebrashy A, Kurjak A, Adra A, et al. Controversial ultrasound findings in mid trimester pregnancy. Evidence based approach. J Perinat Med. 2016;44(2):131-137. 59. Chapman T, Mahalingam S, Ishak GE, et al. Diagnostic imaging of posterior fossa anomalies in the fetus and neonate: part 1, normal anatomy and classification of anomalies. Clin Imaging. 2015;39(1):1-8. 60. Gandolfi Colleoni G, Contro E, et al. Prenatal diagnosis and outcome of fetal posterior fossa fluid collections. Ultrasound Obstet Gynecol. 2012;39(6): 625-631. 61. Chen CY, Chen FH, Lee CC, et al. Sonographic characteristics of the cavum velum interpositum. AJNR Am J Neuroradiol. 1998;19(9):1631-1635. 62. Shah PS, Blaser S, Toi A, et al. Cavum veli interpositi: prenatal diagnosis and postnatal outcome. Prenat Diagn. 2005;25(7):539-542. 63. Eisenberg VH, Zalel Y, Hoffmann C, et al. Prenatal diagnosis of cavum velum interpositum cysts: significance and outcome. Prenat Diagn. 2003; 23(10):779-783. 64. Saba L, Anzidei M, Raz E, et al. MR and CT of brain’s cava. J Neuroimaging. 2013;23(3):326-335. 65. Vergani P, Locatelli A, Piccoli MG, et al. Ultrasonographic differential diagnosis of fetal intracranial interhemispheric cysts. Am J Obstet Gynecol. 1999;180(2 Pt 1):423-428. 66. Gaglioti P, Oberto M, Todros T. The significance of fetal ventriculomegaly: etiology, short- and long-term outcomes. Prenat Diagn. 2009;29(4): 381-388. 67. Tully HM, Dobyns WB. Infantile hydrocephalus: a review of epidemiology, classification and causes. Eur J Med Genet. 2014;57(8):359-368. 68. Verhagen JM, Schrander-Stumpel CT, Krapels IP, et al. Congenital hydrocephalus in clinical practice: a genetic diagnostic approach. Eur J Med Genet. 2011;54(6):e542-e547.

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69. Guibaud L. Fetal cerebral ventricular measurement and ventriculomegaly: time for procedure standardization. Ultrasound Obstet Gynecol. 2009; 34(2):127-130. 70. Heiserman J, Filly RA, Goldstein RB. Effect of measurement errors on sonographic evaluation of ventriculomegaly. J Ultrasound Med. 1991; 10(3):121-124. 71. Melchiorre K, Bhide A, Gika AD, et al. Counseling in isolated mild fetal ventriculomegaly. Ultrasound Obstet Gynecol. 2009;34(2):212-224. 72. Farrell TA, Hertzberg BS, Kliewer MA, et al. Fetal lateral ventricles: reassessment of normal values for atrial diameter at US. Radiology. 1994; 193(2):409-411. 73. Filly RA, Goldstein RB. The fetal ventricular atrium: fourth down and 10 mm to go. Radiology. 1994;193(2):315-317. 74. Mahony BS, Nyberg DA, Hirsch JH, et al. Mild idiopathic lateral cerebral ventricular dilatation in utero: sonographic evaluation. Radiology. 1988;169(3):715-721. 75. Hertzberg BS, Lile R, Foosaner DE, et al. Choroid plexus–ventricular wall separation in fetuses with normal-sized cerebral ventricles at sonography: postnatal outcome. AJR Am J Roentgenol. 1994;163(2):405-410. 76. Pagani G, Thilaganathan B, Prefumo F. Neurodevelopmental outcome in isolated mild fetal ventriculomegaly: systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2014;44(3):254-260. 77. Weichert J, Hartge D, Krapp M, et al. Prevalence, characteristics and perinatal outcome of fetal ventriculomegaly in 29,000 pregnancies followed at a single institution. Fetal Diagn Ther. 2010;27(3):142-148. 78. Gaglioti P, Danelon D, Bontempo S, et al. Fetal cerebral ventriculomegaly: outcome in 176 cases. Ultrasound Obstet Gynecol. 2005;25(4):372-377. 79. D’Addario V, Pinto V, Di Cagno L, Pintucci A. Sonographic diagnosis of fetal cerebral ventriculomegaly: an update. J Matern Fetal Neonatal Med. 2007;20(1):7-14. 80. Vintzileos AM, Ingardia CJ, Nochimson DJ. Congenital hydrocephalus: a review and protocol for perinatal management. Obstet Gynecol. 1983;62(5): 539-549. 81. Lee JE, Gleeson JG. Cilia in the nervous system: linking cilia function and neurodevelopmental disorders. Curr Opin Neurol. 2011;24(2): 98-105. 82. McAllister JP 2nd. Pathophysiology of congenital and neonatal hydrocephalus. Semin Fetal Neonatal Med. 2012;17(5):285-294. 83. Monteagudo A, Timor-Tritsch IE. Moomjy M. Nomograms of the fetal lateral ventricles using transvaginal sonography. J Ultrasound Med. 1993;12(5):265-269. 84. Garel C, Fetal MRI. what is the future? Ultrasound Obstet Gynecol. 2008;31(2):123-128. 85. Morris JE, Rickard S, Paley MN, et al. The value of in-utero magnetic resonance imaging in ultrasound diagnosed foetal isolated cerebral ventriculomegaly. Clin Radiol. 2007;62(2):140-144. 86. Stroustrup Smith A, Levine D, et al. Magnetic resonance imaging of the kinked fetal brain stem: a sign of severe dysgenesis. J Ultrasound Med. 2005;24(12):1697-1709. 87. Baffero GM, Crovetto F, Fabietti I, et al. Prenatal ultrasound predictors of postnatal major cerebral abnormalities in fetuses with apparently isolated mild ventriculomegaly. Prenat Diagn. 2015;35(8):783-788. 88. Laskin MD, Kingdom J, Toi A, et al. Perinatal and neurodevelopmental outcome with isolated fetal ventriculomegaly: a systematic review. J Matern Fetal Neonatal Med. 2005;18(5):289-298. 89. Sadan S, Malinger G, Schweiger A, et al. Neuropsychological outcome of children with asymmetric ventricles or unilateral mild ventriculomegaly identified in utero. BJOG. 2007;114(5):596-602. 90. Uher BF, Golden JA. Neuronal migration defects of the cerebral cortex: a destination debacle. Clin Genet. 2000;58(1):16-24. 91. Barkovich AJ, Guerrini R, Kuzniecky RI, et al. A developmental and genetic classification for malformations of cortical development: update 2012. Brain. 2012;135(Pt 5):1348-1369. 92. Sarnat HB, Flores-Sarnat L. Integrative classification of morphology and molecular genetics in central nervous system malformations. Am J Med Genet A. 2004;126a(4):386-392. 93. van der Knaap MS, Valk J. Classification of congenital abnormalities of the CNS. AJNR Am J Neuroradiol. 1988;9(2):315-326.

94. Greene ND, Copp AJ. Neural tube defects. Annu Rev Neurosci. 2014;37:221-242. 95. Goldstein RB, Filly RA. Prenatal diagnosis of anencephaly: spectrum of sonographic appearances and distinction from the amniotic band syndromex. AJR Am J Roentgenol. 1988;151:547-550. 96. Naidich TP, Griffiths PD, Rosenbloom L. Central nervous system injury in utero: selected entities. Pediatr Radiol. 2015;45(Suppl. 3):S454-S462. 97. Sepulveda W, Corral E, Ayala C, et al. Chromosomal abnormalities in fetuses with open neural tube defects: prenatal identification with ultrasound. Ultrasound Obstet Gynecol. 2004;23(4):352-356. 98. Cafici D, Sepulveda W. First-trimester echogenic amniotic fluid in the acrania-anencephaly sequence. J Ultrasound Med. 2003;22(10): 1075-1079. 99. Engels AC, Joyeux L, Brantner C, et al. Sonographic detection of central nervous system defects in the first trimester of pregnancy. Prenat Diagn. 2016;36(3):266-273. 100. Chen CP, Chang TY, Lin YH, Wang W. Prenatal sonographic diagnosis of acrania associated with amniotic bands. J Clin Ultrasound. 2004;32(5): 256-260. 101. Goldstein RB, LaPidus AS, Filly RA. Fetal cephaloceles: diagnosis with US. Radiology. 1991;180(3):803-808. 102. Kasprian GJ, Paldino MJ, Mehollin-Ray AR, et al. Prenatal imaging of occipital encephaloceles. Fetal Diagn Ther. 2015;37(3):241-248. 103. Hoving EW. Nasal encephaloceles. Childs Nerv Syst. 2000;16(10-11): 702-706. 104. Moron FE, Morriss MC, Jones JJ, Hunter JV. Lumps and bumps on the head in children: use of CT and MR imaging in solving the clinical diagnostic dilemma. Radiographics. 2004;24(6):1655-1674. 105. Hunt JA, Hobar PC. Common craniofacial anomalies: facial clefts and encephaloceles. Plast Reconstr Surg. 2003;112(2):606-615. 106. Tirumandas M, Sharma A, Gbenimacho I, et al. Nasal encephaloceles: a review of etiology, pathophysiology, clinical presentations, diagnosis, treatment, and complications. Childs Nerv Syst. 2013;29(5):739-744. 107. Chen CP. Syndromes, disorders and maternal risk factors associated with neural tube defects (I). Taiwan J Obstet Gynecol. 2008;47(1):1-9. 108. Copp AJ, Stanier P, Greene ND. Neural tube defects: recent advances, unsolved questions, and controversies. Lancet Neurol. 2013;12(8): 799-810. 109. Chen CP. Syndromes, disorders and maternal risk factors associated with neural tube defects (V). Taiwan J Obstet Gynecol. 2008;47(3): 259-266. 110. Brunelle F, Baraton J, Renier D, et al. Intracranial venous anomalies associated with atretic cephalocoeles. Pediatr Radiol. 2000;30(11):743-747. 111. Siverino RO, Guarrera V, Attina G, et al. Parietal atretic cephalocele: associated cerebral anomalies identified by CT and MR imaging. Neuroradiol J. 2015;28(2):217-221. 112. Bannister CM, Russell SA, Rimmer S, et al. Can prognostic indicators be identified in a fetus with an encephalocele? Eur J Pediatr Surg. 2000;10(Suppl. 1):20-23. 113. Bui CJ, Tubbs RS, Shannon CN, et al. Institutional experience with cranial vault encephaloceles. J Neurosurg. 2007;107(1 Suppl.):22-25. 114. Tissir F, Qu Y, Montcouquiol M, et al. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat Neurosci. 2010;13(6):700-707. 115. Waters AM, Beales PL. Ciliopathies: an expanding disease spectrum. Pediatr Nephrol. 2011;26(7):1039-1056. 116. Brancati F, Dallapiccola B, Valente EM. Joubert syndrome and related disorders. Orphanet J Rare Dis. 2010;5:20. 117. Pugash D, Oh T, Godwin K, et al. Sonographic ‘molar tooth’ sign in the diagnosis of Joubert syndrome. Ultrasound Obstet Gynecol. 2011;38(5): 598-602. 118. Chen CP. Meckel syndrome: genetics, perinatal findings, and differential diagnosis. Taiwan J Obstet Gynecol. 2007;46(1):9-14. 119. Aguirre-Pascual E, Epelman M, Johnson AM, et al. Prenatal MRI evaluation of limb-body wall complex. Pediatr Radiol. 2014;44(11):1412-1420. 120. Daltro P, Fricke BL, Kline-Fath BM, et al. Prenatal MRI of congenital abdominal and chest wall defects. AJR Am J Roentgenol. 2005;184(3): 1010-1016.

CHAPTER 34  The Fetal Brain 121. Iqbal CW, Derderian SC, Cheng Y, et al. Amniotic band syndrome: a single-institutional experience. Fetal Diagn Ther. 2015;37(1):1-5. 122. D’Addario V, Rossi AC, Pinto V, et al. Comparison of six sonographic signs in the prenatal diagnosis of spina bifida. J Perinat Med. 2008;36(4): 330-334. 123. Chen CP. Syndromes, disorders and maternal risk factors associated with neural tube defects (III). Taiwan J Obstet Gynecol. 2008;47(2):131-140. 124. Thompson DN. Postnatal management and outcome for neural tube defects including spina bifida and encephalocoeles. Prenat Diagn. 2009;29(4): 412-419. 125. Kawamura T, Morioka T, Nishio S, et al. Cerebral abnormalities in lumbosacral neural tube closure defect: MR imaging evaluation. Childs Nerv Syst. 2001;17(7):405-410. 126. McLone DG, Dias MS. The Chiari II malformation: cause and impact. Childs Nerv Syst. 2003;19(7-8):540-550. 127. Miller E, Widjaja E, Blaser S, et al. The old and the new: supratentorial MR findings in Chiari II malformation. Childs Nerv Syst. 2008;24(5): 563-575. 128. Stoll C, Dott B, Alembik Y, Roth MP. Associated malformations among infants with neural tube defects. Am J Med Genet A. 2011;155A(3): 565-568. 129. Nielsen LA, Maroun LL, Broholm H, et al. Neural tube defects and associated anomalies in a fetal and perinatal autopsy series. APMIS. 2006;114(4): 239-246. 130. Bahlmann F, Reinhard I, Schramm T, et al. Cranial and cerebral signs in the diagnosis of spina bifida between 18 and 22 weeks of gestation: a German multicentre study. Prenat Diagn. 2015;35(3):228-235. 131. Bredaki FE, Poon LC, Birdir C, et al. First-trimester screening for neural tube defects using alpha-fetoprotein. Fetal Diagn Ther. 2012;31(2): 109-114. 132. Campbell J, Gilbert WM, Nicolaides KH, Campbell S. Ultrasound screening for spina bifida: cranial and cerebellar signs in a high-risk population. Obstet Gynecol. 1987;70(2):247-250. 133. Ball RH, Filly RA, Goldstein RB, Callen PW. The lemon sign: not a specific indicator of meningomyelocele. J Ultrasound Med. 1993;12(3):131-134. 134. Barkovich AJ, Gressens P, Evrard P. Formation, maturation, and disorders of brain neocortex. AJNR Am J Neuroradiol. 1992;13(2):423-446. 135. Callen AL, Filly RA. Supratentorial abnormalities in the Chiari II malformation, I: the ventricular “point.”. J Ultrasound Med. 2008;27(1):33-38. 136. Bernard JP, Cuckle HS, Stirnemann JJ, et al. Screening for fetal spina bifida by ultrasound examination in the first trimester of pregnancy using fetal biparietal diameter. Am J Obstet Gynecol. 2012;207(4):306 e1-306 e5. 137. Buisson O, De Keersmaecker B, Senat MV, et al. Sonographic diagnosis of spina bifida at 12 weeks: heading towards indirect signs. Ultrasound Obstet Gynecol. 2002;19(3):290-292. 138. Chaoui R, Benoit B, Heling KS, et al. Prospective detection of open spina bifida at 11-13 weeks by assessing intracranial translucency and posterior brain. Ultrasound Obstet Gynecol. 2011;38(6):722-726. 139. Chaoui R, Nicolaides KH. From nuchal translucency to intracranial translucency: towards the early detection of spina bifida. Ultrasound Obstet Gynecol. 2010;35(2):133-138. 140. Chen FC, Gerhardt J, Entezami M, et al. Detection of spina bifida by first trimester screening—results of the prospective multicenter Berlin IT-Study. Ultraschall Med. 2017;38(2):151-157. 141. Finn M, Sutton D, Atkinson S, et al. The aqueduct of Sylvius: a sonographic landmark for neural tube defects in the first trimester. Ultrasound Obstet Gynecol. 2011;38(6):640-645. 142. Kappou D, Papastefanou I, Pilalis A, et al. Towards detecting open spina bifida in the first trimester: the examination of the posterior brain. Fetal Diagn Ther. 2015;37(4):294-300. 143. Lachmann R, Chaoui R, Moratalla J, et al. Posterior brain in fetuses with open spina bifida at 11 to 13 weeks. Prenat Diagn. 2011;31(1):103-106. 144. Lachmann R, Picciarelli G, Moratalla J, et al. Frontomaxillary facial angle in fetuses with spina bifida at 11-13 weeks’ gestation. Ultrasound Obstet Gynecol. 2010;36(3):268-271. 145. Simon EG, Arthuis CJ, Haddad G, et al. Biparietal/transverse abdominal diameter ratio 97% of cases). This cranial lesion consists of variable degrees of displacement of the cerebellar vermis, fourth ventricle, and medulla oblongata through the foramen magnum into the upper cervical canal and is usually easier to identify than the spinal lesion between 16 and 24 weeks’ gestation. In transaxial scans through the posterior fossa, Chiari II malformation is manifest as a deformation of the cerebellar shape (banana sign) and nonvisualization of the cisterna magna. Cranial malformations may signal the sonographer that a detailed study of the spine is required to search for spina bifida.

Anatomic Landmarks Used to Establish Level of Bony Defect • T12 corresponds to the medial ends of the most caudal ribs. • L5-S1 lies at the superior margin of the iliac wing.28 • S4 is the most caudal vertebral body ossification center in the second trimester.65 • S5 is the most caudal vertebral body ossification center in the third trimester.65 Thoracic (T), lumbar (L), and sacral (S) vertebrae.

CHAPTER 35  The Fetal Spine

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M M

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12 5

5 L

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FIG. 35.13  Myeloschisis.  (A) Posterior transaxial scan shows splaying of the lumbar laminae (arrows) away from midline. Only a thin membrane (M) overlies the spinal defect posteriorly. (B) Posterior transaxial scan of the specimen after delivery shows in more detail the splaying of the laminae (arrows) away from midline and the membrane (M) covering the defect. (C) Lateral transaxial scan of specimen shows increased distance between the pedicles (curved arrows) and mild lateral angulation of the pedicles away from their expected positions (straight arrow, ossified centrum). (D) Lateral longitudinal scan of specimen shows the progressive enlargement of the interpedicular distances in the lumbar spine, indicative of spina bifida. Ossified pedicles (straight arrows); iliac wing (curved arrow). (E) Posterior longitudinal scan of specimen shows abrupt truncation of the soft tissues of the fetal back (long arrow) at the site of the open neural tube defect; short arrow, spinal cord. (F) Radiograph of specimen shows divergence of the laminae (L) away from midline instead of the normal course, which is toward midline. (G) Photograph of myeloschisis defect of the thoracolumbar spine shows exposed, disorganized neural tissue within the defect. (H) Three-dimensional scan of another fetus at 19 weeks, as viewed from the posterior aspect of the fetus. Note the abnormal divergence of the pedicles in the lumbar spine (arrows, 12th rib level; 5, level L5). (I) Three-dimensional scan of a different fetus at 21 weeks, as viewed from the posterior aspect of the fetus. Note the divergence of the lumbar pedicles and the splaying of the laminae (L) away from the midline. (I courtesy of Siemens Ultrasound.)

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SC

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L

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FIG. 35.14  Spina Bifida With Myelomeningocele, 17 Weeks’ Gestation Specimen.  (A) Posterior transaxial scan of the midlumbar spine shows the splaying of the laminae (curved arrows) and the myelomeningocele sac (short arrows). (B) Posterior longitudinal scan of the thoracolumbar area shows the myelomeningocele sac (short arrows) and disorganized neural tissue (long arrows) within it; SC, spinal cord. (C) Radiograph shows the interpedicular distances in the lumbar spine are widened and the laminae are splayed laterally (arrows). (D) Lateral transaxial scan in a different fetus shows the myelomeningocele sac (S) containing linear echoes representing neural tissue and the splayed laminae/pedicles complex (L, arrows).

Spinal dysraphism allows a leak of cerebrospinal fluid from the spinal canal into the amniotic fluid, which causes low intracranial pressure early in pregnancy. Low intracranial pressure induces a smaller-than-normal posterior fossa compartment. The cerebellum then grows into this abnormally small space, which leads to obliteration of the cisterna magna, compression

of the cerebellar hemispheres, herniation of the cerebellar tonsils into the cervical spinal canal, and related abnormalities such as ventriculomegaly. Ventriculomegaly is usually mild in the second trimester and worsens postpartum after repair of the spinal defect. Ventriculomegaly is seen in 44% to 86% of fetuses with spina bifida.71,72 The most common single cause of ventriculomegaly is

A

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FIG. 35.15  Skin-Covered Myelomeningocele.  (A) Endovaginal posterior transaxial scan shows a myelomeningocele sac covered by a thick wall (arrowheads). Echogenic material passes through the spina bifida defect into the myelomeningocele sac. Endocervical canal (arrows). (B) Endovaginal color Doppler posterior transaxial scan demonstrates a blood vessel protruding from the spinal canal into the myelomeningocele sac. (C) Endovaginal posterior longitudinal scan shows the myelomeningocele sac covered by a thick wall (arrowheads). (D) Neonatal picture shows the focal skin-covered lumbar myelomeningocele. The bluish tinge within the sac is a blood vessel detected by endovaginal color Doppler in B. (E) and (F) Longitudinal and posterior transaxial scans of a different fetus at 19 weeks’ gestational age demonstrate a small posterior cyst containing neural elements (calipers) covered by skin protruding through the splayed laminae. No intracranial abnormalities were demonstrated.

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FIG. 35.16  Lumbar Meningocele, 34 Weeks’ Gestation.  (A) Posterior transaxial sonogram demonstrates a fluid-filled sac (short arrows) along the fetal back. There is a small defect in the neural arch (long arrow). (B) Posterior longitudinal sonogram shows the wall of the meningocele (short arrows) and the focal spina bifida defect in the posterior neural arch (long arrow). (C) Posterior longitudinal and (D) posterior transaxial sonograms demonstrate abnormally posterior thoracic spinal cord (arrows) in the nondependent portion of the spinal canal. Cerebrospinal fluid (F) is between the anterior aspect of the spinal cord and the anterior wall of the spinal canal.

spina bifida, although only 30% to 40% of fetuses with enlarged ventricles actually have spina bifida. On ultrasound, the Chiari II malformation manifests as obliteration of the cisterna magna.73,74 The compression of the cerebellum changes its shape, giving the banana sign.71,75 In two different series, obliteration of the cisterna magna was noted in 22 of 23 cases with spina bifida

at 16 to 27 weeks’ gestation74 and in 18 of 20 cases at 24 weeks and earlier.74 Concave deformity of the fetal frontal bones in the second trimester is called the lemon sign.76 Various authors have shown that 85% of fetuses with spina bifida before 24 weeks’ gestation have the lemon sign.72,77-79 In practice, the lemon sign can be

CHAPTER 35  The Fetal Spine difficult to portray unequivocally. The lemon sign spontaneously resolves in the third trimester.78 In addition, it is seen in 1% of normal fetuses.77,78 The lemon sign should prompt detailed examination of the posterior fossa, to search for obliteration of the cisterna magna and for the banana sign, and the fetal spine, for direct evidence of spina bifida.

Associated Noncranial Abnormalities Foot deformities, primarily clubfoot, and dislocation of the hips are frequently associated with spina bifida.80 These abnormalities are caused by imbalanced muscular actions resulting from peripheral nerve involvement with the NTD. In fetuses with open spina bifida, 24% demonstrate additional morphologic abnormalities on second-trimester sonography, such as renal abnormalities, choroid plexus cysts, cardiac ventricular septal defect, omphalocele, and intrauterine growth restriction.58

Sonographic Signs of Spina Bifida Nonvisualization of cisterna magna Deformation of cerebellum (banana sign) Concave frontal bones (lemon sign) Dilation of the lateral ventricles Chiari II malformation (97%) Biparietal diameter lower than expected

Prognosis It is difficult to predict the long-term prognosis in a fetus with an identified myelomeningocele. However, the outcome is better for low lesions (lower lumbar or sacral), closed defects, and those with minimal or no hydrocephalus and no compression of the hindbrain from Chiari II malformation.55,66,75,81 In more than 880 patients82 of live deliveries with spina bifida, about 85% survived past age 10, and 2% died in the neonatal period. Of the survivors, about 50% had some type of learning disability. About 25% of survivors had an intelligence quotient (IQ) above 100, with about 75% above 80. About 33% of survivors developed symptoms and signs related to pressure on the hindbrain and brainstem (e.g., pain, weakness, and spasticity in arms), and some required cervical laminectomy to relieve the pressure. Wong and Paulozzi83 found 5-year survival rates of 82.7% for 1979-1983, 88.5% for 1984-1988, and 91.0% for 1989-1994. Determining prognosis for survival for current newborns is more difficult because of medical and surgical advances since studies describing patients born in the 1960s, 1970s, and 1980s.2 Beyond survival, multiple impairments may affect the individual, including motor dysfunction, bladder and bowel dysfunction, and intellectual impairment.2 Degree of muscle dysfunction is defined by the highest level of the open NTD, not by the number of involved vertebrae or the size of the overlying sac. When the lesion is thoracic, the legs are without muscle function, and when it is upper lumbar (L1-L2), useful leg function is minimal. When the upper level is L3-L5, the prognosis for longterm walking and the need for assistive devices are difficult to predict. Those with sacral defects will usually be able to walk well but with imperfect gait. Almost all people with spina bifida,

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including those with sacral defects, will have some degree of bowel and bladder dysfunction. It is very difficult to predict the ultimate level of intellectual functioning. In general, those who do not require ventricular shunting have much better outcomes for intellectual functioning. In those requiring shunts, the average IQ is approximately 80, which is low-normal range.84 The rate of profound intellectual impairment (IQ < 20) in those with shunts is 5%, usually related to medical complications such as shunt infections and Chiari II effects (e.g., apnea, hypoxia).

Fetal Surgery for Myelomeningocele The first fetal surgery for repair of myelomeningocele was performed in 1997. A formal clinical trial was performed from 2003 to 2010, with early termination of the study due to positive fetal results (decreased hindbrain herniation/need for shunt and improved spinal level of function). However, families and clinicians must evaluate the potential for improved function for the child against the risks of fetal/maternal surgical morbidity, most commonly preterm delivery and uterine dehiscence.85 Fetal myelomeningocele is a nonlethal entity; in utero surgery for repair of myelomeningocele is potentially lethal.86 Although myelomeningocele is a primary embryologic disorder, neurologic damage is also secondary to progressive in utero damage to the exposed spinal cord. The development of techniques to close open NTDs before birth has generated great interest and hope for fetal interventions and outcomes. Prior to the 2003 trial, preliminary observations from two centers suggested that improvements may occur not in spinal cord function as originally postulated87 but in the extent of the hindbrain herniation and the frequency that shunting is required to control hydrocephalus. In a report of 25 patients who underwent intrauterine myelomeningocele repair at Vanderbilt University, no improvement in leg function resulted from the surgery, but there was a substantially reduced incidence of moderate to severe hindbrain herniation (4% vs. 50%) and a moderate reduction in the incidence of shunt-dependent hydrocephalus (58% vs. 92%).88 The number of U.S. centers is limited to prevent the uncontrolled proliferation of new centers offering this complex multidisciplinary procedure.89 Prospective parents electing surgery90 should weigh the potential benefits against the potential risks.90-93

MYELOCYSTOCELE Myelocystocele is an uncommon form of spinal dysraphism. There is dilation of the central canal of the spinal cord. The central canal herniates posteriorly through the spinal cord and through the posterior neural arch to form an exterior sac. There may be no associated spina bifida lesion. The sac is composed of three layers, from inner to outer: the hydromyelia sac, which is lined by spinal canal ependyma; the meningeal layer, which is contiguous with the meninges around the spinal cord; and the skin. The fluid within the inner sac is continuous with the fluid of the central canal of the spinal cord; the fluid between the hydromyelia sac and the meningeal layer is continuous with the subarachnoid fluid.

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Myelocystocele may occur at any level of the spine and is often associated with Chiari II malformation.94-96 Prenatal and postnatal sonography demonstrates a “cyst within a cyst” appearance (Fig. 35.17). Splaying of the laminae and pedicles may or may not be present. The prognosis for a myelocystocele is worse than for a simple meningocele; infants with a simple meningocele may remain normal neurologically after surgical repair. The prognosis with myelocystocele is worse because there is usually some degree of associated myelodysplasia (i.e., dysplasia of spinal cord). Although neurologic function is normal in the immediate postoperative period, neurologic deficits often become apparent later in life. A terminal myelocystocele occurs at the spinal cord termination. The central canal of the spinal cord herniates with overlying

arachnoid and cerebrospinal fluid through a defect in posterior spinal elements and presents as a skin-covered mass along the posterior aspect of the lumbosacral area. There may be associated maldevelopment of the lower spine, pelvis, genitalia, bowel, bladder, kidneys, and abdominal wall. MRI provides the best imaging evaluation of the morphologic abnormalities after birth.97-99

DIASTEMATOMYELIA Diastematomyelia, also termed split-cord malformation, is a partial or complete sagittal cleft in the spinal cord, the distal conus of the cord, or filum terminale. Diastematomyelia is characterized by a sagittal osseous or fibrous septum in the spinal

C H C

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FIG. 35.17  Myelocystocele.  (A) Coronal sonogram of thoracic spine at 18 weeks’ gestation demonstrates a double-walled cystic mass (arrows) with inner cystic component (C) arising from the upper thoracic area. (B) Axial sonogram of the fetal chest 1 week later demonstrates a double-walled cystic mass (arrows) arising along the posterior aspect of the fetal chest; H, fetal heart. The inner cystic component (C) is slightly smaller and flattened compared to the first scan. No abnormality was noted in the ossified neural arch. (C) Sonogram of the specimen demonstrates the double-walled cystic mass (white arrows) arising from the posterior thorax with a hypoechoic tract (black arrows) extending from the posterior aspect of the spinal cord (curved arrow) toward the central cystic component (C) of the posterior mass. (D) CT scan of the specimen after injection of water-soluble contrast material into the cyst demonstrates contrast within the cyst (C) and within a sinus tract (short arrows), leading to the spinal cord (long arrow).

Continued

CHAPTER 35  The Fetal Spine

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S C

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FIG. 35.17, cont’d (E) Lateral view of the posterior cystic thoracic mass (C). (F) Sagittal magnetic resonance scan demonstrates the cystic mass along the upper thoracic area, with the small sinus tract (arrows) extending from the posterior aspect of the spinal cord (S) toward the cystic mass (C). (G) Gross pathologic specimen demonstrates the collapsed cyst (C) in contiguity with the cervical portion of the spinal cord (S). (H) Histologic section shows abnormal channel (arrows) communicating with the posterior aspect of the spinal cord (S), as well as defect in the posterior spinal cord (arrowheads) communicating with the central canal (CC) of the spinal cord. C, Central cystic component of posterior mass (M); E, ependymal lining of central cyst, which communicates with central canal of spinal cord; W, outer wall of cystic mass.

cord.100,101 This may be associated with a spina bifida defect and hydromyelia (dilation of central canal of spinal cord) but may occur in the absence of overt spina bifida.102 Diastematomyelia may also be associated with segmental anomalies of the vertebral bodies or visceral malformations such as horseshoe or ectopic kidney, utero-ovarian malformation, and anorectal malformation. If the spinal canal is traversed by a bony septum or spur, the septum will appear as an abnormal hyperechoic focus,103-105 which is best demonstrated in the posterior transaxial and lateral longitudinal scan planes (Fig. 35.18). When diastematomyelia is not associated with other spinal anomalies, the prognosis is favorable. In seven of eight cases reported by Has et al.,106 the defects had normal amniotic AFP and AChE levels and were considered isolated. Their review of the literature showed 26 cases diagnosed prenatally, 12 of which had no associated abnormality and had a favorable prognosis.

SCOLIOSIS AND KYPHOSIS Kyphosis is exaggerated curvature of the spine in the sagittal plane. Scoliosis is lateral curvature of the spine in the coronal

plane. Kyphosis and scoliosis may be positional and nonpathologic or permanent based on an underlying structural abnormality, such as hemivertebrae, butterfly vertebrae, and block vertebrae. Pathologic kyphosis and scoliosis are often associated with spina bifida or ventral abdominal wall defects.107 Less common associations include limb–body wall complex, amniotic band syndrome, arthrogryposis, skeletal dysplasias, VACTERL association (vertebral abnormalities, anal atresia, cardiac abnormalities, tracheoesophageal fistula, renal agenesis, and limb defects),108,109 and caudal regression syndrome. Mild scoliosis may be caused by a hemivertebra (Fig. 35.19).106,109 The posterior longitudinal scan is the best view to assess for kyphosis; the lateral longitudinal plane is the best to assess for scoliosis (Fig. 35.19). Because oligohydramnios can cause positional curvature in the fetal spine, a confident diagnosis of pathologic kyphosis or scoliosis should be made only if the curvature is severe. Possible associated anomalies must then be sought because prognosis depends on the coexistent anomalies. A hemivertebra represents underdevelopment or nondevelopment of one-half of a vertebral body; that is, one of the two early

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Obstetric and Fetal Sonography

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FIG. 35.18  Diastematomyelia.  (A) Coronal and (B) axial sonograms of the spine demonstrate two hyperechoic foci (arrows) caused by the bony septum within the spinal canal with intact skin along the fetal back. (C) Anteroposterior radiograph and (D) CT scan demonstrate a bony septum (arrows) within the central portion of the spinal canal. (E) Diplomyelia and tethered cord. Posterior transaxial sonogram of another fetus shows cord in the nondependent portion of the spinal canal with fluid (F) interposed between the cord and anterior margin of the spinal canal. The anterior aspect of the cord has a bilobed shape instead of a smooth, circular arc with bilateral central canal echoes (arrows).

A

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FIG. 35.19  Kyphosis.  (A) Sagittal scan of the spine demonstrates a focal kyphosis at the thoracolumbar junction. (B) Three-dimensional image of the same patient demonstrates a left upper lumbar hemivertebra as the cause of the kyphosis.

CHAPTER 35  The Fetal Spine chondrification centers is deficient. The remaining ossification center is displaced laterally with respect to the vertebrae above and below it, leading to a short-segment mild scoliosis. The abnormalities can be detected prenatally and may be best portrayed with 3D ultrasound.31-34 Fetuses with an isolated

hemivertebra have an excellent prognosis, whereas those with other fetal anomalies (e.g., Potter syndrome; cardiac, intestinal, intracranial, and limb anomalies) have a poor prognosis.110 The presence of associated anomalies reduces the survival rate to approximately 50%. If oligohydramnios is also present, the mortality rate approaches 100%.111

Causes of Scoliosis or Kyphosis Hemivertebrae Butterfly vertebrae Block vertebrae Spina bifida Ventral abdominal wall defects Limb–body wall complex Amniotic band syndrome Arthrogryposis Skeletal dysplasias VACTERLa association Caudal regression syndrome a

Vertebral abnormalities, anal atresia, cardiac abnormalities, tracheoesophageal fistula, renal agenesis, and limb defects.

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SACRAL AGENESIS Sacral agenesis is an uncommon fetal abnormality that may be present in conditions such as caudal regression sequence, sirenomelia sequence, cloacal exstrophy sequence, and the VACTERL association. The caudal regression sequence (caudal regression syndrome) and the sirenomelia sequence are thought to be separate pathologic entities.112,113

CAUDAL REGRESSION In caudal regression or dysplasia, abnormalities of the lower spine and limbs occur, including sacral agenesis, lumbar spine deficiency, and leg anomalies such as femoral hypoplasia (Fig. 35.20). Defects of the neural tube and the genitourinary,

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FIG. 35.20  Caudal Regression.  (A) Sagittal sonogram of spine at 21 weeks shows abrupt termination of ossified vertebral bodies. (B) Transverse view of pelvis with legs in long axis shows lack of ossified pelvic bones and atrophic musculature about the lower extremities. (C) Transverse color Doppler image at level of bladder shows lack of ossified pelvic bones. (D) In a different fetal specimen, radiograph shows abrupt termination (arrows) of the lumbar spine and absence of the sacrum. The pelvic bones are small and deformed.

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FIG. 35.21  Sirenomelia.  (A) Sagittal view of fetus at 12 weeks’ gestation shows unusual angulation of lower extremity. (B) Long-axis view of a single lower extremity. (C) In a different fetus, radiograph shows single femur (F) and single tibia (T). Note the segmented defects in the vertebrae of the thoracic and lumbar spine (arrows).

gastrointestinal, and cardiac systems are common. Occurrence is sporadic; caudal regression is more common in infants of mothers with diabetes mellitus. The cause has not been established. Sonography can demonstrate absence of the sacrum and shortened femurs. The legs can be flexed and abducted at the hips, and there may be clubfoot. Sonography may detect associated urinary anomalies (renal agenesis, cystic dysplasia, caliectasis) and gastrointestinal abnormalities (e.g., duodenal atresia).114 The prognosis depends on the severity and extent of the skeletal abnormalities and associated anomalies. In sacral agenesis with no internal organ involvement, there are usually deficits in the legs and deficient control of bladder and bowel functions. In infants with internal organ involvement, the prognosis is related to these defects.

SIRENOMELIA Sirenomelia sequence is a rare disorder in which the legs are fused and the feet are deformed or absent115 (Fig. 35.21). The cause is probably an aberrant fetal artery that branches from the upper abdominal aorta and passes into the umbilical cord to the placenta.116 Arterial blood flow bypasses the lower fetal body. The distal abdominal aorta, the aorta’s distal branches, and subtended structures are small and underdeveloped. This leads to malformations of spine, legs, kidneys, gut, and genitalia. Normally the umbilical arteries, which arise from the fetal iliac arteries, carry blood from the fetus into the umbilical cord and then into the placenta. At sonography, there is advanced oligohydramnios because of reduced or absent renal function. The legs are fused, or there is a single leg. The feet are absent, or there may be a single foot. There may be sacral agenesis, deficiency of the lower lumbar spine, and thoracic anomalies. These findings may be difficult to appreciate because of the advanced oligohydramnios or anhydramnios.112 The prolonged anhydramnios causes pulmonary hypoplasia, which is usually fatal. The risk of recurrence is the same as in the general population.

SACROCOCCYGEAL TERATOMA Fetal teratomas may arise from the sacrum or coccyx, from other midline structures from the level of the brain to the coccyx, or from the gonads.117 Sacrococcygeal teratomas arise from the pluripotent cells of Hensen node located anterior to the coccyx. Sacrococcygeal teratomas contain all three germ layers (ectoderm, mesoderm, and endoderm) and thus may contain elements of many tissues, including neural, respiratory, and gastrointestinal. Sacrococcygeal tumor is rare (1 : 35,000 births)118 but is the most common tumor among neonates. Females are affected four times more frequently than males. Sacrococcygeal teratomas are classified into four types118: type I, tumor predominantly external with only minimal presacral involvement; type II, tumor presenting externally but with significant intrapelvic extension; type III, tumor apparent externally but with predominant pelvic mass and extension into the abdomen; type IV, tumor presacral with no external presentation (Fig. 35.22).117

Types of Sacrococcygeal Teratomas Type I (47%): external mass predominant Type II (34%): external mass with significant internal component Type III (9%): internal mass predominant, with smaller external component Type IV (10%): presacral mass only

At birth, 75% of sacrococcygeal teratomas are benign, 12% are immature, and 13% are malignant. Because malignant potential increases with the age of the infant, surgery must be performed shortly after birth. Sonography usually demonstrates a mass in the rump or buttocks area adjacent to the spine119 (Video 35.6). Most teratomas (85%) are either solid or mixed (solid and cystic); 15% are mostly cystic, which is a benign sign. Calcifications are frequently present.

CHAPTER 35  The Fetal Spine

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FIG. 35.22  Sacrococcygeal Teratoma.  (A) Sagittal sonogram shows type II sacrococcygeal teratoma (SCT) that is predominantly external but has a substantial intrapelvic component. The tumor extends up to level L5 and displaces the fetal urinary bladder (B) anteriorly. Note the calcifications (arrows) within the tumor. (B) T2-weighted sagittal magnetic resonance image demonstrates the extent and internal structure of the sacrococcygeal tumor (SCT); S, stomach. (C) Lateral radiograph in a different neonate. (A and B courtesy of Drs. Fong, Pantazi, and Toi, Mt. Sinai Hospital, Toronto.)

Large masses may displace and distort neighboring structures, such as the rectum and urinary bladder (see Fig. 35.22). Compression of the distal ureters may cause hydronephrosis. Larger solid tumors may develop substantial arteriovenous shunting, causing fetal cardiac failure and hydrops.120 The development of hydrops in the presence of a sacrococcygeal teratoma carries a poor prognosis.120-124

PRESACRAL FETAL MASS The differential diagnosis of a presacral fetal mass also includes chordoma, anterior myelomeningocele, neurenteric cyst, neuroblastoma, sarcoma, lipoma, bone tumor, lymphoma, and rectal duplication. Amniotic fluid AFP is often elevated in sacrococcygeal tumor, and AChE is often present in the amniotic fluid. These results exclude most other causes, except a myelomeningocele.

Presacral Masses Sacrococcygeal teratoma Chordoma Anterior myelomeningocele Neurenteric cyst Neuroblastoma Sarcoma Lipoma Bone tumor Lymphoma Rectal duplication

If a fetal sacrococcygeal teratoma is suspected from prenatal sonograms, serial sonograms should be arranged to monitor the pregnancy to assess for complications, especially signs of fetal cardiac failure. Complete fetal assessment should also include the internal characteristics of the tumor, the size of the tumor, and associated fetal anomalies. For masses less than 4.5 cm in diameter, without associated abnormalities, vaginal delivery is considered. For masses greater

than 4.5 cm diameter, cesarean section may be considered because of the risk of dystocia and hemorrhage during vaginal delivery. In utero surgery for arteriovenous shunting has been described for treatment of fetal hydrops from congestive heart failure in early pregnancy ( 20% LHR, Lung-to-head ratio; LiTR, liver to fetal thoracic volume ratio; MRI, magnetic resonance imaging; o/e, observed-to-expected; PPLV, percent predicted lung volume; TFLV, total fetal lung volume.

Prenatal pulmonary artery measurements at the hila at the level of the four-chamber view have been performed.211-214 Measuring the main right and left pulmonary artery and comparing with normals via an observed-to-expected ratio shows a reduction in values in fetuses with CDH and pulmonary hypoplasia. Doppler wave forms have been useful in defining the most severe CDH cases. Increased pulmonary artery pulsatility index (>1) and peak early diastolic reversed flow in the main pulmonary artery (>3.5) reflect high resistance in pulmonary vascular bed with preferential flow through the ductus arteriosus and are correlated with poor lung growth.215,216 Other tests utilized in CDH include a hyperoxygenation test for pulmonary vascular reactivity at 31 to 36 weeks’ gestation, in which reactivity (20% reduction in pulmonary artery pretest pulsatility index) suggests a good outcome,217,218 and assessment of fractional moving blood volume because a decrease in this fraction is correlated with decreased lung growth and an increased intrapulmonary artery impedance in CDH.219-223 Patients with fetuses with CDH generally undergo extensive prenatal imaging and counseling. Follow-up ultrasound examinations should be performed to assess fetal well-being, amniotic fluid levels, lung volume, and changes in mediastinal shift that could result in hemodynamic changes.

Other Hernias and Eventration In bilateral hernias the falciform ligament is drawn into the hernia.224,225 Mediastinal shift is variable, but typically the heart is displaced anteriorly and superiorly. Features of both right- and left-sided CDH are present. Pericardial hernias result from failure of the retrosternal portion of the septum transversum to close the communication between the pericardial and peritoneal cavities.226 The liver may herniate into the pericardial sac.171,225 Pericardial effusion results from mass effect on the heart and obstruction of venous return or from mechanical irritation of membranes.227 Because the differential diagnosis of a pericardial mass includes pericardial tumors such as teratoma, it is important to recognize the liver as part of the hernial sac contents by identifying the hepatic vessels in the mass.219,228 In diaphragmatic eventration the intact diaphragm is displaced cephalad at the weakened muscular portion, without communication between the abdominal and thoracic cavities229 (Fig. 36.15). Diaphragmatic eventration is associated with a lower

CHAPTER 36  The Fetal Chest

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perinatal mortality rate compared to CDH and may not require surgical repair. Thus it is crucial to make the distinction between the two diagnoses to provide appropriate counseling.

Associated Anomalies CDH may be an isolated defect or may be associated with other structural, chromosomal, or syndromal anomalies. Associated anomalies are present in 25% to 55% of cases. Congenital heart disease is the most common association (20%), with hemodynamically significant heart disease in 11% of cases.230-232 Because of the high rate of associated cardiac abnormalities, formal fetal echocardiography is indicated in fetuses with CDH.

B

FIG. 36.15  Eventration of the Hemidiaphragm.  (A) Transverse view of the thorax demonstrates the stomach in the thorax with mild mediastinal shift. (B) Coronal and (C) sagittal T2-weighted MRI shows the high position of stomach with intact diaphragm.

Associated central nervous system anomalies are second in frequency of associated structural abnormalities in fetuses with CDH; these anomalies include anencephaly, ventriculomegaly, and neural tube defects.191 Chromosomal abnormalities occur in 10% to 20% of antenatally detected CDH, the most common being trisomy 18.192,193 Chromosomal abnormalities are most common when CDH is present in association with other structural abnormalities. Given the high association with aneuploidy, chromosomal assessment is typically performed. Associated syndromes include Fryn, Beckwith-Wiedemann, Simpson-Golabi-Behmel, Brachmann–de Lange, and Perlman.195

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TABLE 36.5  Sample Studies of Predictors of Survival in Left-Sided Congenital Diaphragmatic Hernia Imaging Findings

Sign/ Value

Liver position208

Liver up Liver down 1

1.5 MoM)

MCV of parents to check for thalassemia ( 1.5 MoM or hydropic), unless the pregnancy is at a gestational age when risks associated with delivery are considered to be less than those associated with the procedure.203 If it is anticipated that the fetus may require transfusion (e.g., parvovirus infection with elevated MCA Doppler velocity), it is prudent to have crossmatched blood and platelets ready to avoid the risks with a second procedure. PUBS is usually performed in a setting that allows maternal sedation and intervention for fetal distress after 24 weeks, most often an operating room for labor and delivery. The patient is prepped and sterilely draped and the uterus displaced slightly to the left with appropriate maternal wedging. The ultrasound transducer is draped with a sterile sheath to allow guidance on the sterile field. The patient is often given conscious sedation for comfort and to minimize maternal movement during the procedure. Local anesthetic with lidocaine may be used for patient comfort. Ultrasound guidance may be provided by a second

C

F P

FIG. 41.28  Cordocentesis.  Transverse ultrasound image shows needle (arrows) traversing placenta (P) and entering placental cord insertion. Note loop of umbilical cord (C) and fetus (F).

provider or by the operator using a freehand technique. A 20- to 22-gauge needle is typically used, and most often the umbilical vein is targeted at the placental cord insertion (Fig. 41.28). Other approaches include the umbilical vein at the fetal cord insertion or a free loop of cord. The needle position is confirmed by obtaining a blood specimen, ultrasound observation of the needle in the vein, and sonographic streaming within the umbilical vein after injection of saline. Heparinized syringes are used for fetal blood sampling, and values for hemoglobin/hematocrit, platelets, and mean corpuscular volume (MCV) are obtained. The fetal MCV (which should be >100 µm3) is higher than the maternal value and can help confirm fetal origin of the blood sample. Depending on the insertion site and indication for cordocentesis, fetal paralysis can be considered with vecuronium (0.1 mg/kg estimated fetal weight)204 or atracurium besylate (0.4 mg/kg estimated fetal weight).205 Fetal cardiac activity is documented throughout the procedure. The fetal hematocrit is checked to determine the amount of transfusion needed (Hct < 30% is 2.5th centile >20 weeks). To limit the amount of fluid being transfused into the relatively small circulatory capacity of the fetus, packed RBCs (type O negative; Hct > 90%) are given. The goal is to transfuse to Hct of 40 mL/dL. Successful treatment of anemia with intravascular blood transfusion has been reported as early as 13 weeks’ gestation.145 When performing PUBS it is important to have a team involved that includes genetic counselors (regarding the underlying cause of anemia), laboratory medicine professionals (to check the MCV and have packed RBCs available), and maternal fetal medicine specialists as well as individuals familiar with guidance for procedures with ultrasound. When PUBS is not possible, particularly at early gestational age when the umbilical cord is small and difficult to safely

CHAPTER 41  Fetal Hydrops

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sampling or amniocentesis (Fig. 41.30). This can be both diagnostic (e.g., lymphocyte count in chylothorax or for rapid karyotype) and occasionally therapeutic. Simultaneous sampling does not increase the overall procedure risk.

Postnatal Investigations After birth, the placenta should be sent for pathologic analysis, and a skeletal survey may be helpful. A geneticist may see the neonate to provide additional input. In cases of death, detailed autopsy and placental examination, correlated with antenatal findings, is the best way to determine the cause of nonimmune hydrops.210,211 Further investigations may be prompted by additional physical findings at autopsy.212 If a metabolic condition is suspected as the cause of hydrops, inclusion bodies can be sought on microscopy. In some series the cause of hydrops was identified in only 40% to 50% of patients without autopsy,135 versus 80% to 90% after postmortem examination.210,213

FIG. 41.29  Fetal Blood Sampling in Intrahepatic Portion of Umbilical Vein.  Arrows point to the position of the 20-gauge needle in the intrahepatic portion of the umbilical vein.

instrument, intraperitoneal, intrahepatic (Fig. 41.29), or intracardiac transfusion can be performed.206

Fetal Transfusion If fetal transfusion is required, T-connector tubing is often employed for ease of transfusion. The volume to be transfused can be calculated by using the following formula207: Volume transfused (mL) = Volume fetoplacental unit (mL)  Hematocrit final − Hematocrit initial  ×  Hematocrit transfused blood  The fetoplacental volume can be estimated as 1.046 + fetal weight in grams × 0.14.207 Either maternal cells or donated O-negative, washed, leukocyte-reduced blood is used for transfusion. Maternal cells may be consumed less rapidly than anonymous donation, but timing and pregnancy-associated anemia limit its use.208 A posttransfusion sample is obtained to evaluate the effects of the procedure. Future transfusions are scheduled based on fetal Doppler assessment26 or by estimating a 0.7% decrease in the hematocrit per day and scheduling transfusion for estimated hematocrits of 20 to 22 mL/dL.209 If the cordocentesis or transfusion is being performed for reasons other than Rh(D) isoimmunization, in a Rh(D)-negative mother, RhoGAM should be administered after the procedure.

Cavity Aspiration The clinician can usually advance the needle easily into the fetal chest, abdomen, or amniotic fluid at the time of fetal blood

FETAL WELFARE ASSESSMENT IN NONIMMUNE HYDROPS Noninvasive ultrasound techniques for fetal well-being assessment in pregnancies complicated by nonimmune hydrops include biophysical assessment, pulsed Doppler velocimetry of umbilical and regional fetal vessels, and functional cardiac assessment. Fetal Doppler evaluation may give some indication of anemia, cardiac failure, and well-being.25 Umbilical vein and intrahepatic vein pulsations, or ductus venosus a-wave reversal, represent cardiac diastolic dysfunction and have been correlated with poor perinatal outcomes.214

OBSTETRIC PROGNOSIS The overall mortality rate among fetuses with nonimmune hydrops is approximately 70%,31 with mortality in cases of structural abnormalities not amenable to therapy as high as 100%. In a series of 100 cases of nonimmune hydrops, 74 were thought to have a nontreatable cause, and none of these resulted in a live birth; of 26 with a treatable cause, 18 resulted in a live birth and were alive at 1 year of age.31 Gestational age at diagnosis of hydrops has been used to predict outcome. A 10-year review of 82 cases presenting after 20 weeks135 reported an overall mortality rate of 87%, and those diagnosed after 24 weeks were more likely to be idiopathic or related to cardiothoracic abnormalities. Spontaneous resolution of hydrops has been reported in fetuses with normal chromosomes diagnosed before 24 weeks. Although the overall prognosis for fetal hydrops has improved in recent years, most series are small with a mixture of causes and thus are difficult to compare. Some improvement in outcome over earlier reports is attributable to the growing number of cases that are amenable to in utero therapy. Unfortunately, many cases still represent a terminal process. Earlier identification and referral, thorough evaluation, and fetal therapy in appropriate cases are the cornerstone to further improvements in prognosis. Obtaining the best diagnosis is helpful in counseling about recurrence risks.

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A

C

Maternal Complications (Mirror Syndrome) Maternal complications may occur in association with fetal hydrops. Hypoproteinemia, edema, weight gain, hypertension, oliguria, and preeclampsia may develop.215 This association has been termed mirror syndrome because edema in the pregnant patient mirrors that of the hydropic fetus.34,216,217 The syndrome has been described in conjunction with hydrops of various causes.215,218,219 Perinatal mortality and morbidity rates are high. Maternal outcome can be improved by delivery of the fetus and placenta or by fetal intervention to treat the cause of the hydrops.217,220-222 If hydrops cannot be cured, delivery may limit the risk of maternal complications.35,222 Espinoza et al.223 recently suggested the high plasma concentrations of soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) is implicated in the pathophysiology of mirror syndrome. Hypoxia of the villous trophoblast in cases of villous edema leads to increased production and release of sVEGFR-1

B

FIG. 41.30  Drainage of Ascites in Fetus at 26 Weeks With Lymphatic Duct Dysplasia.  (A) Transverse view of fetal abdomen shows ascites with omentum (arrows) outlined by ascitic fluid. (B) and (C) Images during draining procedure show the needle in the amniotic fluid (B) and ascitic fluid (C).

and other antiangiogenic factors into the maternal circulation. Excessive concentrations of these products may be responsible for maternal edema in mirror syndrome.

Delivery Mode and location of delivery are based on obstetric factors, taking into account the underlying prognosis.224 Uterine overdistention in severe polyhydramnios carries the risks of placental abruption and cord prolapse after membrane rupture and postpartum hemorrhage from uterine atony. Prematurity secondary to polyhydramnios is a major contributing factor to the poor outcome of some neonates. Therapeutic amniocentesis before induction of labor may be considered in cases with massive polyhydramnios to decrease the risk of malpresentation or cord prolapse. Indomethacin has also been used to decrease the amniotic fluid volume.225 This drug should be used with caution after 32 weeks’ gestation because of the potential for ductal constriction.

CHAPTER 41  Fetal Hydrops

Predelivery Aspiration Procedures Fetal fluid collections may be drained under ultrasound guidance just before delivery to assist with neonatal resuscitation. This is particularly relevant if large fetal pleural effusions are present.115 Massive ascites may also be drained to prevent abdominal dystocia (when vaginal birth is planned) and aid in fetal breathing when ascites has caused elevation of the diaphragms.

Postnatal Outcome Because of the high incidence of in utero demise, the cause of hydrops in utero is different from that with a live neonate. In a review of 30 cases of hydrops diagnosed between 10 and 14 weeks of pregnancy, all pregnancies with nonimmune hydrops resulted in abortion, intrauterine fetal death, or pregnancy termination.136 A 2007 national database review of live-born neonates with hydrops found heart problems (13.7%), abnormalities in heart rate (10.4%), TTTS (9%), congenital anomalies (8.7%), chromosomal abnormalities (7.5%), congenital viral infections (6.7%), isoimmunization (4.5%), and congenital chylothorax (3.2%).226 Mortality rates were highest among neonates with congenital anomalies (57.7%) and lowest among those with congenital chylothorax (5.9%), and a cause could not be determined in 26%. Factors associated independently with death were younger gestational age, low 5-minute Apgar score, and high levels of support needed the first day after birth.226 This study reported a 36% death rate before discharge or transfer to another hospital. The severity of hydrops and birth gestational age of the infant are the key determinants for survival. This is important because delivering a fetus early to treat worsening hydrops may not improve survival. Data are limited regarding long-term outcome of children surviving after hydrops. In one series, 13 in 19 (68%) children surviving beyond 1 year of age were normal; two had mild developmental delay at 1 year of age; one 8-year-old child was mentally retarded; and three (16%) had severe psychomotor impairment with marked growth failure.227 Haverkamp et al.228 found that 86% of patients had normal psychomotor development, 86% showed normal neurologic status, 7% had minor neurologic dysfunction, and 4% had spastic cerebral paresis.

CONCLUSION Hydrops represents a terminal stage for many conditions, the vast majority of which are fetal in origin. The onset of hydrops signifies fetal decompensation. Immune causes can be successfully treated in utero, as can an increasing number of nonimmune causes. Whereas in the past, nonimmune hydrops carried virtually 100% mortality, this is no longer the case. A team approach using obstetric imagers, maternal fetal medicine specialists, neonatologists, and geneticists can help to decide which cases are suitable for therapeutic intervention. A comprehensive approach must be taken to the investigation of hydrops, both for the management of the index case and for future counseling. Cornerstones of this investigation are detailed ultrasound, including echocardiography, fetal karyotyping, and other

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98. Peranteau WH, Wilson RD, Liechty KW, et al. Effect of maternal betamethasone administration on prenatal congenital cystic adenomatoid malformation growth and fetal survival. Fetal Diagn Ther. 2007;22(5): 365-371. 99. Adzick NS. Management of fetal lung lesions. Clin Perinatol. 2003;30(3): 481-492. 100. Dolkart LA, Reimers FT, Helmuth WV, et al. Antenatal diagnosis of pulmonary sequestration: a review. Obstet Gynecol Surv. 1992;47(8): 515-520. 101. da Silva OP, Ramanan R, Romano W, et al. Nonimmune hydrops fetalis, pulmonary sequestration, and favorable neonatal outcome. Obstet Gynecol. 1996;88(4 Pt 2):681-683. 102. Slotnick RN, McGahan J, Milio L, et al. Antenatal diagnosis and treatment of fetal bronchopulmonary sequestration. Fetal Diagn Ther. 1990;5(1): 33-39. 103. Salomon LJ, Audibert F, Dommergues M, et al. Fetal thoracoamniotic shunting as the only treatment for pulmonary sequestration with hydrops: favorable long-term outcome without postnatal surgery. Ultrasound Obstet Gynecol. 2003;21(3):299-301. 104. Becmeur F, Horta-Geraud P, Donato L, Sauvage P. Pulmonary sequestrations: prenatal ultrasound diagnosis, treatment, and outcome. J Pediatr Surg. 1998;33(3):492-496. 105. Chan V, Greenough A, Nicolaides KN. Antenatal and postnatal treatment of pleural effusion and extra-lobar pulmonary sequestration. J Perinat Med. 1996;24(4):335-338. 106. Anandakumar C, Biswas A, Chua TM, et al. Direct intrauterine fetal therapy in a case of bronchopulmonary sequestration associated with non-immune hydrops fetalis. Ultrasound Obstet Gynecol. 1999;13(4): 263-265. 107. Nicolini U, Cerri V, Groli C, et al. A new approach to prenatal treatment of extralobar pulmonary sequestration. Prenat Diagn. 2000;20(9):758760. 108. Ruano R, de A Pimenta EJ, Marques da Silva M, et al. Percutaneous intrauterine laser ablation of the abnormal vessel in pulmonary sequestration with hydrops at 29 weeks’ gestation. J Ultrasound Med. 2007;26(9):12351241. 109. Oepkes D, Devlieger R, Lopriore E, Klumper FJ. Successful ultrasound-guided laser treatment of fetal hydrops caused by pulmonary sequestration. Ultrasound Obstet Gynecol. 2007;29(4):457-459. 110. Kalache KD, Chaoui R, Tennstedt C, Bollmann R. Prenatal diagnosis of laryngeal atresia in two cases of congenital high airway obstruction syndrome (CHAOS). Prenat Diagn. 1997;17(6):577-581. 111. Achiron R, Weissman A, Lipitz S, et al. Fetal pleural effusion: the risk of fetal trisomy. Gynecol Obstet Invest. 1995;39(3):153-156. 112. Eddleman KA, Levine AB, Chitkara U, Berkowitz RL. Reliability of pleural fluid lymphocyte counts in the antenatal diagnosis of congenital chylothorax. Obstet Gynecol. 1991;78(3 Pt 2):530-532. 113. Rodeck CH, Fisk NM, Fraser DI, Nicolini U. Long-term in utero drainage of fetal hydrothorax. N Engl J Med. 1988;319(17):1135-1138. 114. Deurloo KL, Devlieger R, Lopriore E, et al. Isolated fetal hydrothorax with hydrops: a systematic review of prenatal treatment options. Prenat Diagn. 2007;27(10):893-899. 115. Cardwell MS. Aspiration of fetal pleural effusions or ascites may improve neonatal resuscitation. South Med J. 1996;89(2):177-178. 116. Mayock DE, Hickok DE, Guthrie RD. Cystic meconium peritonitis associated with hydrops fetalis. Am J Obstet Gynecol. 1982;142(6 Pt 1):704-705. 117. Mark K, Reis A, Zenker M. Prenatal findings in four consecutive pregnancies with fetal Pierson syndrome, a newly defined congenital nephrosis syndrome. Prenat Diagn. 2006;26(3):262-266. 118. Bellini C, Hennekam RC, Boccardo F, et al. Nonimmune idiopathic hydrops fetalis and congenital lymphatic dysplasia. Am J Med Genet A. 2006;140(7): 678-684. 119. Quintero RA, Morales WJ, Allen MH, et al. Staging of twin-twin transfusion syndrome. J Perinatol. 1999;19(8 Pt 1):550-555. 120. Huhta JC. Right ventricular function in the human fetus. J Perinat Med. 2001;29(5):381-389. 121. Berghella V, Kaufmann M. Natural history of twin-twin transfusion syndrome. J Reprod Med. 2001;46(5):480-484.

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122. Senat MV, Deprest J, Boulvain M, et al. Endoscopic laser surgery versus serial amnioreduction for severe twin-to-twin transfusion syndrome. N Engl J Med. 2004;351(2):136-144. 123. Quintero RA, Dickinson JE, Morales WJ, et al. Stage-based treatment of twin-twin transfusion syndrome. Am J Obstet Gynecol. 2003;188(5): 1333-1340. 124. Gebb J, Dar P, Rosner M, Evans MI. Long-term neurologic outcomes after common fetal interventions. Am J Obstet Gynecol. 2015;212(4):527.e1-527. e9. 125. Moore T, Gale S, Benirschke K. Perinatal outcome of forty-nine pregnancies complicated by acardiac twinning. Am J Obstet Gynecol. 1990;163(3): 907-912. 126. Quintero RA, Reich H, Puder KS, et al. Brief report: umbilical-cord ligation of an acardiac twin by fetoscopy at 19 weeks of gestation. N Engl J Med. 1994;330(7):469-471. 127. Peeters S, Devlieger R, Middeldorp J, et al. Fetal surgery in complicated monoamniotic pregnancies: case series and systematic review of the literature. Prenat Diagn. 2014;34(6):586-591. 128. Tan TYT, Sepulveda W. Acardiac twin: a systematic review of minimally invasive treatment modalities. Ultrasound Obstet Gynecol. 2003;22(4): 409-419. 129. Hirose M, Murata A, Kita N, et al. Successful intrauterine treatment with radiofrequency ablation in a case of acardiac twin pregnancy complicated with a hydropic pump twin. Ultrasound Obstet Gynecol. 2004;23(5): 509-512. 130. Tsao K, Feldstein VA, Albanese CT, et al. Selective reduction of acardiac twin by radiofrequency ablation. Am J Obstet Gynecol. 2002;187(3): 635-640. 131. Ville Y, Hyett JA, Vandenbussche FP, Nicolaides KH. Endoscopic laser coagulation of umbilical cord vessels in twin reversed arterial perfusion sequence. Ultrasound Obstet Gynecol. 1994;4(5):396-398. 132. Rodeck C, Deans A, Jauniaux E. Thermocoagulation for the early treatment of pregnancy with an acardiac twin. N Engl J Med. 1998;339(18): 1293-1295. 133. Lee H, Bebbington M, Crombleholme TM. North American Fetal Therapy Network. The North American Fetal Therapy Network Registry data on outcomes of radiofrequency ablation for twin-reversed arterial perfusion sequence. Fetal Diagn Ther. 2013;33(4):224-229. 134. Iskaros J, Jauniaux E, Rodeck C. Outcome of nonimmune hydrops fetalis diagnosed during the first half of pregnancy. Obstet Gynecol. 1997;90(3): 321-325. 135. McCoy MC, Katz VL, Gould N, Kuller JA. Non-immune hydrops after 20 weeks’ gestation: review of 10 years’ experience with suggestions for management. Obstet Gynecol. 1995;85(4):578-582. 136. Has R. Non-immune hydrops fetalis in the first trimester: a review of 30 cases. Clin Exp Obstet Gynecol. 2001;28(3):187-190. 137. Hojo S, Tsukimori K, Kitade S, et al. Prenatal sonographic findings and hematological abnormalities in fetuses with transient abnormal myelopoiesis with Down syndrome. Prenat Diagn. 2007;27(6):507-511. 138. Zerres K, Schwanitz G, Niesen M, et al. Prenatal diagnosis of acute nonlymphoblastic leukaemia in Down syndrome. Lancet. 1990;335(8681):117. 139. Hyett JA, Perdu M, Sharland GK, et al. Increased nuchal translucency at 10-14 weeks of gestation as a marker for major cardiac defects. Ultrasound Obstet Gynecol. 1997;10(4):242-246. 140. Jenderny J, Schmidt W, Hecher K, et al. Increased nuchal translucency, hydrops fetalis or hygroma colli. A new test strategy for early fetal aneuploidy detection. Fetal Diagn Ther. 2001;16(4):211-214. 141. Hedrick HL, Flake AW, Crombleholme TM, et al. Sacrococcygeal teratoma: prenatal assessment, fetal intervention, and outcome. J Pediatr Surg. 2004;39(3):430-438. 142. Sananes N, Javadian P, Britto IS, et al. Technical aspects and effectiveness of percutaneous fetal therapies for large sacrococcygeal teratomas—a cohort study and a literature review. Ultrasound Obstet Gynecol. 2015. 143. Van Mieghem T, Al-Ibrahim A, Deprest J, et al. Minimally invasive therapy for fetal sacrococcygeal teratoma: case series and systematic review of the literature. Ultrasound Obstet Gynecol. 2014;43(6):611-619. 144. Dame C, Albers N, Hasan C, et al. Homozygous alpha-thalassaemia and hypospadias—common aetiology or incidental association? Long-term

survival of Hb Bart’s hydrops syndrome leads to new aspects for counselling of alpha-thalassaemic traits. Eur J Pediatr. 1999;158(3):217-220. 145. Kempe A, Rosing B, Berg C, et al. First-trimester treatment of fetal anemia secondary to parvovirus B19 infection. Ultrasound Obstet Gynecol. 2007; 29(2):226-228. 146. Perkins RP. Hydrops fetalis and stillbirth in a male glucose-6-phosphate dehydrogenase-deficient fetus possibly due to maternal ingestion of sulfisoxazole; a case report. Am J Obstet Gynecol. 1971;111(3):379-381. 147. Lallemand AV, Doco-Fenzy M, Gaillard DA. Investigation of nonimmune hydrops fetalis: multidisciplinary studies are necessary for diagnosis—review of 94 cases. Pediatr Dev Pathol. 1999;2(5):432-439. 148. Rodriguez MM, Chaves F, Romaguera RL, et al. Value of autopsy in nonimmune hydrops fetalis: series of 51 stillborn fetuses. Pediatr Dev Pathol. 2002;5(4):365-374. 149. Barron SD, Pass RF. Infectious causes of hydrops fetalis. Semin Perinatol. 1995;19(6):493-501. 150. Porter HJ, Quantrill AM, Fleming KA. B19 parvovirus infection of myocardial cells. Lancet. 1988;1(8584):535-536. 151. Naides SJ, Weiner CP. Antenatal diagnosis and palliative treatment of non-immune hydrops fetalis secondary to fetal parvovirus B19 infection. Prenat Diagn. 1989;9(2):105-114. 152. Morey AL, Keeling JW, Porter HJ, Fleming KA. Clinical and histopathological features of parvovirus B19 infection in the human fetus. Br J Obstet Gynaecol. 1992;99(7):566-574. 153. Oyer CE, Ongcapin EH, Ni J, et al. Fatal intrauterine adenoviral endomyocarditis with aortic and pulmonary valve stenosis: diagnosis by polymerase chain reaction. Hum Pathol. 2000;31(11):1433-1435. 154. Bates Jr HR. Coxsackie virus B3 calcific pancarditis and hydrops fetalis. Am J Obstet Gynecol. 1970;106(4):629-630. 155. von Kaisenberg CS, Jonat W. Fetal parvovirus B19 infection. Ultrasound Obstet Gynecol. 2001;18(3):280-288. 156. Gray ES, Davidson RJ, Anand A. Human parvovirus and fetal anaemia. Lancet. 1987;1(8542):1144. 157. Miller E, Fairley CK, Cohen BJ, Seng C. Immediate and long term outcome of human parvovirus B19 infection in pregnancy. Br J Obstet Gynaecol. 1998;105(2):174-178. 158. Bhal PS, Davies NJ, Westmoreland D, Jones A. Spontaneous resolution of non-immune hydrops fetalis secondary to transplacental parvovirus B19 infection. Ultrasound Obstet Gynecol. 1996;7(1):55-57. 159. Pryde PG, Nugent CE, Pridjian G, et al. Spontaneous resolution of nonimmune hydrops fetalis secondary to human parvovirus B19 infection. Obstet Gynecol. 1992;79(5 Pt 2):859-861. 160. Humphrey W, Magoon M, O’Shaughnessy R. Severe nonimmune hydrops secondary to parvovirus B-19 infection: spontaneous reversal in utero and survival of a term infant. Obstet Gynecol. 1991;78(5 Pt 2): 900-902. 161. Cossart YE, Field AM, Cant B, Widdows D. Parvovirus-like particles in human sera. Lancet. 1975;1(7898):72-73. 162. Kovacs BW, Carlson DE, Shahbahrami B, Platt LD. Prenatal diagnosis of human parvovirus B19 in nonimmune hydrops fetalis by polymerase chain reaction. Am J Obstet Gynecol. 1992;167(2):461-466. 163. Nagel HT, de Haan TR, Vandenbussche FP, et al. Long-term outcome after fetal transfusion for hydrops associated with parvovirus B19 infection. Obstet Gynecol. 2007;109(1):42-47. 164. Dembinski J, Haverkamp F, Maara H, et al. Neurodevelopmental outcome after intrauterine red cell transfusion for parvovirus B19-induced fetal hydrops. BJOG. 2002;109(11):1232-1234. 165. De Jong EP, Lindenburg IT, van Klink JM, et al. Intrauterine transfusion for parvovirus B19 infection: long-term neurodevelopmental outcome. Am J Obstet Gynecol. 2012;206(3):204.e1-204.e5. 166. Daffos F, Forestier F, Capella-Pavlovsky M, et al. Prenatal management of 746 pregnancies at risk for congenital toxoplasmosis. N Engl J Med. 1988;318(5):271-275. 167. Friedman S, Ford-Jones LE, Toi A, et al. Congenital toxoplasmosis: prenatal diagnosis, treatment and postnatal outcome. Prenat Diagn. 1999; 19(4):330-333. 168. Zornes SL, Anderson PG, Lott RL. Congenital toxoplasmosis in an infant with hydrops fetalis. South Med J. 1988;81(3):391-393.

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195. Galjaard H. Fetal diagnosis of inborn errors of metabolism. Baillieres Clin Obstet Gynaecol. 1987;1(3):547-567. 196. Van Kamp IL, Klumper FJ, Oepkes D, et al. Complications of intrauterine intravascular transfusion for fetal anemia due to maternal red-cell alloimmunization. Am J Obstet Gynecol. 2005;192(1):171-177. 197. Tongsong T, Wanapirak C, Kunavikatikul C, et al. Fetal loss rate associated with cordocentesis at midgestation. Am J Obstet Gynecol. 2001;184(4): 719-723. 198. Tongsong T, Wanapirak C, Kunavikatikul C, et al. Cordocentesis at 16-24 weeks of gestation: experience of 1,320 cases. Prenat Diagn. 2000;20(3): 224-228. 199. Weiner CP, Okamura K. Diagnostic fetal blood sampling-technique related losses. Fetal Diagn Ther. 1996;11(3):169-175. 200. Ghidini A, Sepulveda W, Lockwood CJ, Romero R. Complications of fetal blood sampling. Am J Obstet Gynecol. 1993;168(5):1339-1344. 201. Liao C, Wei J, Li Q, et al. Efficacy and safety of cordocentesis for prenatal diagnosis. Int J Gynaecol Obstet. 2006;93(1):13-17. 202. Pasman SA, Claes L, Lewi L, et al. Intrauterine transfusion for fetal anemia due to red blood cell alloimmunization: 14 years experience in Leuven. Facts Views Vis Obgyn. 2015;7(2):129-136. 203. Mari G, Norton ME, Stone J, et al. Society for Maternal-Fetal Medicine (SMFM) Clinical Guideline #8: the fetus at risk for anemia—diagnosis and management. Am J Obstet Gynecol. 2015;212(6):697-710. 204. Daffos F, Forestier F, Mac Aleese J, et al. Fetal curarization for prenatal magnetic resonance imaging. Prenat Diagn. 1988;8(4):312-314. 205. Bernstein HH, Chitkara U, Plosker H, et al. Use of atracurium besylate to arrest fetal activity during intrauterine intravascular transfusions. Obstet Gynecol. 1988;72(5):813-816. 206. Yinon Y, Visser J, Kelly EN, et al. Early intrauterine transfusion in severe red blood cell alloimmunization. Ultrasound Obstet Gynecol. 2010;36(5):601-606. 207. Mandelbrot L, Daffos F, Forestier F, et al. Assessment of fetal blood volume for computer-assisted management of in utero transfusion. Fetal Ther. 1988; 3(1-2):60-66. 208. el-Azeem SA, Samuels P, Rose RL, et al. The effect of the source of transfused blood on the rate of consumption of transfused red blood cells in pregnancies affected by red blood cell alloimmunization. Am J Obstet Gynecol. 1997;177(4):753-757. 209. Mari G, Zimmermann R, Moise Jr KJ, Deter RL. Correlation between middle cerebral artery peak systolic velocity and fetal hemoglobin after 2 previous intrauterine transfusions. Am J Obstet Gynecol. 2005;193(3 Pt 2): 1117-1120. 210. Ruiz Villaespesa A, Suarez Mier MP, Lopez Ferrer P, et al. Nonimmunologic hydrops fetalis: an etiopathogenetic approach through the postmortem study of 59 patients. Am J Med Genet. 1990;35(2):274-279. 211. Knisely AS. The pathologist and the hydropic placenta, fetus, or infant. Semin Perinatol. 1995;19(6):525-531. 212. Steiner RD. Hydrops fetalis: role of the geneticist. Semin Perinatol. 1995;19(6):516-524. 213. Santolaya J, Alley D, Jaffe R, Warsof SL. Antenatal classification of hydrops fetalis. Obstet Gynecol. 1992;79(2):256-259. 214. Gudmundsson S, Huhta JC, Wood DC, et al. Venous Doppler ultrasonography in the fetus with nonimmune hydrops. Am J Obstet Gynecol. 1991; 164(1 Pt 1):33-37. 215. Kaiser IH. Ballantyne and triple edema. Am J Obstet Gynecol. 1971;110(1):115-120. 216. Kumar B, Nazaretian SP, Ryan AJ, Simpson I. Mirror syndrome: a rare entity. Pathology. 2007;39(3):373-375. 217. Vidaeff AC, Pschirrer ER, Mastrobattista JM, et al. Mirror syndrome. A case report. J Reprod Med. 2002;47(9):770-774. 218. Ordorica SA, Marks F, Frieden FJ, et al. Aneurysm of the vein of Galen: a new cause for Ballantyne syndrome. Am J Obstet Gynecol. 1990; 162(5):1166-1167. 219. Dorman SL, Cardwell MS. Ballantyne syndrome caused by a large placental chorioangioma. Am J Obstet Gynecol. 1995;173(5):1632-1633. 220. Livingston JC, Malik KM, Crombleholme TM, et al. Mirror syndrome: a novel approach to therapy with fetal peritoneal-amniotic shunt. Obstet Gynecol. 2007;110(2 Pt 2):540-543.

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221. Duthie SJ, Walkinshaw SA. Parvovirus associated fetal hydrops: reversal of pregnancy induced proteinuric hypertension by in utero fetal transfusion. Br J Obstet Gynaecol. 1995;102(12):1011-1013. 222. Heyborne KD, Chism DM. Reversal of Ballantyne syndrome by selective second-trimester fetal termination. A case report. J Reprod Med. 2000; 45(4):360-362. 223. Espinoza J, Romero R, Nien JK, et al. A role of the anti-angiogenic factor sVEGFR-1 in the ‘mirror syndrome’ (Ballantyne’s syndrome). J Matern Fetal Neonatal Med. 2006;19(10):607-613. 224. McCurdy Jr CM, Seeds JW. Route of delivery of infants with congenital anomalies. Clin Perinatol. 1993;20(1):81-106. 225. Kirshon B, Mari G, Moise Jr KJ. Indomethacin therapy in the treatment of symptomatic polyhydramnios. Obstet Gynecol. 1990;75(2):202-205. 226. Abrams ME, Meredith KS, Kinnard P, Clark RH. Hydrops fetalis: a retrospective review of cases reported to a large national database and identification of risk factors associated with death. Pediatrics. 2007;120(1):84-89. 227. Nakayama H, Kukita J, Hikino S, et al. Long-term outcome of 51 liveborn neonates with non-immune hydrops fetalis. Acta Paediatr. 1999; 88(1):24-28. 228. Haverkamp F, Noeker M, Gerresheim G, Fahnenstich H. Good prognosis for psychomotor development in survivors with nonimmune hydrops fetalis. BJOG. 2000;107(2):282-284. 229. Mari G, Abuhamad AZ, Cosmi E, et al. Middle cerebral artery peak systolic velocity: technique and variability. J Ultrasound Med. 2005;24(4): 425-430.

230. Machin GA. Hydrops revisited: literature review of 1,414 cases published in the 1980s. Am J Med Genet. 1989;34(3):366-390. 231. Santo S, Mansour S, Thilaganathan B, et al. Prenatal diagnosis of non-immune hydrops fetalis: what do we tell the parents? Prenat Diagn. 2011;31(2): 186-195. 232. Center for Disease Control (CDC). Risks associated with human parvovirum B19 infection. MMWR Morb Mortal Wkly Rep. 1989;38(6):81-88, 93-97. 233. Dijkmans AC, de Jong EP, Dijkmans BA, et al. Parvovirus B19 in pregnancy: prenatal diagnosis and management of fetal complications. Curr Opin Obstet Gynecol. 2012;24(2):95-101. 234. Cavoretto P, Molina F, Poggi S, et al. Prenatal diagnosis and outcome of echogenic fetal lung lesions. Ultrasound Obstet Gynecol. 2008;32(6): 769-783. 235. Wilson RD, Baxter JK, Johnson MP, et al. Thoracoamniotic shunts: fetal treatment of pleural effusions and congenital cystic adenomatoid malformations. Fetal Diagn Ther. 2004;19(5):413-420. 236. Loh KC, Jelin E, Hirose S, et al. Microcystic congenital pulmonary airway malformation with hydrops fetalis: steroids vs open fetal resection. J Pediatr Surg. 2012;47(1):36-39. 237. Society for Maternal-Fetal Medicine, Simpson LL. Twin-twin transfusion syndrome. Am J Obstet Gynecol. 2013;208(1):3-18.

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Fetal Measurements: Normal and Abnormal Fetal Growth and Assessment of Fetal Well-Being Carol B. Benson and Peter M. Doubilet

SUMMARY OF KEY POINTS • Accurate assignment of gestational age to a pregnancy is important for several reasons, including timing of screening tests for aneuploidy, monitoring fetal growth and diagnosing growth disturbances, and scheduling of delivery by elective induction or cesarean. • If a woman has more than one sonogram during her pregnancy, the pregnancy should not be redated after the first scan; instead, the gestational age at the time of subsequent scans is the age at initial scan plus the time elapsed since that scan. • In the first trimester, dating by sonographic findings or mean sac diameter prior to 6.0 weeks’ gestation has an accuracy of ±0.5 weeks, while dating by crown-rump length at 6.0 weeks or later has an accuracy of ±0.7 weeks. • Sonographic dating in the second and third trimesters has an accuracy of ±1.2 weeks at 14 to 20 weeks, ±1.9 weeks

•

•

•

•

at 20 to 26 weeks, ±3.1 to 3.4 weeks at 26 to 32 weeks, and ±3.5 to 3.8 after 32 weeks. Fetal weight is estimated using a formula that incorporates measurements of the fetal head, abdomen, and femur and has an accuracy (95% confidence range) of ±15% to 18%. Estimated fetal weight should be assessed in relation to gestational age to determine whether the fetus is appropriate in size for gestational age. If a fetus is diagnosed as small-for-gestational-age, with an estimated fetal weight less than 10th percentile for gestational age, an attempt should be made to determine the cause through evaluation of both mother and fetus. When a fetus is suspected of being growth restricted, antenatal surveillance with biophysical profiles and fetal Doppler can guide management and improve outcome.

CHAPTER OUTLINE GESTATIONAL AGE DETERMINATION First Trimester Second and Third Trimesters Fetal Head Measurements Femur Length Abdominal Circumference Composite Formulas Gestational Age Estimation by Ultrasound: Most Accurate Approach at Each Stage of Pregnancy

S

WEIGHT ESTIMATION AND ASSESSMENT Estimation of Fetal Weight Recommended Approach Weight Assessment in Relation to Gestational Age FETAL GROWTH ABNORMALITIES The Large Fetus General Population Diabetic Mothers

onographic measurements of the fetus provide information about fetal age and growth. These data are used to assign gestational age, estimate fetal weight, and diagnose growth disturbances. As discussed in other chapters, fetal measurements are also used in the diagnosis of a number of fetal anomalies, such as skeletal dysplasias1 and microcephaly.2 Each of these abnormalities can be diagnosed or suspected on the basis of measurements that deviate from the “normal for dates.”

The Small-for-Gestational-Age Fetus and Fetal Growth Restriction ASSESSMENT OF FETAL WELL-BEING Biophysical Profile Fetal Doppler Umbilical Artery Doppler Ductus Venosus Doppler Middle Cerebral Artery Doppler Summary of Fetal Doppler

It is important to begin by defining the various terms used in the evaluation of the age of a pregnancy. The true measure of a pregnancy’s age is the number of days since conception, termed conceptual age. Historically, however, pregnancies were dated by the number of days since the first day of the last menstrual period (LMP), termed menstrual age, because for most of human history it was unknown when conception occurred. In women with regular 28-day cycles, menstrual age

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is 2 weeks more than conceptual age, because conception occurs approximately 2 weeks after the LMP in such women. Currently, the term most often used to date pregnancies is gestational age, which is similar to menstrual age and is defined as follows: Gestational age = Conceptual age + 2 weeks In women with 28-day cycles, gestational age and menstrual age are equal. In women with longer cycles, gestational age is less than menstrual age; the opposite holds in women with shorter cycles. Accurate knowledge of gestational age is important for a number of reasons. The timing of screening tests in the first trimester, such as nuchal translucency measurement and maternal cell free fetal DNA analysis,3,4 genetic amniocentesis in the second trimester, and elective induction or cesarean delivery in the third trimester are all based on the gestational age. The differentiation between term and preterm labor and the characterization of a fetus as “postdates” depend on gestational age. Knowledge of the gestational age can be critical in distinguishing normal from pathologic fetal development. Midgut herniation, for example, is normal up to 11 to 12 weeks of gestation5 but signifies omphalocele thereafter. The normal size of a variety of fetal body parts depends on gestational age, as do levels of maternal serum alpha-fetoprotein,6 human chorionic gonadotropin,7 and estriol.8 When a fetal anomaly is detected prenatally, the maternal choices and obstetric management are significantly influenced by gestational age. Estimation of the fetal weight, on its own and in relation to the gestational age, can influence obstetric management decisions concerning the timing and route of delivery. A fetus growing poorly may benefit from close monitoring of fetal well-being to determine if early delivery is indicated. Such a fetus may be inadequately supplied by its placenta with oxygen and nutrients and, therefore, may do better in the care of a neonatologist than in utero. When a fetus is large, cesarean may be the preferred route of delivery, particularly in pregnancies complicated by maternal diabetes. In view of these considerations, fetal measurements should be a component of every complete obstetric sonogram.9 The well-being of the fetus at risk for perinatal morbidity and mortality, such as a growth-restricted fetus, can be monitored by ultrasound using the biophysical profile and Doppler. Abnormalities and changes in any of these surveillance tests may guide decisions about timing of delivery.10,11

GESTATIONAL AGE DETERMINATION Clinical dating of a pregnancy is usually based on the patient’s recollection of the first day of her LMP and on physical examination of uterine size. Unfortunately, both of these methods are imprecise, leading to inaccuracies in gestational age assignment. Dating by LMP (menstrual age) may be inaccurate because of variability in length of menstrual cycles, faulty memory,12,13 recent exposure to oral contraceptives, or bleeding during early pregnancy.14 Determining gestational age from the palpated dimension of the uterus may be affected by uterine fibroids, multiple pregnancy, and maternal body habitus.

Clinical dating is accurate only if either of the following two conditions apply: (1) the patient is a good historian with regular menstrual cycles, and the uterine size correlates closely with LMP; or (2) information is available specifying the time of conception, such as a basal body temperature chart or pregnancy achieved via assisted reproductive technologies in women treated for infertility. Ultrasound provides an alternative and, in many cases, superior approach to gestational age estimation. Sonographic age estimation is based on sonographic findings or measurements taken during the ultrasound examination. Because biologic variability in the size of fetuses increases as pregnancy progresses, the accuracy of sonographic age estimates declines as pregnancy proceeds.15-28 Thus, if a woman has more than one sonogram during a pregnancy, the pregnancy should never be redated after the first scan. The decision as to whether to use clinical dating or sonographic dating at the time of the first scan is not well established for all pregnancies. In some cases, though, the decision is clear-cut: pregnancies achieved via in vitro fertilization should be dated based on the embryo transfer dates, and naturally conceived pregnancies in women with irregular menstrual cycles or with poor recollection of their LMP should be dated based on sonographic criteria. In other situations, however, particularly for pregnancies conceived naturally in women with regular cycles and good recollection of LMP, there are two reasonable alternatives. The first approach is to date the pregnancy based on LMP whenever the ages based on LMP and sonography are close to one another: within 5 days up to 8.9 weeks; within 7 days from 9.0 weeks to 15.9 weeks; within 10 days from 16.0 weeks to 21.9 weeks; within 14 days from 22.0 weeks to 27.9 weeks; and within 21 days from 28.0 weeks onward.16 An alternative approach is to use sonographic dating routinely up to 24 weeks and the LMP thereafter, if the LMP is clearly recalled and within 21 days of sonographic dating.15 Whichever approach is used, it is important to know what sonographic criteria are available for gestational age estimation and which are the most accurate at each stage of pregnancy.

First Trimester Sonographic findings and measurements allow highly accurate dating from 5 weeks’ gestation until the end of the first trimester. The earliest sign of an intrauterine pregnancy is identification of a gestational sac in the uterine cavity. This appears as a round or oval fluid collection within the uterine cavity first seen on transvaginal sonography at approximately 5 weeks’ gestation.29 In some cases, the early gestational sac is surrounded by one or two echogenic rings, formed by the proliferating chorionic villi and the deeper layer of the decidua vera.30,31 These rings are not consistently present, however, and any round or oval fluid collection in the mid uterus of a woman with a positive pregnancy test is highly likely to be a gestational sac32 (Fig. 42.1). From 5 to 6 weeks’ gestation, two methods can be used to assign gestational age by ultrasound: (1) measurement of mean sac diameter (MSD) or (2) sonographic identification of gestational sac contents. The MSD is calculated as the average of the anteroposterior diameter, the transverse diameter, and the longitudinal diameter. It increases from 2 mm at 5 weeks to

CHAPTER 42  Fetal Measurements

FIG. 42.1  Gestational Sac.  At 5.0 weeks’ gestation, gestational sac (arrow) appears as a small, intrauterine fluid collection.

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FIG. 42.2  Yolk Sac.  Gestational sac contains yolk sac (arrow) on transvaginal sonogram at 5.5 weeks’ gestation. No embryo is seen. SAG ML, Sagittal midline.

TABLE 42.1  Gestational Dating by Mean Sac Diameter (MSD) in the Early First Trimester MSD (mm)  2  3  4  5  6  7  8  9 10

Gestational Age (Weeks) 5.0 5.1 5.2 5.4 5.5 5.6 5.7 5.9 6.0

95% Confidence interval = ±0.5 week. Values from Daya S, Wood S, Ward S, et al. Early pregnancy assessment with transvaginal ultrasound scanning. CMAJ. 1991; 144(4):441-446.33

10 mm at 6 weeks,33 a growth pattern that can be used to assign gestational age during this period (Table 42.1). The second method, based on the sonographic findings within the gestational sac, is best done by transvaginal sonography and relies on the observation that, on average, the gestational sac is first identifiable at 5.0 weeks, the yolk sac at 5.5 weeks (Fig. 42.2), and the embryo and embryonic heartbeat at 6.0 weeks34 (Fig. 42.3, Video 42.1). The timing of these milestones is subject to minimal variability, with a 95% confidence range of approximately 0.5 weeks.31 Gestational age can be assigned based on these milestones (Table 42.2). From 6 weeks until the end of the first trimester, gestational age correlates closely with the crown-rump length (CRL) of the embryo or fetus.35,36 The term embryo is commonly used up to 10 weeks’ gestation, and the term fetus applies thereafter.37 The CRL is the length of the embryo or fetus from the top of its head to the bottom of its torso. It is measured as the longest dimension of the embryo, excluding the yolk sac and extremities. From 9 or 10 weeks onward, the CRL measurements are most accurate

FIG. 42.3  Embryonic Heartbeat.  Transvaginal sonogram and M-mode at 6 weeks demonstrate cardiac activity originating from tiny embryo (arrow) adjacent to the yolk sac. See also Video 42.1.

if taken with the fetus in neutral position38 (Fig. 42.4). The CRL can be used to assign gestational age accurately up to 14 weeks because there is little biologic variability in fetal length up until that age39 (Table 42.3). After that point, the CRL of the longer, more developed fetus becomes less reliable. At this later stage, the CRL is affected by the fetal position, measuring shorter in a fetus whose spine is flexed and longer in a fetus whose spine is extended.

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TABLE 42.2  Gestational Dating by Ultrasound in the First Trimester Sonographic Finding

Gestational Age (Weeks)

Gestational sac, no yolk sac, embryo, or heartbeat Gestational sac with yolk sac, no embryo or heartbeat Gestational sac with heartbeat and embryo ) = 1.4787 − 0.003343 AC × FL + BPD2 + 0.0458 AC + 0.158 FL FORMULA 2a Log10 (EFW >) = 1.1134 + 0.05845 AC − 0.000604 AC2 − 0.007365 BPD2 + BPD2 + 0.00595 BPD × AC + 0.1694 BPD FORMULA 3a Log10 (EFW) = 1.3598 + 0.051 AC + 0.01844 FL − 0.0037 AC × FL a

Formulas from Hadlock FP, Harrist RB, Sharman RS, et al. Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol. 1985;151(3):333-337.26 AC, Abdominal circumference (cm); BPD, biparietal diameter (cm); EFW, estimated fetal weight, in grams (g); FL, femur length (cm); OFD, occipitofrontal diameter (cm).

of gestational age (Table 42.10), several of which appear in the literature.71-76 There is some debate about a number of aspects of fetal weight assessment in relation to gestational age. Should a weight table or chart based on neonatal weights or on estimated fetal weights be used? Should the table or chart be derived solely from pregnancies of low-risk mothers? Should “population norms” or “customized norms” be used? Most weight norms (tables or charts) are derived from large data sets of neonatal birth weights from babies born at a known gestational age.71-76 At least one chart, on the other hand, was produced using estimated fetal weights instead of neonatal birth weights.77,78 A rationale for the latter is that several studies have shown that fetuses that deliver preterm are smaller, on average, than those of the same gestational age that remain in utero.79-83 Babies born preterm thus represent an abnormal group with a negatively skewed weight distribution. This supports the argument that fetuses should be compared to fetuses, not to babies.84 A large international study, INTERGROWTH-21st, used another approach to produce weight norms derived from a healthy population.85,86 Although it is based on birth weights rather than

TABLE 42.10  Fetal Weight Percentiles in the Third Trimester WEIGHT PERCENTILES (GRAMS) Gestational Age (Weeks)

10th

50th

90th

25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43

490 568 660 765 884 1020 1171 1338 1519 1714 1919 2129 2340 2544 2735 2904 3042 3142 3195

660 760 875 1005 1153 1319 1502 1702 1918 2146 2383 2622 2859 3083 3288 3462 3597 3685 3717

889 1016 1160 1322 1504 1706 1928 2167 2421 2687 2959 3230 3493 3736 3952 4127 4254 4322 4324

With permission from Doubilet PM, Benson CB, Nadel AS, Ringer SA. Improved birth weight table for neonates developed from gestations dated by early ultrasonography. J Ultrasound Med. 1997;16(4):241-249.71

fetal weights, the study population used to generate these norms consists of babies born at or beyond 33 weeks to mothers with no known pregnancy-related risk factors. The INTERGROWTH21st norms, however, are of limited use for assessing fetal weight in relation to gestational age, because they do not cover the period prior to 33 weeks’ gestation. Perhaps the biggest controversy in weight assessment is whether the estimated weight of a fetus should be compared to norms from the overall population or to customized norms87-91 derived from a subgroup of fetuses similar to that fetus. For example, if an African-American fetus has an estimated weight of 1200 g at 30 weeks’ gestation, should the weight percentile be determined from overall population norms or from African-American norms? In that example, the population-based percentile would be lower than the customized percentile, because African-American fetuses and neonates are smaller, on average, than those in the general population.92 Although there are proponents of customized norms,93-95 a major concern with this approach is that it can do harm by inadvertently normalizing the weight of a fetus who is small on a pathologic basis.96,97 This viewpoint is supported by the fact that at least some population groups with small babies have elevated rates of postnatal complications98 and by the INTERGROWTH-21st finding that neonates of healthy mothers do not differ in size based on ethnic background.99 Overall, our recommended approach is to use population norms. Although it would theoretically be preferable to use norms

FETAL GROWTH ABNORMALITIES The Large Fetus The large-for-gestational-age (LGA) neonate (or fetus) is defined as one whose weight is above the 90th percentile for gestational age.71,103-105 Macrosomia, a related entity, is most often defined on the basis of a weight above 4000 g; other weight cutoffs (4100 g, 4500 g) are sometimes used.74,76-80,106 These growth disturbances occur with different frequencies and are associated with different morbidities and mortalities in diabetic mothers as compared to the general population. Therefore these two patient populations are considered separately.

General Population About 10% of all infants have birth weights above the 90th percentile for gestational age and are considered LGA infants.

5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5

A

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99th percentile 90th percentile 50th percentile 10th percentile 1st percentile

25

30 35 Gestational age (wks)

25

30 35 Gestational age (wks)

40

100 90 80 EFW percentile

derived from estimated fetal weights,77,78 norms derived from birth weights are better established and are based on larger study populations.71-76 The weight gain between two ultrasound examinations can be estimated as the difference between the two estimated weights. Adequacy of weight gain can be assessed by comparing this difference to established normal fetal growth rate as a function of gestational age. INTERGROWTH-21st data indicate that median fetal weight gain per week decreases progressively from 33 weeks of gestation onward, with a maximum rate of 270 g per week at 33 weeks, down to 100 g per week at 41 weeks.86 Other older growth tables suggest that weight gain may increase until 36 weeks, then decline steadily thereafter.71,72 The longer the time is between scans, the more accurate the sonographic estimate of interval weight gain will be. When two scans are performed within 1 week of each other, weight gain cannot be determined reliably, because weight prediction is too imprecise to detect small changes in growth. Furthermore, estimating weight too close to the time of the prior scan could raise unnecessary concern by a spurious finding that the fetus has grown subnormally or even lost weight. Thus there is little or no value in computing an estimated weight at the time of the second scan 1 week after the first. Instead, it is recommended that fetal weight gain only be assessed after an interval of at least 2 weeks’ duration.10,11 When several examinations have been performed, fetal growth can be depicted graphically by means of a trend plot or growth curve. One form of growth curve plots the estimated fetal weight versus gestational age, with the curve for the fetus being examined superimposed on lines depicting the 1st, 10th, 50th, 90th, and 99th percentiles (Fig. 42.10A). An alternative mode of display plots the estimated fetal weight percentile versus gestational age (Fig. 42.10B). In this latter format, the graph for a normally growing fetus will be a horizontal line, indicating maintenance of a particular weight percentile throughout gestation. A down sloping line suggests subnormal growth rate. Calculation of weight percentiles and plotting of growth curves are most easily accomplished by computer, using an obstetric ultrasound software package that performs these tasks.100-102 Alternatively, similar results can be achieved by means of a calculator and manual plotting of data.

EFW (kg)

CHAPTER 42  Fetal Measurements

70 60 50 40 30 20 10 0

B

40

FIG. 42.10  Fetal Growth Curves.  (A) Estimated fetal weight plotted against gestational age, superimposed on 1st, 10th, 50th, 90th, and 99th percentile curves. The fetus depicted here has a normal growth pattern, with estimated fetal weights between the 50th and 90th percentile over four sonograms. (B) Estimated fetal weight (EFW) percentile against gestational age.

Of all newborns, 8% to 10% have birth weights over 4000 g and thus are classified as “macrosomic,” and 2% weigh over 4500 g.104,106-109 These rates, however, vary considerably among different patient subgroups, depending on presence or absence of risk factors. Risk factors for LGA and macrosomia include maternal obesity, history of a previous LGA infant, prolonged pregnancy (>40 weeks), excess pregnancy weight gain, multiparity, and advanced maternal age.103,104,107,110-112 Large fetuses have an increased incidence of perinatal morbidity and mortality, in large part because of obstetric complications. Shoulder dystocia, fractures, and facial and brachial plexus palsies occur more frequently as a result of traumatic delivery.106,110,113,114 The incidence of perinatal asphyxia, meconium aspiration, neonatal hypoglycemia, and other metabolic complications is significantly increased in these pregnancies.103,106,107,110 The most straightforward approach to diagnosing fetal LGA and macrosomia is to use the estimated fetal weight computed from sonographic measurements. An estimated weight above the 90th percentile for gestational age suggests LGA, and a weight estimate above 4000 g suggests macrosomia. Although weight estimation is somewhat less accurate in large than in average-sized fetuses,62,115 this approach has been demonstrated to be moderately good for diagnosing LGA and macrosomia. It has a positive

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predictive value (PPV) of up to 51% for LGA and 67% for macrosomia. Other proposed sonographic parameters have lower sensitivity or lower PPV than the estimated fetal weight62,103,106,116-124 (Table 42.11).

Diabetic Mothers Fetuses of insulin-dependent and gestational diabetic mothers are exposed to high levels of glucose throughout pregnancy and, as a result, produce excess insulin. This leads to overgrowth of the fetal trunk and abdominal organs, while the head and brain grow at a normal rate.104,105 Therefore these fetuses tend to have different body proportions than fetuses of nondiabetic mothers. Sonographic measurements of fetuses of diabetic mothers demonstrate accelerated growth of the fetal thorax and abdomen beginning between 28 and 32 weeks’ gestation.104,105,125 An LGA weight occurs in 25% to 42% and macrosomia in 10% to 50% of infants of diabetic mothers.104,105,126 As many as 12% of infants of mothers with diabetes weigh more than 4500 g at birth. Perinatal complications are more frequent in macrosomic fetuses of diabetic mothers than in those of nondiabetic mothers.109,113,114,127,128 Shoulder dystocia, for example, occurs in 31% of macrosomic fetuses of diabetic mothers and only 3% to 10% of macrosomic fetuses of nondiabetic mothers.110,113 Many sonographic parameters, involving a variety of measurements, formulas, and ratios, have been proposed for diagnosing LGA and macrosomia in the fetus of the diabetic mother117,129-131 (Table 42.12). As a group, these have higher sensitivities and PPVs than sonographic criteria in the general population, in part because of the higher prevalence of large fetuses in diabetic mothers. As in the general population, the most straightforward approach to diagnosing LGA and macrosomia in the fetuses of diabetic mothers is by means of the sonographically estimated

fetal weight.68,117,129,132,133 A fetus whose estimated weight falls above the 90th percentile for gestational age has a 74% likelihood of being LGA, versus 19% if the estimated weight lies below the 90th percentile.129 A weight estimate above 4000 g is associated with a 77% chance of macrosomia, and one above 4500 g with an 86% chance. The chance of macrosomia is only 16% when the weight estimate is less than 4000 g.68 Thus, if vaginal delivery is believed to be contraindicated for the macrosomic fetuses of diabetic mothers, the estimated fetal weight should be considered when selecting the route of delivery.

The Small-for-Gestational-Age Fetus and Fetal Growth Restriction Fetuses are termed small for gestational age (SGA) if their estimated weights are below the 10th percentile for gestational age. SGA fetuses are a heterogeneous group and can be subdivided into constitutionally small fetuses (e.g., those with small parents) and fetuses whose small size is due to a pathologic process.

Small-for-Gestational-Age Fetuses: Causes CONSTITUTIONALLY SMALL PATHOLOGICALLY SMALL Placenta Mediated Primary placental Maternal Fetal Aneuploidy Malformations Infections

TABLE 42.11  Sonographic Criteria for Large-for-Gestational Age (LGA) and Macrosomia in the General Population: Performance Characteristics PREDICTIVE VALUES (%)a

(%) Sensitivity

Specificity

Positive

Negative

CRITERIA TO PREDICT LGAa Elevated AD-BPD115 Low FL/AC103,115 Elevated AFV119,123 Elevated ponderal index103,115 High EFW103,123 Elevated growth score103 Elevated AFV, high EFW123

46 24-75 12-17 13-15 20-74 14 11

79 44-93 92-98 85-98 93-96 91 99

19 13-26 19-35 13-36 6-51 10 54

93 92-94 91 91-94 88-94 90 99

CRITERIA TO PREDICT MACROSOMIA Elevated FL121 Elevated AC121 High EFW63,124,121 Elevated BPD121

24 53 11-65 29

96 94 89-96 98

52 63 38-67 71

88 89 83-91 92

a Predictive values for criteria for LGA computed using Bayes’ theorem,112 assuming an LGA prevalence rate of 10%. AC, Abdominal circumference; AD, abdominal diameter; AFV, amniotic fluid volume; BPD, biparietal diameter; EFW, estimated fetal weight; FL, femur length; FL/AC, femur length to abdominal circumference ratio. With permission from Doubilet PM, Benson CB. Fetal growth disturbances. Semin Roentgenol. 1990;25(4):309-316.117

CHAPTER 42  Fetal Measurements As a group, SGA fetuses have a poor prognosis, with increased perinatal morbidity and mortality rates. Their mortality rate is four to eight times that of non-SGA fetuses.134-136 Half of surviving SGA fetuses have serious short- or long-term morbidity, including meconium aspiration, pneumonia, and metabolic disorders.134,137-139 The risk, however, is dependent on the cause of the small size. Constitutionally small fetuses carry no elevated risk, unlike those who are small because of a pathologic condition. Furthermore, the potential to improve outcome by appropriate management of pathologically small fetuses varies depending on causation. For example, when the small size is caused by placental insufficiency, early delivery may improve outcome, but this intervention is unlikely to affect outcome in chromosomally abnormal fetuses. The term fetal growth restriction (FGR), also called intrauterine growth restriction, is used differently by different authors. Some use FGR and SGA synonymously, considering all fetuses below the 10th percentile for gestational age to be growth restricted. Others use FGR to refer to pathologically small fetuses. Terminology aside, determination of the cause(s) of small fetal size is often difficult, so that all SGA fetuses should be classified as suspected FGR.140 The approach to SGA or FGR involves three steps: (1) diagnosis: identify small fetuses; (2) classification: attempt to determine the cause of the small size; (3) management: institute monitoring and decide on timing of delivery. The most direct approach to identifying SGA fetuses is to diagnose SGA if the estimated fetal weight falls below the 10th percentile for the best estimate of gestational age. Several other criteria for diagnosing SGA or FGR have been proposed, including sonographic measurements and ratios,141 as well as a multiparameter scoring system.142,143 None of the individual parameters

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has a high PPV,141 and the performance characteristics of the scoring system143 are not good enough to make up for its complexity and cumbersome nature. Thus the straightforward approach of using the estimated fetal weight percentile is the preferred method for diagnosing SGA fetuses. Once SGA has been diagnosed, an attempt should be made to determine its cause through evaluation of both the mother and the fetus. Maternal assessment should include physical examination and blood tests, directed toward diagnosis of hypertension, renal disease, and other maternal conditions that can cause FGR. Fetal assessment begins with a careful sonographic examination, looking especially for findings suggestive of a chromosomal or viral cause (e.g., holoprosencephaly, clenched hands, rocker-bottom feet, intracranial calcifications). If such a finding is present, amniocentesis or umbilical blood sampling can confirm the diagnosis of a chromosomal abnormality. A viral cause of FGR may also be diagnosed by these procedures, in some cases.144 Growth-restricted fetuses, other than those with a lethal condition, such as trisomy 13 or 18, should be carefully monitored for the remainder of the pregnancy. The monitoring is typically performed at weekly or semiweekly intervals. Sonographic features to be followed include amniotic fluid volume, biophysical profile score, estimated fetal weight percentile, and fetal Doppler. A worsening trend in one or more of these features should prompt consideration of early delivery.

ASSESSMENT OF FETAL WELL-BEING It has been shown that when a fetus is suspected of being growth restricted or having another condition that could affect the

TABLE 42.12  Sonographic Criteria for Large-for-Gestational Age (LGA) and Macrosomia in Diabetic Mothers: Performance Characteristics (%)

PREDICTIVE VALUES (%)

Sensitivity

Specificity

Positive

Negative

CRITERIA TO PREDICT LGAa Elevated HC129 Elevated AC/BPD130 High EFW129 Elevated BPD129 Elevated AC105,127,129 Elevated AC growth105 Low FL/AC105,130 Elevated AC, high EFW129

50 83 78 13 71-88 84 58-79 72

80 60 78 86 81-85 85 75-80 71

64 71 74 75 56-78 79 68-83 89

70 75 81 57 81-96 89 75-76 89

CRITERIA TO PREDICT MACROSOMIA Elevated AC127 Low FL/AC131 Elevated TD-BPD126 High EFW68

84 48-64 87 48

78 60-74 72 95

41 36-42 61 77

96 80-83 92 84

a Predicted values for criteria for LGA computed using Bayes theorem,112 assuming an LGA prevalence rate of 10%. AC, Abdominal circumference; AC/BPD, abdominal circumference to biparietal diameter ratio; BPD, biparietal diameter; EFW, estimated fetal weight; FL, femur length; FL/AC, femur length to abdominal circumference ratio; HC, head circumference; TD, thoracic diameter. With permission from Doubilet PM, Benson CB. Fetal growth disturbances. Semin Roentgenol. 1990;25(4):309-316.117

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Fetal and Placental Risk Factors Associated With Fetal Growth Restriction

Maternal Risk Factors Associated With Fetal Growth Restriction

FETAL FACTORS Chromosomal Abnormalities Trisomy 13, 18, 21 Monosomy (45,XO) Deletions Uniparental disomy Confined placental mosaicism

GENETIC/CONSTITUTIONAL NUTRITION/STARVATION Inflammatory bowel disease Ileojejunal bypass Chronic pancreatitis Low prepregnancy weight Poor pregnancy weight gain, second and third trimesters

Congenital Malformations Absence of fetal pancreas Anencephaly Diaphragmatic hernia Omphalocele Gastroschisis Renal agenesis/dysplasia Multiple malformations

HYPOXIC Severe lung disease Cyanotic heart disease Sickle cell anemia

Multiple Gestations Monochorionic twins One fetus with malformations Twin-to-twin transfusion Discordant twins Triplets PLACENTAL FACTORS Abnormal trophoblastic invasion Multiple placental infarctions (chronic abruption) Umbilical-placental vascular anomalies Abnormal cord insertion (velamentous cord insertion) Placenta previa Circumvallate placenta Chorioangiomata With permission from Lin C. Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol. 1998;92(6):1044-1055.135

oxygenation or nutrition to the fetus, antenatal surveillance can improve the outcome for these fetuses. Surveillance of such a fetus includes serial ultrasounds to monitor fetal growth, perform biophysical profiles (BPPs), and measure Doppler parameters. Nonstress tests (NSTs) are also used to monitor fetal well-being. The nature and frequency of monitoring tests depends on the apparent severity of fetal compromise.10,11

VASCULAR Chronic hypertension Preeclampsia Collagen vascular disease Type 1 diabetes mellitus RENAL Glomerulonephritis Lipoid nephritis Arteriolar nephrosclerosis Renal transplantation ANTIPHOSPHOLIPID ANTIBODIES ENVIRONMENT AND DRUGS High altitude Emotional stress Physical stress Cigarette smoking Alcohol abuse Substance abuse (heroin, cocaine) Therapeutic drugs Antimetabolites Anticonvulsants Anticoagulants POOR OBSTETRIC HISTORY Previous stillbirths Recurrent aborters Previous birth of growth-restricted fetus Previous preterm births With permission from Lin C. Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol. 1998;92(6):1044-1055.135

Biophysical Profile The BPP, introduced in the 1980s, is a noninvasive test of fetal well-being based on four ultrasound parameters and the NST. The four ultrasound parameters are (1) fetal movement, (2) fetal tone, (3) fetal breathing movements, and (4) amniotic fluid volume (Table 42.13, Fig. 42.11, Videos 42.2 and 42.3). Each parameter receives 2 points if the fetus meets criteria and 0 points if it does not. Thus a perfect score for the ultrasound portion of the BPP is 8 out of 8, with 2 points given for each of the four parameters.145,146 The parameters were chosen to assess both the acute and the chronic state of the fetus, with acute parameters being fetal tone, movement, and breathing movements, and amniotic

fluid volume being a chronic marker of fetal well-being.145 Studies have shown that the BPP is reliable and reproducible, and that scores of 8 out of 8 are associated with a low rate of stillbirths and low rate of fetal asphyxia within 1 week of testing.11,145,147-150 Lower scores, those below 6 out of 8, are associated with increased risk for fetal asphyxia, low cord pH, cerebral palsy, and stillbirth. The lower the score is, the higher the risk of perinatal compromise will be.11,145,148 The BPP exam is performed within 30 minutes. If a fetus does not meet criteria for a parameter within the 30-minute time period, that parameter is given a score of 0. The BPP score

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TABLE 42.13  Biophysical Profile Parameters for 30-Minute Ultrasound Examination Parameter

2 Points Given

0 Points Given

Fetal movement

At least 3 discrete body or limb movements At least 1 episode of extension and flexion of extremity or spine At least 30 seconds of continuous, rhythmic breathing movements Single pocket at least 1 cm across and 2 cm in vertical

Less than 3 discrete body or limb movements No episode of extension and flexion of extremity or spine No episode of continuous breathing movement for 30 seconds No pocket 1 cm across and 2 cm in vertical

Fetal tone Fetal breathing movement Amniotic fluid volume

With permission from Manning FA, Platt LD, Sipos L. Antepartum fetal evaluation: development of a fetal biophysical profile. Am J Obstet Gynecol. 1980;136(6):787-795.146

A

C

B

FIG. 42.11  Ultrasound Parameters for the Biophysical Profile.  (A) Sonogram of amniotic fluid pocket measuring 5.8 cm in vertical and more than 1 cm across, an adequate amount to earn 2 points for amniotic fluid for the biophysical profile. (B) Fetal breathing motion is identified by observing the diaphragm (arrow) of the fetus in longitudinal view to detect rhythmic inspiratory and expiratory movements. Two points are given if the fetus has 30 seconds of continuous breathing movements during the 30-minute exam. (C) Three-dimensional sonogram of fetus in curled position. In the biophysical profile, points for fetal movement are given if the fetus has at least three movements of the body or extremities in the 30-minute period and points are given for tone if there is at least one episode of flexion and extension. See also Videos 42.2 and 42.3.

is reported as the number of points earned over the total for the study, which is 8 for an ultrasound BPP without NST. When a score of less than 8 out of 8 is given, the parameter or parameters for which no points were given should also be reported. For example, if a fetus has normal amniotic fluid volume with a

pocket of fluid more than 2 cm vertical and 1 cm wide, demonstrates adequate fetal movement and tone to obtain 2 points for each, but does not demonstrate fetal breathing movement during the 30-minute exam, that BPP would be reported as 6 out of 8 with 2 points deducted for lack of fetal breathing movement. In

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most cases, the BPP does not require a full 30 minutes of sonographic evaluation, because, given the short sleep cycles of the fetus, it typically meets criteria in less than that time, sometimes as short as 5 minutes.145 The BPP as a test of fetal well-being has several limitations. First, the test is less reliable in the severely premature fetus because of lack of brain maturity and should not be administered before 24 weeks’ gestation.145 Second, the biophysical state of the fetus is affected by administration of corticosteroids, which may cause depression of fetal breathing and movement for a few days after treatment.151-155 This latter limitation must be kept in mind when using the BPP to guide management decisions shortly after steroid treatment.145

Fetal Doppler Doppler parameters of a number of vessels, including the umbilical artery, umbilical vein, ductus venosus, middle cerebral artery, aortic isthmus, and uterine artery in the mother, have been studied to determine if Doppler parameters can be used to predict outcome and direct management.140,156-160 Among vessels studied, umbilical artery Doppler has been shown to be the most useful for monitoring fetuses at risk for compromise, particularly those with suspected FGR.11,140,148,156,160,161 When umbilical artery Doppler is incorporated into surveillance of fetuses with suspected growth restriction, overall outcome is improved, with fewer unnecessary interventions, inductions of labor, cesarean deliveries, and perinatal deaths. 10,148,160-162 Although umbilical artery Doppler has been shown to improve outcome in fetuses with suspected growth restriction and in mothers with preeclampsia or hypertension, routine screening with umbilical artery Doppler in low-risk pregnancies is not recommended, because it has not resulted in improved outcome in this patient population.140,161 Although some advocate adding middle cerebral artery and/or ductus venosus Doppler to the evaluation of fetuses with suspected growth restriction and abnormal umbilical artery Doppler,161,163-165 studies have not yet shown improved outcomes when these additional Doppler studies are performed.10,11,140,148,160

Umbilical Artery Doppler Umbilical artery Doppler is used to assess fetal well-being after 24 weeks’ gestation for those fetuses with suspected growth restriction or in mothers with preeclampsia or hypertension.140,148,156,160,161 To obtain a waveform, the Doppler gate is placed on a free loop of umbilical cord, away from the placental and fetal cord insertions and in the absence of fetal breathing movements. The ratio of peak systolic to end-diastolic velocity is calculated (S/D ratio). Flow in the umbilical artery is normally low resistance, with an S/D ratio of less than 3.5 up to 28 weeks’ gestation and less than 3.0 thereafter166 (Fig. 42.12A). With significant placental dysfunction, resistance in the placenta increases and flow in the umbilical artery demonstrates diminished diastolic flow, with an S/D ratio above the normal range (Fig. 42.12B). In such cases, the risk of fetal compromise and perinatal mortality is increased. The risk of fetal compromise is increased further when end-diastolic flow in the umbilical artery is absent

(Fig. 42.12C), and is highest when end-diastolic flow is reversed (Fig. 42.12D). In particular, the risk of perinatal mortality within 1 week of diagnosing reversed end-diastolic flow in the umbilical artery of a growth-restricted fetus is so high, close to 50%, that delivery is generally recommended, regardless of the gestational age.10,11,140,156,167-170

Ductus Venosus Doppler The ductus venosus is the short vessel connecting the umbilical vein near its junction with the left portal vein directly to the inferior vena cava. This allows shunting of umbilical venous blood directly to the heart, bypassing the liver. Normal flow in the ductus venosus is antegrade, toward the heart, throughout the cardiac cycle (Fig. 42.13A). Studies have shown that absent or reversed flow (Fig. 42.13B) in the ductus venosus at any time during the cardiac cycle is a sign of cardiovascular instability and is associated with increased morbidity and mortality rates in growth-restricted fetuses.10,11,140,148,150,160 However, these same studies demonstrate poor sensitivities and specificities, and, therefore, the value of ductus venosus Doppler for directing the management of growth-restricted fetuses has not been established.11,140,148,160 Middle Cerebral Artery Doppler Doppler of the middle cerebral artery (MCA) provides information about flow resistance in the fetal brain. For optimal interrogation of the MCA, the Doppler gate should be placed on the middle cerebral artery in the proximal third of the vessel, close to its origin from the circle of Willis. If peak systolic velocity is being measured, the Doppler angle must be zero or angle correction must be used. Normally, flow in the MCA is high resistance, with low diastolic flow (Fig. 42.14A). In the compromised fetus, vessels in the brain vasodilate, a response called “brain sparing,” leading to decreased resistance to blood flow and increased diastolic flow in the MCA. This “brain-sparing” effect can be measured by calculating the resistive index (RI) of the MCA waveform. The RI is considered abnormal when it is less than the fifth percentile for gestational age 148,159,160 (Fig. 42.14B). An abnormal RI in the MCA is associated with perinatal mortality and morbidity, including acidosis at birth, low 5-minute Apgars, and neonatal intracranial hemorrhage.148,159 However, the published studies are inconsistent, and an abnormal MCA Doppler is a poor predictor of adverse outcome in preterm infants. There is no convincing evidence that the use of MCA Doppler for guiding management of growth-restricted fetuses improves outcome.10,148,160,171 Some have advocated using the MCA Doppler in conjunction with umbilical artery Doppler to improve the identification of fetuses at risk for poor outcome. In particular, some have recommended comparing the RI or pulsatility index (PI) in the MCA to the corresponding RI or PI in the umbilical artery in a ratio called the “cerebroplacental ratio” (Fig. 42.15): Cerebroplacental ratio Middle cerebral artery pulsatility index = Umbilical artery pulsatility index

CHAPTER 42  Fetal Measurements

A

C

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B

D

FIG. 42.12  Umbilical Artery Doppler.  (A) Color and spectral Doppler of umbilical artery demonstrating normal flow with systolic to diastolic ratio (S/D) normal at 2.13. (B) Sonogram of term fetus showing Doppler gate on umbilical artery and spectral waveform with elevated S/D of 4.15 due to diminished diastolic flow. (C) Sonogram showing Doppler gate on umbilical artery and spectral waveform below demonstrating absent end-diastolic flow (arrows). (D) Color and spectral Doppler demonstrating reversed end-diastolic flow (arrows).

A

B

FIG. 42.13  Ductus Venosus Doppler.  (A) Color and spectral Doppler of the ductus venosus demonstrating normal flow, toward the heart throughout the cardiac cycle. (B) Color and spectral Doppler of the ductus venosus demonstrating reversed flow (arrows) during part of the cardiac cycle, an abnormal finding.

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A

B

FIG. 42.14  Middle Cerebral Artery Doppler.  (A) Color and spectral Doppler of normal fetal middle cerebral artery with normal resistive index (RI) of 0.89. (B) Color and spectral Doppler of abnormal fetal middle cerebral artery demonstrating abnormally low resistive index (RI) of 0.64 (arrow) as a result of elevated diastolic flow.

A

B

FIG. 42.15  Cerebroplacental Ratio.  Normal cerebroplacental ratio of 1.49, calculated by taking the ratio of A, the resistive index in the middle cerebral artery (0.85) to B, the resistive index in the umbilical artery (0.57).

The cerebroplacental ratio is abnormal if it is less than 1.0.161,163 This ratio takes into account the decreased MCA resistance with “brain sparing” and vasodilation and increased umbilical artery resistance from increased placental resistance associated with placental dysfunction. An abnormal cerebroplacental ratio is associated with increased fetal distress in labor, low cord pH, and high neonatal intensive care admissions.10,140,159,160,163,172 However, the utility of this ratio in the surveillance of the growthrestricted fetus has not been well established.

Summary of Fetal Doppler To date, the only Doppler surveillance study that has been shown to improve outcome in growth-restricted fetuses is umbilical artery Doppler. Although ductus venosus and MCA Doppler have been shown to demonstrate changes with fetal compromise, their use in guiding management of high-risk pregnancies with FGR has not been proven.

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57. Lee W, Deter RL, Ebersole JD, et al. Birth weight prediction by threedimensional ultrasonography: fractional limb volume. J Ultrasound Med. 2001;20(12):1283-1292. 58. Song T. Fetal weight prediction by thigh volume measurement with three-dimensional ultrasonography. Obstet Gynecol. 2000;96(2): 157-161. 59. Schild RL, Fimmers R, Hansmann M. Fetal weight estimation by threedimensional ultrasound. Ultrasound Obstet Gynecol. 2000;16(5): 445-452. 60. Uotila J, Dastidar P, Heinonen T, et al. Magnetic resonance imaging compared to ultrasonography in fetal weight and volume estimation in diabetic and normal pregnancy. Acta Obstet Gynecol Scand. 2000;79(4):255-259. 61. Hatab MR, Zaretsky MV, Alexander JM, Twickler DM. Comparison of fetal biometric values with sonographic and 3D reconstruction MRI in term gestations. AJR Am J Roentgenol. 2008;191(2):340-345. 62. Benacerraf BR, Gelman R, Frigoletto FD. Sonographically estimated fetal weights: accuracy and limitation. Am J Obstet Gynecol. 1988;159(5): 1118-1121. 63. Townsend RR, Filly RA, Callen PW, Laros RK. Factors affecting prenatal sonographic estimation of weight in extremely low birthweight infants. J Ultrasound Med. 1988;7(4):183-187. 64. Barel O, Vaknin Z, Tovbin J, et al. Assessment of the accuracy of multiple sonographic fetal weight estimation formulas: a 10-year experience from a single center. J Ultrasound Med. 2013;32(5):815-823. 65. Kehl S, Schmidt U, Spaich S, et al. What are the limits of accuracy in fetal weight estimation with conventional biometry in two-dimensional ultrasound? A novel postpartum study. Ultrasound Obstet Gynecol. 2012; 39(5):543-548. 66. Scioscia M, Scioscia F, Vimercati A, et al. Estimation of fetal weight by measurement of fetal thigh soft-tissue thickness in the late third trimester. Ultrasound Obstet Gynecol. 2008;31(3):314-320. 67. Hill LM, Breckle R, Wolfgram KR, O’Brien PC. Evaluation of three methods for estimating fetal weight. J Clin Ultrasound. 1986;14(3):171-178. 68. Benson CB, Doubilet PM, Saltzman DH. Sonographic determination of fetal weights in diabetic pregnancies. Am J Obstet Gynecol. 1987;156(2): 441-444. 69. Chauhan SP, Scardo JA, Hendrix NW, et al. Accuracy of sonographically estimated fetal weight with and without oligohydramnios. A case-control study. J Reprod Med. 1999;44(11):969-973. 70. Pineau JC, Grange G, Kapitaniak B, et al. Estimation of fetal weight: accuracy of regression models versus accuracy of ultrasound data. Fetal Diagn Ther. 2008;24(2):140-145. 71. Doubilet PM, Benson CB, Nadel AS, Ringer SA. Improved birth weight table for neonates developed from gestations dated by early ultrasonography. J Ultrasound Med. 1997;16(4):241-249. 72. Brenner WE, Edelman DA, Hendricks CH. A standard of fetal growth for the United States of America. Am J Obstet Gynecol. 1976;126(5): 555-564. 73. Lubchenco LO, Hansman C, Dressler M, Boyd E. Intrauterine growth as estimated from liveborn birth-weight data at 24 to 42 weeks of gestation. Pediatrics. 1963;32:793-800. 74. Gruenwald P. Growth of the human fetus. I. Normal growth and its variation. Am J Obstet Gynecol. 1966;94(8):1112-1119. 75. Thomson AM, Billewicz WZ, Hytten FE. The assessment of fetal growth. Br J Obstet Gynaecol. 1968;75(9):903-916. 76. Hutchins CJ. Delivery of the growth-retarded infant. Obstet Gynecol. 1980;56(6):683-686. 77. Deter RL, Harrist RB, Hadlock FP, Poindexter AN. Longitudinal studies of fetal growth with the use of dynamic image ultrasonography. Am J Obstet Gynecol. 1982;143(5):545-554. 78. Hadlock FP, Harrist RB, Martinez-Poyer J. In utero analysis of fetal growth: a sonographic weight standard. Radiology. 1991;181(1):129-133. 79. Doubilet PM, Benson CB, Wilkins-Haug L, Ringer S. Fetuses subsequently born premature are smaller than gestational age-matched fetuses not born premature. J Ultrasound Med. 2003;22(4):359-363. 80. Lysikiewicz A, Bracero LA, Tejani N. Sonographically estimated fetal weight percentile as a predictor of preterm delivery. J Matern Fetal Med. 2001;10(1):44-47.

81. Mercer BM, Merlino AA, Milluzzi CJ, Moore JJ. Small fetal size before 20 weeks’ gestation: associations with maternal tobacco use, early preterm birth, and low birthweight. Am J Obstet Gynecol. 2008;198(6):673.e1-673. e8. 82. Bukowski R, Gahn D, Denning J, Saade G. Impairment of growth in fetuses destined to deliver preterm. Am J Obstet Gynecol. 2001;185(2):463-467. 83. Secher NJ, Hansen PK, Thomsen BL, Keiding N. Growth retardation in preterm infants. Br J Obstet Gynaecol. 1987;94(2):115-120. 84. Burkhardt T, Schaffer L, Zimmermann R, Kurmanavicius J. Newborn weight charts underestimate the incidence of low birthweight in preterm infants. Am J Obstet Gynecol. 2008;199(2):139.e1-139.e6. 85. Villar J, Altman DG, Purwar M, et al. The objectives, design and implementation of the INTERGROWTH-21st Project. Br J Obstet Gynaecol. 2013;120(Suppl. 2):9-26. 86. Villar J, Ismail LC, Victora CG, et al. International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014;384(9946):857-868. 87. Gardosi J, Chang A, Kalyan B, et al. Customised antenatal growth charts. Lancet. 1992;339(8788):283-287. 88. Gardosi J, Mongelli M, Wilcox M, Chang A. An adjustable fetal weight standard. Ultrasound Obstet Gynecol. 1995;6(3):168-174. 89. de Jong CL, Gardosi J, Dekker GA, et al. Application of a customised birthweight standard in the assessment of perinatal outcome in a high risk population. Br J Obstet Gynaecol. 1998;105(5):531-535. 90. Clausson B, Gardosi J, Francis A, Cnattingius S. Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. Br J Obstet Gynaecol. 2001;108(8):830-834. 91. Figueras F, Figueras J, Meler E, et al. Customised birthweight standards accurately predict perinatal morbidity. Arch Dis Child Fetal Neonatal Ed. 2007;92(4):F277-F280. 92. Alexander GR, Wingate MS, Mor J, Boulet S. Birth outcomes of AsianIndian-Americans. Int J Gynaecol Obstet. 2007;97(3):215-220. 93. Resnik R. One size does not fit all. Am J Obstet Gynecol. 2007;197(3):221-222. 94. Melamed N, Ray JG, Shah PS, et al. Should we use customized fetal growth percentiles in urban Canada? J Obstet Gynaecol Can. 2014;36(2): 164-170. 95. Steer PJ. Possible differences in fetal size by racial origin. Lancet Diabetes Endocrinol. 2014;2(10):766-767. 96. Hutcheon JA, Zhang X, Platt RW, et al. The case against customised birthweight standards. Paediatr Perinat Epidemiol. 2010;25(1):11-16. 97. McCarthy EA, Walker SP. International fetal growth standards: one size fits all. Lancet. 2014;384(9946):835-836. 98. Wong LF, Caughey AB, Nakagawa S, et al. Perinatal outcomes among different Asian-American subgroups. Am J Obstet Gynecol. 2008;199(4):382.e1-382. e6. 99. Villar J, Papageorghiou AT, Pang R, et al. The likeness of fetal growth and newborn size across non-isolated populations in the INTERGROWTH-21st Project: the Fetal Growth Longitudinal Study and Newborn Cross-Sectional Study. Lancet Diabetes Endocrinol. 2014;2(10):781-792. 100. Greenes RA. OBUS: a microcomputer system for measurement, calculation, reporting, and retrieval of obstetric ultrasound examinations. Radiology. 1982;144(4):879-883. 101. Jeanty P. A simple reporting system for obstetrical ultrasonography. J Ultrasound Med. 1985;4(11):591-593. 102. Ott WJ. The design and implementation of a computer-based ultrasound data system. J Ultrasound Med. 1986;5(1):25-32. 103. Ott WJ. The diagnosis of altered fetal growth. Obstet Gynecol Clin North Am. 1988;15(2):237-263. 104. Mintz MC, Landon MB. Sonographic diagnosis of fetal growth disorders. Clin Obstet Gynecol. 1988;31(1):44-52. 105. Landon MB, Mintz MC, Gabbe SG. Sonographic evaluation of fetal abdominal growth: predictor of the large-for-gestational-age infant in pregnancies complicated by diabetes mellitus. Int J Gynaecol Obstet. 1989;30(1):83. 106. Abramowicz JS. Fetal macrosomia. UpToDate. 2015. 107. Boyd ME, Usher RH, McLean FH. Fetal macrosomia: prediction, risks, proposed management. Obstet Gynecol. 1983;61(6):715-722.

CHAPTER 42  Fetal Measurements 108. Modanlou HD, Dorchester WL, Thorosian A, Freeman RK. Macrosomia— maternal, fetal, and neonatal implications. Obstet Gynecol. 1980;55(4): 420-424. 109. Deter RL, Hadlock FP. Use of ultrasound in the detection of macrosomia: a review. J Clin Ultrasound. 1985;13(8):519-524. 110. Golditch IM, Kirkman K. The large fetus. Management and outcome. Obstet Gynecol Surv. 1979;34(2):137-139. 111. Rodriguez MH. Ultrasound evaluation of the postdate pregnancy. Clin Obstet Gynecol. 1989;32(2):257-261. 112. Arias F. Predictability of complications associated with prolongation of pregnancy. Obstet Gynecol. 1987;70(1):101-106. 113. Acker DB, Sachs BP, Friedman EA. Risk factors for shoulder dystocia in the average-weight infant. Obstet Gynecol. 1986;67(5):614-618. 114. Gross SJ, Shime J, Farine D. Shoulder dystocia: predictors and outcome. Am J Obstet Gynecol. 1987;156(2):334-336. 115. Miller JM Jr, Korndorffer Jr FA, Kissling GE, et al. Recognition of the overgrown fetus: in utero ponderal indices. Am J Perinatol. 1987; 4(2):86-89. 116. Miller JM, Korndorffer FA, Gabert HA. Fetal weight estimates in late pregnancy with emphasis on macrosomia. J Clin Ultrasound. 1986;14(6): 437-442. 117. Doubilet PM, Benson CB. Fetal growth disturbances. Semin Roentgenol. 1990;25(4):309-316. 118. Miller J, Korndorffer F, Kissling G, et al. Recognition of the overgrown fetus: in utero ponderal indices. Am J Perinatol. 1987;4(2):86-89. 119. Chamberlain PF, Manning FA, Morrison I, et al. Ultrasound evaluation of amniotic fluid volume. II. The relationship of increased amniotic fluid volume to perinatal outcome. Am J Obstet Gynecol. 1984;150(3):250-254. 120. Benson CB, Coughlin BF, Doubilet PM. Amniotic fluid volume in largefor-gestational-age fetuses of nondiabetic mothers. J Ultrasound Med. 1991;10(3):149-151. 121. Miller Jr JM, Brown HL, Khawli OF, et al. Ultrasonographic identification of the macrosomic fetus. Am J Obstet Gynecol. 1988;159(5):1110-1114. 122. Chauhan SP, West DJ, Scardo JA, et al. Antepartum detection of macrosomic fetus: clinical versus sonographic, including soft-tissue measurements. Obstet Gynecol. 2000;95(5):639-642. 123. Benson CB, Coughlin BF, Doubilet PM. Amniotic fluid volume in largefor-gestational-age fetuses of nondiabetic mothers. J Ultrasound Med. 1991;10(3):149-151. 124. Miller Jr JM, Kissling GA, Brown HL, Gabert HA. Estimated fetal weight: applicability to small- and large-for-gestational-age fetus. J Clin Ultrasound. 1988;16(2):95-97. 125. Basel D, Lederer R, Diamant YZ. Longitudinal ultrasonic biometry of various parameters in fetuses with abnormal growth rate. Acta Obstet Gynecol Scand. 1987;66(2):143-149. 126. Elliott JP, Garite TJ, Freeman RK, et al. Ultrasonic prediction of fetal macrosomia in diabetic patients. Obstet Gynecol. 1982;60(2):159-162. 127. Bochner CJ, Medearis AL, Williams J, et al. Early third-trimester ultrasound screening in gestational diabetes to determine the risk of macrosomia and labor dystocia at term. Am J Obstet Gynecol. 1987;157(3):703-708. 128. Sandmire HF, O’Halloin TJ. Shoulder dystocia: its incidence and associated risk factors. Int J Gynaecol Obstet. 1988;26(1):65-73. 129. Tamura RK, Sabbagha RE, Depp R, et al. Diabetic macrosomia: accuracy of third trimester ultrasound. Obstet Gynecol. 1986;67(6):828-832. 130. Bracero LA, Baxi LV, Rey HR, Yeh MN. Use of ultrasound in antenatal diagnosis of large-for-gestational age infants in diabetic gravid patients. Am J Obstet Gynecol. 1985;152(1):43-47. 131. Benson CB, Doubilet PM, Saltzman DH, et al. Femur length/abdominal circumference ratio. Poor predictor of macrosomic fetuses in diabetic mothers. J Ultrasound Med. 1986;5(3):141-144. 132. Combs CA, Rosenn B, Miodovnik M, Siddiqi TA. Sonographic EFW and macrosomia: is there an optimum formula to predict diabetic fetal macrosomia? J Matern Fetal Med. 2000;9(1):55-61. 133. Colman A, Maharaj D, Hutton J, Tuohy J. Reliability of ultrasound estimation of fetal weight in term singleton pregnancies. N Z Med J. 2006;119(1241): U2146. 134. Lockwood CJ, Weiner S. Assessment of fetal growth. Clin Perinatol. 1986;13(1):3-35.

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135. Lin C. Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol. 1998;92(6):1044-1055. 136. Pilliod RA, Cheng YW, Snowden JM, et al. The risk of intrauterine fetal death in the small-for-gestational-age fetus. Am J Obstet Gynecol. 2012;207(4):318.e1-318.e6. 137. Reed K, Droegmueller W. Intrauterine growth retardation. In: Centrullo CL, Sbarra AJ, editors. The problem-oriented medical record. New York: Plenum; 1984. p. 175-194. 138. Seeds JW. Impaired fetal growth: definition and clinical diagnosis. Obstet Gynecol. 1984;64(3):303-310. 139. Dobson PC, Abell DA, Beischer NA. Mortality and morbidity of fetal growth retardation. Austr N Z J Obstet Gynaecol. 1981;21(2):69-72. 140. Berkley E, Chauhan SP, Abuhamad A. Doppler assessment of the fetus with intrauterine growth restriction. Am J Obstet Gynecol. 2012;206(4): 300-308. 141. Benson CB, Doubilet PM, Saltzman DH. Intrauterine growth retardation: predictive value of US criteria for antenatal diagnosis. Radiology. 1986;160(2):415-417. 142. Benson CB, Boswell SB, Brown DL, et al. Improved prediction of intrauterine growth retardation with use of multiple parameters. Radiology. 1988; 168(1):7-12. 143. Benson CB, Belville JS, Lentini JF, et al. Intrauterine growth retardation: diagnosis based on multiple parameters—a prospective study. Radiology. 1990;177(2):499-502. 144. Doubilet PM, Benson CB. Sonographic evaluation of intrauterine growth retardation. AJR Am J Roentgenol. 1995;164(3):709-717. 145. Manning FA. The fetal biophysical profile. UpToDate. 2015. 146. Manning FA, Platt LD, Sipos L. Antepartum fetal evaluation: development of a fetal biophysical profile. Am J Obstet Gynecol. 1980;136(6): 787-795. 147. Manning FA, Baskett TF, Morrison I, Lange I. Fetal biophysical profile scoring: a prospective study in 1,184 high-risk patients. Am J Obstet Gynecol. 1981;140(3):289-294. 148. Everett TR, Peebles DM. Antenatal tests of fetal wellbeing. Semin Fetal Neonatal Med. 2015;20(3):138-143. 149. Manning FA, Morrison I, Harman CR, et al. Fetal assessment based on fetal biophysical profile scoring: experience in 19,221 referred high-risk pregnancies. II. An analysis of false-negative fetal deaths. Am J Obstet Gynecol. 1987;157(4):880-884. 150. Seravalli V, Baschat AA. A uniform management approach to optimize outcome in fetal growth restriction. Obstet Gynecol Clin North Am. 2015;42(2):275-288. 151. Subtil D, Tiberghien P, Devos P, et al. Immediate and delayed effects of antenatal corticosteroids on fetal heart rate: a randomized trial that compares betamethasone acetate and phosphate, betamethasone phosphate, and dexamethasone. Am J Obstet Gynecol. 2003;188(2):524-531. 152. Mulder EJH, Derks JB, Visser GHA. Antenatal corticosteroid therapy and fetal behaviour: a randomised study of the effects of betamethasone and dexamethasone. Br J Obstet Gynaecol. 1997;104(11):1239-1247. 153. Senat MV, Minoui S, Multon O, et al. Effect of dexamethasone and betamethasone on fetal heart rate variability in preterm labour: a randomised study. Br J Obstet Gynaecol. 1998;105(7):749-755. 154. Rotmensch S, Liberati M, Vishne TH, et al. The effect of betamethasone and dexamethasone on fetal heart rate patterns and biophysical activities: a prospective randomized trial. Acta Obstet Gynecol Scand. 1999; 78(6):493-500. 155. Rotmensch S, Lev S, Kovo M, et al. Effect of betamethasone administration on fetal heart rate tracing: a blinded longitudinal study. Fetal Diagn Ther. 2005;20(5):371-376. 156. Maulik D. Doppler ultrasound of the umbilical artery for fetal surveillance. UpToDate. 2015. 157. Maulik DEV, Mundy D, Heitmann E, Maulik D. Evidence-based approach to umbilical artery Doppler fetal surveillance in high-risk pregnancies: an update. Clin Obstet Gynecol. 2010;53(4):869-878. 158. Dahlbäck C, Pihlsgård M, Gudmundsson S. Abnormal ductus venosus pulsatility index in the absence of concurrent umbilical vein pulsations does not indicate worsening fetal condition. Ultrasound Obstet Gynecol. 2013;42(3):322-328.

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159. Cruz-Martinez R, Figueras F, Hernandez-Andrade E, et al. Changes in myocardial performance index and aortic isthmus and ductus venosus Doppler in term, small-for-gestational age fetuses with normal umbilical artery pulsatility index. Ultrasound Obstet Gynecol. 2011;38(4):400-405. 160. Mone F, McAuliffe FM, Ong S. The clinical application of Doppler ultrasound in obstetrics. Obstet Gynaecol. 2014;17(1):13-19. 161. Copel JA, Bahtiyar MO. A practical approach to fetal growth restriction. Obstet Gynecol. 2014;123(5):1057-1069. 162. Alfirevic Z, Stampalija T, Gyte GML. Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev. 2013;(11):CD007529. 163. DeVore GR. The importance of the cerebroplacental ratio in the evaluation of fetal well-being in SGA and AGA fetuses. Am J Obstet Gynecol. 2015;213(1):5-15. 164. Baschat AA. Venous Doppler for fetal assessment. UpToDate. 2015. 165. Cruz-Martinez R, Tenorio V, Padilla N, et al. Risk of ultrasound-detected neonatal brain abnormalities in intrauterine growth-restricted fetuses born between 28 and 34 weeks’ gestation: relationship with gestational age at birth and fetal Doppler parameters. Ultrasound Obstet Gynecol. 2015;46(4):452-459. 166. Acharya G, Wilsgaard T, Berntsen GKR, et al. Reference ranges for serial measurements of umbilical artery Doppler indices in the second half of pregnancy. Am J Obstet Gynecol. 2005;192(3):937-944.

167. Karsdorp VHM, van Vugt JMG, van Geijn HP, et al. Clinical significance of absent or reversed end diastolic velocity waveforms in umbilical artery. Lancet. 1994;344(8938):1664-1668. 168. Valcamonico A, Danti L, Frusca T, et al. Absent end-diastolic velocity in umbilical artery: risk of neonatal morbidity and brain damage. Am J Obstet Gynecol. 1994;170(3):796-801. 169. Ertan AK, He JP, Tanriverdi HA, et al. Comparison of perinatal outcome in fetuses with reverse or absent enddiastolic flow in the umbilical artery and/or fetal descending aorta. J Perinat Med. 2003;31(4):307-312. 170. Gerber S, Hohlfeld P, Viquerat F, et al. Intrauterine growth restriction and absent or reverse end-diastolic blood flow in umbilical artery (Doppler class II or III): a retrospective study of short- and long-term fetal morbidity and mortality. Eur J Obstet Gynecol Reprod Biol. 2006;126(1):20-26. 171. Fieni S, Gramellini D, Piantelli G. Lack of normalization of middle cerebral artery flow velocity prior to fetal death before the 30th week of gestation: a report of three cases. Ultrasound Obstet Gynecol. 2004;24(4):474-476. 172. Figueras F, Savchev S, Triunfo S, et al. An integrated model with classification criteria to predict small-for-gestational-age fetuses at risk of adverse perinatal outcome. Ultrasound Obstet Gynecol. 2015;45(3):279-285.

CHAPTER

43

 

Sonographic Evaluation of the Placenta Thomas D. Shipp

SUMMARY OF KEY POINTS • The placenta undergoes tremendous development within the first half of pregnancy yet continues to mature and develop during the gestation. • A placenta that lies near or over the internal cervical os is common early in gestation, yet most of these will resolve by the end of pregnancy. Ultrasound, especially transvaginal sonography, is instrumental to determine placental position. • Placenta accreta is increasingly common and ultrasound is vital for its identification, especially in patients at high risk for its development. Sonographic findings most important for identifying placenta accreta are placental lacunae, loss of the placental-myometrial hypoechoic space, abnormalities of the uterine-bladder interface, and color Doppler abnormalities. • Placental infarctions are commonly identified within the placenta, especially in patients at high risk for their

development (e.g., those who have preeclampsia, maternal vascular disease, or thrombophilia). • Abnormalities of placental shape are common, as are differences in location of the placental umbilical cord insertion. • The presence of a vasa previa is associated with increased perinatal morbidity and mortality rates. Vasa previa should be evaluated for all gravidas, especially for those with an increased risk of its development. • Those parturients with abnormal postpartum bleeding should be evaluated for the presence of retained products of conception. Echogenic endometrial masses in these patients strongly suggest the presence of retained products of conception.

CHAPTER OUTLINE PLACENTAL DEVELOPMENT Placental Appearance Placental Size Placental Vascularity and Doppler Ultrasound Amnion-Chorion Separation Elastography PLACENTA PREVIA PLACENTA ACCRETA PLACENTAL ABRUPTION PLACENTAL INFARCTION PLACENTAL MASSES

T

MESENCHYMAL DYSPLASIA OF THE PLACENTA MOLAR GESTATIONS MORPHOLOGIC PLACENTAL ABNORMALITIES Circumvallate Placenta Succenturiate Lobe Bilobed Placenta UMBILICAL CORD Size and Appearance Insertion Into the Placenta

he use of ultrasound to evaluate the placenta is routine among the majority of pregnant American women because they have at least one ultrasound examination during pregnancy. A wide range of pregnancy complications result from abnormal placental development, including preeclampsia, intrauterine growth restriction (IUGR), and abruption. Other placental and umbilical cord abnormalities, such as placenta previa, placenta accreta/increta/percreta, or vasa previa, may cause major maternal and fetal complications, especially if not recognized antenatally. Timely recognition of these abnormalities can lead to improved management of pregnancy and delivery. Thus careful examination

Velamentous and Marginal Cord Insertions Vasa Previa PLACENTA DURING LABOR AND POSTPARTUM Third Stage of Labor Retained Products of Conception CONCLUSION

of the placenta by ultrasound can contribute directly to enhanced patient care and improved outcomes.

PLACENTAL DEVELOPMENT The early developing embryo is surrounded by amnion and chorion. Villi cover the entire surface of the chorion up to about 8 weeks of gestation (Fig. 43.1). The villi, which are the basic structures of the placenta, initially form by 4 or 5 weeks’ gestation. The villi next to the decidua capsularis degenerate, forming the chorion laeve. The villi contiguous with the decidua basalis

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Decidual vessel Maternal decidua

ET

EVT Intervillus space

Floating villus

CT

Anchoring villus

ST

Fetal vessels

FIG. 43.1  Human Placenta Microarchitecture.  Fetal derivatives in the placenta consist of fetal vessels and placental cotyledons (villi). Villi consist of fetal vessels surrounded by cytotrophoblast cells (CT). Covering the cytotrophoblast cells is a multinucleated cellular layer called the syncytiotrophoblast (ST). Anchoring villi are in direct contact with the maternal uterine lining, called the decidua. The decidua is traversed by maternal vasculature. Blood from these vessels empties into the intervillous space and bathes the placental villi. Note that maternal and fetal blood vessels are separated by trophoblast, villous stroma, and fetal vascular endothelium. Cytotrophoblast cells from anchoring villi can change into an invasive phenotype called extravillous cytotrophoblast cells (EVT). EVT invade deeply into the maternal decidua. Some EVT, called endovascular trophoblast cells (ET), embed within the walls of the maternal vasculature. (With permission from Comiskey M, Warner CM, Schust DJ. MHC molecules of the preimplantation embryo and trophoblast. In: Mor G, editor. Immunology of pregnancy. Austin/New York: Landes Bioscience, 2006.)

become the chorion frondosum and later the placenta. The fetal side of the placenta consists of the chorionic plate and chorionic villi. The maternal side consists of the decidua basalis, which opens up into large cisterns, the intervillous spaces. The fetal villi are immersed in maternal blood located in the intervillous spaces. Anchoring villi develop from the chorionic plate.1 These attach to the decidua basalis, holding the placenta in place.2,3 By the end of pregnancy, the villi have a surface area of 12 to 14 square meters.4 This type of placentation, seen in humans and some rodents, is termed hemochorial placentation.

Placental Appearance Sonographically, the placenta in the first and second trimesters is slightly more echogenic than the surrounding myometrium (Fig. 43.2A). The attachment site, or base of the placenta, should be clearly delineated from the underlying myometrium. The edges of the placenta usually have a small sinus, the marginal sinus of the placenta (Fig. 43.2B), where intervillous blood drains into the maternal venous circulation. This area should not be confused with a placental separation. Placental lakes (venous lakes, at least 2 × 2 cm) occur in up to 5% of pregnancies5-10 (Fig. 43.2C, Video 43.1). They represent areas of intervillous spaces devoid of placental villous trees and are seen as hypoechoic structures within the placenta. Moving blood flow can be seen in these areas. They may have irregular shapes or a narrow, cleftlike appearance and may change in appearance over the gestation. Large placental lakes (>5 cm in largest dimension) have been associated with IUGR.10 As the placenta matures, areas of echogenicity within the placenta are visualized (Fig. 43.2D and E). In cases of placental infarction, there may be hypoechoic lesions with echogenic borders.

Placental Size The placenta typically has a round shape with a central umbilical cord insertion, but variability in the shape of the placenta is quite common.11 Placental length is approximately six times its maximal width at 18 to 20 weeks’ gestation. The mean thickness of the placenta in millimeters in the first half of pregnancy closely approximates the gestational age in weeks.12 If the placenta thickness is greater than 4 cm (40 mm) before 24 weeks, an abnormality should be suspected. These abnormalities include ischemic-thrombotic damage, intraplacental hemorrhage, chorioangioma, and fetal hydrops13 (Fig. 43.3, Video 43.2). Given the variable shape of the placenta, calculating a placental volume from two-dimensional (2D) imaging can be complicated. Multiplanar volume calculation involves sequential sections of the placenta at intervals such as 1.0 mm. The margins are manually traced, and a volume is calculated.14 Most current studies appraising the use of three-dimensional (3D) sonography have used the VOCAL (Virtual Organ Computer-aided AnaLysis) method,14 in which the 3D volume in question is rotated and the area of interest traced at its margin, after which a volume is calculated (Fig. 43.4). Placental volume approximation in the first trimester holds promise as an important part of early pregnancy evaluation. Uterine artery Doppler analysis provides limited information regarding IUGR and the effects of maternal hypertension, but it is insufficient as a sole indicator of trophoblast invasion, in part because it is typically performed late in the second trimester. Small placental volumes in the first trimester presage abnormal uterine artery perfusion.15 Uterine artery Doppler ultrasound combined with assessment of placental volume may identify pregnant women at risk for hypertension, abruption, or IUGR.16,17 First-trimester placental volumes correlate with both placental

CHAPTER 43  Sonographic Evaluation of the Placenta

A

C

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B

D

E

FIG. 43.2  Normal Appearance of Placenta.  (A) At 18 weeks, note the uniformly echogenic appearance of the placenta. (B) Note marginal sinus of placenta (arrow), a circumferential venous drainage point into the maternal uterine veins that should not be mistaken for placental separation. (C) Placental lake (arrow) at 20 weeks. See also Video 43.1. (D) Placenta at 32 weeks’ gestation. Note the diffuse placental calcifications. (E) Placenta at 39 weeks’ gestation with defined linear calcifications outlining the placental cotyledons. Note the increasing echogenicity in the placenta as it matures.

weight and birth weight, but they have not been shown to predict the development of preeclampsia.18,19 The first-trimester placental volume quotient (placental volume/crown-rump length) is low for aneuploid fetuses, with 53% having a quotient less than 10th percentile.20 For twins, the placental volume is 83%, and for triplets 76%, that of singletons, for a given gestational age.21 The placenta dramatically increases in size until approximately 15 to 17 weeks’ gestation. From this point, there is a fourfold increase in placental size until delivery, whereas over this same time period the fetus has a 50-fold increase in size.22 Midtrimester placental volume is associated with maternal nutritional status, birth weight, and pregnancy outcome.23-27

Placental Vascularity and Doppler Ultrasound

FIG. 43.3  Thick Placenta in Fetal Hydrops.  The calipers indicate how one would measure the thickness of the placenta. Note the ascites (arrow). See also Video 43.2 for thick placenta in fetus with villitis.

The human placenta is a discoidal, villous, hemochorial structure. Nutrients are exchanged over many villi. Surrounding the villi are the intervillous spaces, which are bathed in maternal blood. The villi are sproutlike projections from the chorionic plate into the intervillous space. The villi are directly connected to the fetal vascular system, whereas the maternal blood emanates from the developing spiral arteries to the intervillous spaces to contact

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FIG. 43.4  Three-Dimensional Assessment of Placental Volume in Second Trimester.

Amniochorionic membrane

Umbilical vein

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Decidua parietalis Chorion

Chorionic plate

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Amnion

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Endometrial Endometrial veins arteries Maternal circulation

FIG. 43.5  Schematic Drawing of Placental Vasculature.

directly the trophoblasts of the villi28 (Fig. 43.5). Maternal blood flow of the intervillous space depends on flow from the spiral arteries. Maternal vascular disease (e.g., hypertension) can directly affect the pregnancy by limiting this blood flow.29 Intervillous blood flow begins early in the first trimester.30-32 Color Doppler ultrasound has been used to detect this intervillous and spiral artery flow by 12 weeks’ gestation, but the flow, if any, that occurs before this time is not well understood.33 Before 12 weeks, the presence of intervillous blood flow by gray-scale imaging may indicate failed pregnancy.34 Color and power Doppler sonography have been used to identify blood flow in intraplacental villous arteries.35 A decrease

in the number of detectable intraplacental villous arteries is associated with IUGR.36 Three-dimensional power Doppler ultrasound provides a better appreciation of placental vascularity and pathophysiology by assessing placental flow and documenting the amount of flow in a given area. Because of its low variability between sampling sites in varied parts of the placenta, 3D imaging may have a future role in assessing flow in high-risk pregnancies (e.g., hypertension, IUGR).37 Recent work by multiple researchers has shown that 3D placental vascularization indices are lower for those with preeclampsia,19 are not aided by the inclusion of pregnancy-associated plasma protein A (PAPP-A) and uterine artery Doppler indices,38 and may be improved with the addition

CHAPTER 43  Sonographic Evaluation of the Placenta of 3D placental volume and computer analysis of placental calcification.39 How well these indices can be used for the prediction of preeclampsia requires further investigation. First-trimester 3D power Doppler placental indices are unable to differentiate between those destined to have growth restriction as compared to normally grown fetuses.40 Recent work in an animal model, however, demonstrating discrimination of maternal and fetal blood flow in the microvasculature of the placenta may allow further insights into placental blood flow and its effects on placental function.41

Amnion-Chorion Separation The amnion normally “fuses” with the chorion early in the second trimester. Failure of the amnion and chorion to fuse after 17 weeks is a rare complication of pregnancy, associated with multiple abnormalities. Previous amniocentesis is a risk factor for amnionchorion separation.42 Associated factors may include IUGR, preterm delivery, oligohydramnios, placental abruption, and Down syndrome43 (Fig. 43.6).

Elastography A preliminary report has attempted to differentiate subchorionic hematoma from placenta previa using elastography.44 More rigorous evaluations have shown that the use of both shear wave and strain elastography of the placenta was different between normal pregnancies and those that developed preeclampsia.45,46 This exciting novel area of placental research offers much promise for the future.

PLACENTA PREVIA The term placenta previa refers to a placenta that is “previous” to the fetus in the birth canal. The incidence at delivery is approximately 0.5% of all pregnancies.47 Bleeding in the second and third trimesters is the hallmark of placenta previa. This bleeding can be life threatening to the mother and fetus. With antenatal detection, expectant management and cesarean delivery,

FIG. 43.6  Chorioamniotic Separation in Second Trimester.  Amnion (short arrow) is separated from the chorion (long arrow).

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both maternal and perinatal mortality rates have decreased over the past 40 years.48,49 Accurate diagnosis of placenta previa is vital to improve the outcome for mother and neonate. The differentiation of placental position has historically been performed by digital assessment of the lower uterine segment and placenta through the cervix. Using this potentially hazardous method of evaluation, placental position was classified as complete placenta previa, partial placenta previa, incomplete placenta previa, marginal placenta previa, low-lying placenta, and placenta distant from the internal cervical os. These classifications do not directly apply to the ultrasound examination of placental position relative to the cervix. The use of ultrasound to evaluate the position of the placenta in the uterus has both improved knowledge of the placenta within the uterus and simplified terminology with respect to placental position (Fig. 43.7). Complete placenta previa describes the situation in which the internal cervical os is totally covered by the placenta. Some differentiate those placentas that have a portion of placental substance that extends over the internal cervical os from those that are centrally placed over the cervix, a so-called central placenta previa. Marginal placenta previa denotes placental tissue at the edge of, or encroaching on, the internal cervical os. A low placenta is one in which the placental edge is within 2 cm, but not covering any portion, of the internal cervical os. The terms incomplete placenta previa and partial placenta previa have no place in the current sonographic assessment of placental position and should be used only by a clinician performing a digital examination when a “double setup” is necessary to determine where the leading edge of the placenta lies. Transabdominal scanning can be used to visualize the internal cervical os and to determine the relation of the placenta to the cervix in most cases. Factors that can adversely affect the visualization of the cervix include prior abdominal surgery, obesity, deep or low position of the fetal head or presenting part, overfilled or underfilled maternal bladder, or uterine contractions. Transvaginal sonography (TVS) is safe50 and accurate in depicting the internal cervical os. The proximity of the cervix to the vaginal probe allows higher-frequency probes to be used, with better resolution and thus better visualization of the internal cervical os. With improved resolution, clinicians can accurately determine the position of the leading placental edge to the internal cervical os. The use of TVS has been shown to change the assessment of the placental location in 25% of cases when the placenta is within 2 cm of the internal cervical os, as identified with transabdominal sonography.51 A leading placental edge greater than 2 cm from the internal cervical os is associated with vaginal delivery, and distances less than 2 cm are associated with bleeding, potentially leading to cesarean delivery.52,53 Although placenta previa can occur in nulliparas, risk factors include number of prior cesarean deliveries (odds ratio: 4.5 for one; 44.9 for four54), increasing parity independent of number of prior cesarean deliveries,55 and increasing maternal age.56 Early in the second trimester, the placenta occupies a relatively large portion of the uterine cavity and often is positioned near the cervix. As the uterus grows, a lesser proportion of placentas are located near the internal cervical os. This relative change in placental position is best understood by the placental migration

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FIG. 43.7  Placental Position.  (A)-(D) Transabdominal sonography (TAS) and (E)-(H) transvaginal sonography (TVS) can be used to determine placental position with respect to the internal os (arrows). If the position is unclear with TAS, TVS should be used. (A) and (E) Complete central placenta previa. (B) and (F) Complete posterior placenta previa. (C) and (G) Marginal placenta previa. (D) and (H) Low placenta. The calipers show the distance from the internal cervical os to the leading placental edge.

theory.57 This theory of “dynamic placentation” suggests that as the uterus develops, the placenta is “drawn away” from the internal cervical os. It is unclear whether the primary mechanism is disproportionate development of the lower uterine segment so that the placenta, although it does not detach from the uterine wall, comes to lie more distant from the internal cervical os. This theory would also be consistent with complete central placenta previas that do not resolve at a rate approaching that of other low-lying placentas, because the expansion of the lower uterine segment would not lead to the resolution of this type of placenta previa. If the placenta overlaps the cervix by less than 2 cm at the end of the second trimester, more than 88% of patients deliver vaginally.58 A rate of migration (in the second and third trimesters) away from the internal os of 3.0 to 5.4 mm per week is also associated with vaginal delivery, whereas a placental-internal os distance of less than 2 cm or a pattern of migration of 0.3 to 0.6 mm weekly are associated with interventional cesarean delivery and a higher rate of peripartum complications.58,59 The prediction of a placenta previa at delivery is best when the placenta overlaps the internal cervical os by 1.4 cm at 10 to 16 weeks’ gestation,60 or 2 cm at 20 to 23 weeks’ gestation.61 Mustafa et al.62 demonstrated that if the placenta overlaps by 2.3 cm at 11 to 14 weeks, the probability of a placenta previa at term is 8%, with a sensitivity of 83% and a specificity of 86%.62 Aside from a complete central placenta previa, given the current data, it is still difficult to predict precisely which patients will have resolution of their low placenta; therefore further ultrasound examinations are required to assess placental position if a low

placenta is identified early in gestation. In a large retrospective study, if the placenta was low (5 mm from a straight line connecting the external and internal os), the cervical length can be either traced or the sum of two straight lines that follow the curve can be used.21,28 Using these standard criteria, the interobserver coefficient of variation can be improved to 3.3%.27 TVS is superior to the TAS technique. Higher-frequency transducers and closer proximity to the structures studied allow for better resolution. Potential complications of TVS include an increased risk of bleeding in the presence of placenta previa,

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induction of uterine activity in women with cervical shortening caused by cervical stimulation, and chorioamnionitis in the presence of ruptured membranes. However, increased risk of chorioamnionitis or neonatal sepsis with TVS after preterm premature rupture of membranes (PPROM) has not been demonstrated.29,30 TVS has also been deemed safe to use in patients with placenta previa with no increased risk for bleeding; however, caution is advised to ensure that the probe is always carefully inserted under real-time visualization.31 To date, TVS assessment of cervical length by three-dimensional sonography has been limited to the development of a normal distribution curve of cervical length through gestation. Overall, mean cervical length appears to be longer than the measurement by traditional two-dimensional scanning. However, there is to be high intra/interobserver variability.32 Currently, there are no reported studies of the relationship between three-dimensional TVS and SPTB prediction.

Technical Limitations and Pitfalls As mentioned previously, one limitation of TAS, especially in advanced gestation, is that the cervix may be obscured by the presenting part, in particular with a cephalic presentation. In addition, a short cervix or empty bladder may reduce the quality of the measurement obtained, whereas a full bladder may artificially elongate the cervix. There are a number of technical limitations and pitfalls associated with TVS of the cervix. Large maternal body habitus can limit visualization. Bowel gas can obscure visualization. A lower uterine segment myometrial contraction, immediately superior to the cervix, may result in a pseudoelongation of the cervix (Fig. 44.6). The classic tips to recognize this appearance is the artificially elongated length of the cervix (>5 cm), the thicker diameter of the “cervix” at the proximal extent, which actually incorporates the lower uterine muscle so that it appears thicker than at the external os. The thickness of the internal and external cervical os should be similar. Lower uterine segment contractions are transient and rarely persist beyond 15 minutes. A second pitfall associated with the lower uterine segment contraction has been termed “pseudodilation” of the cervix. It

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FIG. 44.5  Example of Poor Technique During TVS of Cervix.  (A) Excessive pressure on the cervix with anterior lip appearing thinner than the posterior lip causing false elongation and increased echogenicity of the cervix. (B) Removal of pressure with equal anterior and posterior lips. Calipers measure appropriate cervical length.

CHAPTER 44  Cervical Ultrasound and Preterm Birth

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FIG. 44.6  Uterine Contractions.  (A) TAS longitudinal image shows contraction (*) leading to a falsely elongated cervical canal (calipers), which measures 7.4 cm. (B) After relaxation of the contraction, the cervix (calipers) measures 4.2 cm. P, Placenta. 60

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FIG. 44.7  Pseudodilation Caused by Uterine Contractions.  Transabdominal longitudinal scan shows a lower uterine segment contraction (*) leading to a false appearance of dilated cervical canal. The closed cervix (calipers) measures 3.5 cm.

is caused by a lower uterine segment contraction with partial (Fig. 44.7) or complete approximation of the anterior and posterior myometrium with the resultant false appearance of a “funnel” above the closed cervix. The classic tips to recognize this appearance is the artificially elongated length of the cervix (>5 cm), the normal cervix lying caudal with respect to the pseudodilation, and the transient nature of this appearance.

Normal Cervix Sonographically, the cervix appears as a distinct, soft tissue structure containing midrange echoes. The endocervical canal

FIG. 44.8  Reference Ranges for Cervical Length Across Gestation.  First to 99th percentiles are indicated. (With permission from Salomon LJ, Diaz-Garcia C, Bernard JP, Ville Y. Reference range for cervical length throughout pregnancy: non-parametric LMS-based model applied to a large sample. Ultrasound Obstet Gynecol. 2009;33[4]: 459-464.33)

often appears as an echogenic line surrounded by a hypoechoic zone attributed to the endocervical glands (see Fig. 44.4B). Occasionally, the endocervical canal may appear hypoechoic and minimally dilated along its entire length. Benign nabothian cysts can be seen within the cervical soft tissues. Numerous studies have evaluated cervical length in normal pregnancy. The typical cervix increases its length in the first trimester because of elaboration of the glandular content of the cervix.27 Salomon et al.33 published a reference curve of cervical length through gestation using TVS based on a large sample (Fig. 44.8). Based on this study, at about 20 weeks’ gestation,

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FIG. 44.9  Cervical Length and Risk of Preterm Delivery Percentile Ranking.  Transvaginal ultrasound cervical length percentile rank, at 24 weeks’ gestation, and relative risk of preterm delivery before 35 weeks. (With permission from Iams JD, Goldenberg RL, Meis PJ, et al. The length of the cervix and the risk of spontaneous premature delivery. National Institute of Child Health and Human Development Maternal Fetal Medicine Unit Network. N Engl J Med. 1996;334[9]:567-572.34)

the 10th, 50th, and 90th percentiles of cervical length are 32.3, 41.9, and 50.5 mm, respectively.33 A progressive linear reduction in cervical length occurs over the 10th to 40th week of gestation.

“Short” Cervix With the goal of understanding the relationship between cervical length and SPTB (delivery before 35 weeks’ gestation), in 1996, Iams et al.34 published a prospective, multicenter study in which an unselected general population of women with singleton pregnancies underwent TVS at 24 and 28 weeks’ gestation. Cervical length at both examinations was comparable and normally distributed, with a mean ±SD of 35.2 ± 8.3 mm at 24 weeks and 33.7 ± 8.5 mm at 28 weeks. A correlation between cervical length and the rate of SPTB was determined (Fig. 44.9); if the cervix was less than 26 mm (10th percentile) or less than 13 mm (1st percentile), risk of SPTB was increased by 6.49-fold and 13.99-fold, respectively, compared with the rate of SPTB if the cervix was at the 75th percentile length (40 mm) or greater.34 Based on this landmark study, the definition of a “short cervix” as less than 25 mm (or