Diagnostic Imaging of Child Abuse [3 ed.] 1107010535, 9781107010536

Table of contents :
Half title page
Title page
Copyright page
Dedication
Contents
List of contributors
Editor’s note on the Foreword to the third edition
Foreword to the third edition, Diego Jaramillo
Foreword to the second edition, Clément J. Fauré
Foreword to the first edition, John A. Kirkpatrick, Jr.
Preface
Acknowledgments
List of acronyms
Introduction
Section I Skeletal trauma
1 The skeleton: structure, growth and development, and basis of skeletal injury
2 Skeletal trauma: general considerations
3 Lower extremity trauma
4 Upper extremity trauma
5 Bony thoracic trauma
6 Dating fractures
7 Differential diagnosis I: diseases, dysplasias, and syndromes
8 Differential diagnosis II: disorders of calcium and phosphorus metabolism
9 Differential diagnosis III: osteogenesis imperfecta
10 Differential diagnosis IV: accidental trauma
11 Differential diagnosis V: obstetric trauma
12 Differential diagnosis VI: normal variants
13 Evidence-based radiology and child abuse
14 Skeletal imaging strategies
15 Postmortem skeletal imaging
Section II Abusive head and spinal trauma
Editor’s note
16 Abusive head trauma: clinical, biomechanical, and imaging considerations
17 Abusive head trauma: scalp, subscalp, and cranium
18 Abusive head trauma: extra-axial hemorrhage and nonhemic collections
19 Abusive head trauma: parenchymal injury
20 Abusive head trauma: intracranial imaging strategies
21 Abusive craniocervical junction and spinal trauma
Section III Visceral trauma and miscellaneous abuse and neglect
22 Visceral trauma
23 Miscellaneous forms of abuse and neglect
Section IV Diagnostic imaging of abuse in societal context
24 Psychosocial considerations
25 Child abuse and the law I: general issues for the radiologist
26 Child abuse and the law II: the radiologist in court and fundamental legal issues
27 The radiologist’s response to child abuse
Section V Technical considerations and dosimetry
28 Radiologic image formation: physical principles, technology, and radiation dose considerations
29 The physics and biology of magnetic resonance imaging: medical miracle anyone?
30 Quality assurance and radiographic skeletal survey standards
Index

Citation preview

Diagnostic Imaging of Child Abuse Third Edition

Diagnostic Imaging of Child Abuse

Third Edition Edited by Paul K. Kleinman MD, FAAP Department of Radiology, Boston Children’s Hospital, and Harvard Medical School, Boston, Massachusetts, USA

University Printing House, Cambridge CB2 8BS, United Kingdom Cambridge University Press is part of the University of Cambridge. It furthers the University’s mission by disseminating knowledge in the pursuit of education, learning, and research at the highest international levels of excellence. www.cambridge.org Information on this title: www.cambridge.org/9781107010536 © Paul K. Kleinman 2015 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published: 1987 Second edition: 1998 Third edition: 2015 Printed in the United Kingdom by Bell and Bain Ltd A catalogue record for this publication is available from the British Library Library of Congress Cataloguing in Publication data Kleinman, Paul K., editor. Diagnostic imaging of child abuse / Paul K. Kleinman. – Third edition. p. ; cm. Includes bibliographical references and index. ISBN 978-1-107-01053-6 (Hardback : alk. paper) I. Title. [DNLM: 1. Battered Child Syndrome–diagnosis. 2. Bone and Bones–injuries. 3. Child Abuse. 4. Child. 5. Diagnostic Imaging. 6. Infant. WA 325]

RA1122.5 617.1′0757–dc23 2014046556 ISBN 978-1-107-01053-6 Hardback Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. Every effort has been made in preparing this book to provide accurate and up-to-date information which is in accord with accepted standards and practice at the time of publication. Although case histories are drawn from actual cases, every effort has been made to disguise the identities of the individuals involved. Nevertheless, the authors, editors, and publishers can make no warranties that the information contained herein is totally free from error, not least because clinical standards are constantly changing through research and regulation. The authors, editors, and publishers therefore disclaim all liability for direct or consequential damages resulting from the use of material contained in this book. Readers are strongly advised to pay careful attention to information provided by the manufacturer of any drugs or equipment that they plan to use.

Dedicated to Sandy Marks

Contents List of contributors Editor’s note on the Foreword to the third edition Foreword to the third edition, Diego Jaramillo Foreword to the second edition, Clément J. Fauré Foreword to the first edition, John A. Kirkpatrick, Jr. Preface Acknowledgments List of acronyms Introduction Paul K. Kleinman Section I Skeletal trauma 1 The skeleton: structure, growth and development, and basis of skeletal injury Andrew E. Rosenberg 2 Skeletal trauma: general considerations Paul K. Kleinman, Andrew E. Rosenberg, and Andy Tsai 3 Lower extremity trauma Paul K. Kleinman 4 Upper extremity trauma Paul K. Kleinman 5 Bony thoracic trauma Paul K. Kleinman 6 Dating fractures Paul K. Kleinman and Michele M. Walters 7 Differential diagnosis I: diseases, dysplasias, and syndromes Paul K. Kleinman and Paula W. Brill 8 Differential diagnosis II: disorders of calcium and phosphorus metabolism Ingrid Holm and Jeannette M. Perez-Rossello 9 Differential diagnosis III: osteogenesis imperfecta

10 11 12 13 14 15

Deborah Krakow, Ralph S. Lachman, and Paul K. Kleinman Differential diagnosis IV: accidental trauma Paul K. Kleinman Differential diagnosis V: obstetric trauma Paul K. Kleinman Differential diagnosis VI: normal variants Paul K. Kleinman Evidence-based radiology and child abuse Christopher S. Greeley Skeletal imaging strategies Paul K. Kleinman Postmortem skeletal imaging Paul K. Kleinman

Section II Abusive head and spinal trauma Editor’s note Paul K. Kleinman 16 Abusive head trauma: clinical, biomechanical, and imaging considerations Lori D. Frasier and Brittany Coats 17 Abusive head trauma: scalp, subscalp, and cranium Paul K. Kleinman, Brittany Coats, and V. Michelle Silvera 18 Abusive head trauma: extra-axial hemorrhage and nonhemic collections Gary L. Hedlund 19 Abusive head trauma: parenchymal injury P. Ellen Grant 20 Abusive head trauma: intracranial imaging strategies V. Michelle Silvera, P. Ellen Grant, Gary L. Hedlund, and Paul K. Kleinman 21 Abusive craniocervical junction and spinal trauma Paul K. Kleinman and V. Michelle Silvera Section III Visceral trauma and miscellaneous abuse and neglect 22 Visceral trauma Katherine Nimkin and Paul K. Kleinman 23 Miscellaneous forms of abuse and neglect Paul K. Kleinman

Section IV Diagnostic imaging of abuse in societal context 24 Psychosocial considerations Alice W. Newton and Amy C. Tishelman 25 Child abuse and the law I: general issues for the radiologist Sandeep K. Narang 26 Child abuse and the law II: the radiologist in court and fundamental legal issues Martha Coakley 27 The radiologist’s response to child abuse Paul K. Kleinman Section V Technical considerations and dosimetry 28 Radiologic image formation: physical principles, technology, and radiation dose considerations Andrew Karellas and Srinivasan Vedantham 29 The physics and biology of magnetic resonance imaging: medical miracle anyone? Robert V. Mulkern 30 Quality assurance and radiographic skeletal survey standards Patricia L. Kleinman Index

Contributors Paula W. Brill MD, FAAP Chief of the Division of Pediatric Radiology at the New YorkPresbyterian Hospital-Weill Cornell Center and Professor of Radiology and Pediatrics at Weill Cornell Medical College, New York, New York, USA Martha Coakley JD Former Attorney General of the Commonwealth of Massachusetts, Boston, Massachusetts, USA Brittany Coats PhD Assistant Professor of Mechanical Engineering and Adjunct Assistant Professor of Bioengineering at the University of Utah, Salt Lake City, Utah, USA Lori D. Frasier, MD, FAAP Division Director, Center for the Protection of Children at Penn State Hershey Children’s Hospital and Professor of Pediatrics at Penn State Hershey College of Medicine, Hershey, Pennsylvania, USA P. Ellen Grant MD, MSc Director, Center on Fetal-Neonatal Neuroimaging and Developmental Science Center, Boston Children’s Hospital and Associate Professor of Radiology at Harvard Medical School, Boston, Massachusetts, USA Christopher S. Greeley MD, FAAP Professor of Pediatrics at the Center for Clinical Research and EvidenceBased Medicine, University of Texas Health Science Center at Houston, Houston, Texas, USA Gary L. Hedlund DO Chief of Neuroimaging at the Primary Children’s Medical Center and

Adjunct Professor of Radiology at the University of Utah, Salt Lake City, Utah, USA Ingrid Holm MD, MPH Director of the Phenotype Core of the Program in Genomics at Boston Children’s Hospital and Assistant Professor of Pediatrics at Harvard Medical School, Boston, Massachusetts, USA Andrew Karellas PhD, FAAPM, FACR Director of Radiological Physics at UMass Memorial Health Care and Professor of Radiology at the University of Massachusetts Medical School, Worcester, Massachusetts, USA Patricia L. Kleinman MPH, RT(R)(QM) Radiologic Physics Technology Specialist, Department of Radiology, Boston Children’s Hospital, Boston, Massachusetts, USA Paul K. Kleinman MD, FAAP Division Chief of Musculoskeletal Imaging at Boston Children’s Hospital and Professor of Radiology at Harvard Medical School, Boston, Massachusetts, USA Deborah Krakow MD Professor of Orthopaedic Surgery, Human Genetics and Obstetrics and Gynecology, David Geffen School of Medicine at UCLA, Los Angeles, California, USA Ralph S. Lachman MD Pediatric Radiologist at Harbor/UCLA Medical Center, International Skeletal Dysplasia Registry at Cedars-Sinai Medical Center and Professor of Radiology and Pediatrics at the University of California, Los Angeles School of Medicine, Los Angeles, California, USA Robert V. Mulkern PhD Associate Physicist at the Department of Radiology, Boston Children’s Hospital and Associate Professor of Radiology at Harvard Medical School, Boston, Massachusetts, USA

Sandeep K. Narang MD, JD, FAAP Director, Child Abuse Fellowship at the Division of Child Protection, Department of Pediatrics, CARE Center and Assistant Professor of Pediatrics, University of Texas Health Science Center at Houston, Houston, Texas, USA Alice W. Newton MD, FAAP Medical Director, Child Protection Program, Massachusetts General Hospital and Assistant Professor of Pediatrics at Harvard Medical School, Boston, Massachusetts, USA Katherine Nimkin MD Associate Director of Pediatric Imaging at the Massachusetts General Hospital and Assistant Clinical Professor of Radiology at Harvard Medical School, Boston, Massachusetts, USA Jeannette M. Perez-Rossello MD Staff Pediatric Radiologist at Boston Children’s Hospital and Assistant Professor of Radiology at Harvard Medical School, Boston, Massachusetts, USA Andrew E. Rosenberg MD Director of Anatomic Pathology and Director of Bone and Soft Tissue Pathology at the University of Miami Hospital and Professor of Pathology at the University of Miami Miller School of Medicine, Miami, Florida, USA V. Michelle Silvera MD Staff Pediatric Neuroradiologist at Boston Children’s Hospital and Assistant Professor of Radiology at Harvard Medical School, Boston, Massachusetts, USA Amy C. Tishelman PhD Research Director and Senior Psychologist, Child Protection Program at the Massachusetts General Hospital, and Assistant Professor of Psychology at Harvard Medical School, Boston, Massachusetts, USA Andy Tsai MD, PhD

Staff Pediatric Radiologist at Boston Children’s Hospital and Instructor in Radiology at Harvard Medical School, Boston, Massachusetts, USA Srinivasan Vedantham PhD Department of Radiology at UMass Memorial Health Care and Associate Professor of Radiology at the University of Massachusetts Medical School, Worcester, Massachusetts, USA Michele M. Walters MD Staff Pediatric Radiologist at Boston Children’s Hospital and Instructor in Radiology at Harvard Medical School, Boston, Massachusetts, USA

Editor’s note on the Foreword to the third edition In the 1987 first edition of Diagnostic Imaging of Child Abuse, the Foreword was written by John Kirkpatrick, Radiologist-in-Chief at Boston Children’s Hospital and Professor of Radiology at Harvard Medical School. For me, he was the consummate pediatric radiologist in intellect, spirit, and conduct. A special relationship has existed between North American and European pediatric radiology, and for this reason I asked the eminent French pediatric radiologist Professor Clément Fauré to write the Foreword to the second edition. This highly respected scholar and teacher had a long interest in the subject of child maltreatment and made many significant contributions to the field. I was privileged that this distinguished radiologist agreed to share his recollections and perspectives with us. For the third edition, I sought a gifted and distinguished pediatric radiologist, who like his predecessors garnered both the respect and affections of the radiologic community. The choice was obvious – Diego Jaramillo. No radiologist has contributed more to our understanding of normal bone growth and development. Our interests intersect in a variety of planes, most notably in the response of the physis to traumatic injury. Diego shares many of the remarkable traits of his predecessors in this task and I am in his debt for taking the time from his busy schedule to contribute to this volume. Paul. K. Kleinman MD

Foreword to the third edition The only real voyage of discovery consists not in seeking new landscapes, but in having new eyes. Marcel Proust, In Search of Lost Time Throughout history, humanity has tended either to turn a blind eye on the abuse of children or to deny its existence. Since 1962, when Kempe and Silverman wrote their landmark article on the battered child, the scientific community has developed an increasing awareness of the issue. In recent years, our understanding of the imaging findings in battered children has increased substantially thanks to the two previous editions of the most authoritative book on the subject, Diagnostic Imaging of Child Abuse, by Dr. Paul Kleinman. The book is not just a review of findings in the literature; it is the summation of decades of outstanding research, deep thought and great teaching. In his journey to clarify the nature of the radiologic manifestations of child abuse, Dr. Kleinman now looks at the subject for a third time, with “new eyes.” With this third edition, Dr. Kleinman has taken a large step to increase the depth and extent of what was included in the prior editions. The new edition begins with a chapter about the structure, growth, and development of the skeleton by Professor Andrew Rosenberg, a premier pathologist in the United States. The first two chapters also deal with important concepts about the pathophysiology of skeletal injury, which are fundamental to the understanding of the imaging manifestations of skeletal trauma. The following chapters are divided regionally, dealing with specific findings that are related to the particular bone that is injured. Six chapters address the differential diagnosis of abusive skeletal injury. At a time where there is discussion about the etiology of many radiologic findings, particularly in the metaphysis, this book provides a brilliant guide to differentiating inflicted traumatic findings from many potential mimickers. The chapters on the differentiation from normal variants and other sources of trauma reflect the meticulous research performed by Dr. Kleinman. The

chapter on disorders of calcium and phosphorus metabolism, co-authored by Dr. Ingrid Holm, an expert in metabolic bone disease, and Dr. Jeannette Perez-Rossello, who has studied the subject in great depth, is particularly important. There is a balanced and very well-supported discussion of how the radiologic manifestations of vitamin D deficiency and rickets differ from those of inflicted trauma, which should bring light to current “controversial” issues. Chapters on skeletal dysplasias and osteogenesis imperfecta are authored by some of the best experts in the field. The chapter on evidencebased radiology provides useful information about how to judge the literature and specifically analyze the soundness (or lack thereof) of the diagnosis of “temporary brittle bone disease.” The second part of the book addresses the manifestations of trauma to the head and spine. In multiple chapters by a group of prominent experts in the pediatric central nervous system and biomechanics, there are detailed descriptions of the imaging manifestations of trauma to the scalp and cranium, and to the extra-axial and parenchymal structures. Imaging strategies are discussed in a succinct, practical way, both for the head and the spine. The third part deals with visceral trauma and other important manifestations of abuse and neglect. Section IV is very useful for radiologists, as it clarifies the psychosocial picture as well as the legal considerations and the obligations of the radiologists. The final part is dedicated to technical considerations in radiography, CT, and MRI; and serves as an invaluable reference for the practicing radiologist. In the foreword to the second edition of this book, Professor Clement Fauré said, “Today, of course, the syndrome of the abused and neglected child is generally accepted.” This remains true, but now more than ever it is crucial to expand our knowledge about mechanisms of injury and their manifestations. Those of us dealing with investigations of child abuse will do well by heeding the advice of Hippocrates: “Leave nothing to chance. Overlook nothing. Combine contradictory observations. Allow yourself enough time.” We come closer to the truth by having more data, and by understanding it better. With this invaluable contribution of the third edition, Dr. Paul Kleinman and his co-authors have done society a great service: they have brought us closer to the truth in matters of child abuse.

Diego Jaramillo MD, MPH

Foreword to the second edition “It is not given to everyone to be an orphan,” deplores Poil de Carotte (Carrot Top), hero of a French novel most of us have read. This wretched boy, our French counterpart to the American Huckleberry Finn, was rejected, neglected, and battered by a mother who nonetheless loved her other children. We have also learned that in past centuries, children were inflicted with severe limb injuries to produce permanent deformities that would make them more efficient beggars. But society tended to consider these facts a good subject for novels and did not appreciate their true frequency. Forgotten were the works of Ambroise Tardieu, a French forensic physician, who in 1860 described the injuries he found in infants or children who died of inflicted trauma. Until the 1940s, these lesions often remained undiagnosed, and when a baby was found dead, the diagnosis of natural “sudden infant death” was commonly accepted. Radiology has been used in infants and children since its origins, but images were generally of poor quality, often blurred by patient movement. It was with the introduction of newer x-ray tubes enabling shorter exposure times that pediatric radiology made a quantum leap. This improved radiographic technology led to the discovery in 1946 of what the pediatric radiologist John Caffey MD recognized as inflicted trauma. In France, it took years for this concept of “unrecognized skeletal trauma” to be accepted. As a fellow in pediatric radiology at the Hôpital des Enfants Malades in Paris in the early 1950s, I shared the difficulties encountered by my chief, Jacques Lefebvre, in convincing our clinicians of its occurrence. Having as our bible Caffey’s Pediatric X-Ray Diagnosis, as well as other American publications in pediatric radiology, we were perfectly aware of the “battered child syndrome.” However, when we proposed this diagnosis to our colleagues, we were told we were wrong, mistaken by lesions due to scurvy, rickets, or hereditary (sic) syphilis. When a subdural hematoma was encountered without an associated skull fracture, trauma was unsuspected and the finding was often attributed to pachymeningitis, or to cerebral

collapse secondary to hypovolemic shock. Associated bone lesions of extremities were considered “neurotrophic,” related to central nervous system disorders. Even our great professor of pediatrics, Robert Debré, who later popularized this entity as Silverman’s syndrome, was reluctant at first to accept our conclusions. Why Silverman’s syndrome and not Caffey’s or Kempe’s? I can relate the story. Robert Debré was a great friend of George M. Guest MD, Professor of Pediatrics in Cincinnati. Each time the two met, whether in Paris or Cincinnati, there was an opportunity for case presentations. Professor Debré also sent some of his best pupils each year for residency training in Guest’s department. During one of Debré’s visits to Cincinnati in the early 1950s, Fred N. Silverman MD, at that time the hospital’s pediatric radiologist, presented a case of a “battered child.” After the presentation, Debré told one of his residents who had attended the meeting that he was reluctant to accept Silverman’s diagnosis. One year later in France, at a weekly gathering of Professor Debré and his assistants and pupils, that same resident presented a compelling case of child abuse. After the presentation, Debré’s comment was “But of course, this is a case of Silverman’s syndrome!” remembering the syndrome Fred Silverman had presented in Cincinnati. Hearing this, the audience asked to learn more of Silverman’s “discovery” from their respected teacher. Since that day, child abuse has been known as Silverman’s syndrome in French medical literature. What we had tried to make evident for two or three years was now suddenly accepted. As the French saying goes, “On ne prête qu’aux riches” (Only to the rich is money lent). Where are we in France at the end of the century? Today, of course, the syndrome of the abused and neglected child is generally accepted. It is taught to our medical students, and then more completely explored with our residents in pediatrics, radiology, and orthopedic surgery. But we still face some difficulties – when bone lesions are not evident at first glance and even more so when a diagnosis appears to some observers to contradict the “social status” of the caretakers. By this long preamble I wish to highlight the general assistance that American pediatric radiology has brought its French and other European counterparts. And in this field of child abuse, Paul Kleinman’s book

Diagnostic Imaging of Child Abuse will continue to improve our fund of knowledge. A major contribution from the author is the radiologic and pathologic descriptions of the subtle lesion he calls the “classic metaphyseal lesion” (CML). To familiarize our eyes to its appearance, the book offers a large display of CMLs in several locations and in different stages of evolution. In a similar manner, the chapter devoted to bony thoracic trauma injury is particularly informative, explaining the location of rib fractures according to their mechanisms of injury. This can help in questioning the caretaker about the origin of the rib fractures noted radiographically. This chapter, as well as the others, offers a rich iconography. All the classic bone lesions of the abused child are thoroughly described and illustrated. Bone scintigraphy plays an important role in the early detection of skeletal lesions that are initially undetected radiographically and revealed only by the development of callus some weeks later. Initial scintigraphic data can prevent a defendant’s attorney from convincing the jury that the fractures noted were sustained during the patient’s hospitalization and were therefore due to underlying bone fragility; we have found ourselves involved in such a case. The book also provides an in-depth description of the diseases simulating abuse, particularly osteogenesis imperfecta. The great contribution of cross-sectional imaging modalities is evident when we evaluate craniocephalic or visceral lesions. Indeed, this book covers all that is known regarding the imaging of child abuse at the turn of the century. The last chapters of the book are of paramount interest. They share information about child abuse and the law. Readers will appreciate, as I have, all the pertinent advice offered to the radiologist involved in civil or criminal cases as an expert witness. In such cases, the radiologist is called upon to use his or her expertise to determine whether lesions discovered by imaging can be attributed to a pre-existing disease or clearly point to inflicted trauma. The radiologist is not a judge, however; his or her main concern is the child’s safety. In cases where the child survives, the best we can hope for is the child’s placement in a safe and loving home. What punishment should be given to the abuser is beyond our mission. When the maltreatment results in death, determining whether it is due to the ignorance, irritability, stupidity, or perversity of the caretakers is the domain of social workers and the courts.

Clément J. Fauré

Foreword to the first edition The concept of willful assault upon children by their caretakers is almost incomprehensible. Sometimes the physician needs reassurance that what is seen by physical examination of radiography can be believed. The chapters on the radiologic aspects of child abuse, 2 through 9, present in exquisite detail, with gross microscopic pathologic correlation, the many radiographic findings caused by willful injury to the skeleton and solid organs. The discussion of the incidence and patterns of injury reminds us of the underestimation of the incidence of skeletal injury and that the overall concept of child abuse has been expanded. The discussion of the skeletal survey and the scintigraphic examination of the skeleton shows that each has value – they are more complementary than supplementary. The chapter dealing with the radiologic dating of fractures is important in the diagnosis of the abused child and also has everyday applicability. The pathophysiology of fracture healing is lucidly presented, as is its modification by repetitive trauma. The discussion of trauma to solid viscera and the central nervous system includes the use of computed tomography and mechanisms of injury; for example, mesenteric injury can result from blunt trauma or sudden deceleration. Involvement of the distal colon and rectum is most often caused by sexual abuse. Inflicted abuse seldom injures the spleen, the kidneys, or the lower urinary tract. Dr. Kleinman has had a long and fruitful relationship with his colleagues in pathology. The material derived from autopsies is of interest to both disciplines. The value of postmortem radiographic study and of its correlation to the actual pathologic anatomy is persuasively presented. The differential diagnosis of inflicted skeletal injury is discussed in Chapter 11, followed by a chapter dealing with the legal aspects of child abuse. In the chapter dealing with legal issues, it is stated that “sensitive management of family violence cases requires both medical and legal input.” The radiologist has a role in determining the nature and degree of inflicted injury – information that often can be obtained in no other way. Of further

interest to the radiologist is the discussion concerned with legal consent, medical records, reporting statutes, and procedures relative to service as a witness or expert witness. This is followed by a chapter on psychological considerations associated with abuse that includes the role of the radiologist in the initial detection of skeletal injury, its documentation, and the subsequent support provided for psychological or legal intervention. The last chapter reviews technical considerations in dosimetry and includes a discussion of radiation risks entailed in the examination as well as methods for the reduction of exposure through appropriate selection of equipment, techniques, and the application of clinical judgment. All in all, one can be enthusiastic about this work and thankful to Dr. Kleinman and his co-authors for presenting a cogent examination of the radiologic aspects of child abuse. The radiologist may be the first to note the possibility of an unfortunately common occurrence. John A. Kirkpatrick, Jr. MD

Preface The origins of my interest in the subject of child abuse rest in part with a bizarre incident that occurred during my pediatric residency. The episode began with a middle-of-the-night phone call from a woman who introduced herself as only “Clara.” She spoke in an authoritative and well-polished manner and quickly drew me from my groggy state. Without any apology for waking me, she said my court testimony was required in a child custody trial set to take place the following day. The matter entailed a dispute between estranged parents who were each seeking to gain custody of their children, one of whom was allegedly abused. She indicated that the child had been seen in our acute care clinic by a physician who was not available to testify and so, as I had been assigned to the same clinic, my testimony was required to validate the clinical record of the visit. Because I did not recall seeing the patient and the examining physician was unfamiliar to me, I suggested she seek the assistance of the director of the clinic where the child was seen. She would not relent and explained in further detail the abusive assaults perpetrated by the mother and the vital importance of placing the children with the father. The conversation drew to a close only after I pressed her to explain her special interest in the case. I soon fell back to sleep, and the following morning I wondered if I had dreamt the entire incident. Shortly after morning rounds, I was summoned to the office of the chief of staff and was escorted into a stately wood-paneled board room. Seated around a huge imposing table were the chief of staff, the director of the pediatric clinic, a lawyer, and a number of other unfamiliar individuals. They asked if I had been contacted by anyone requesting my testimony in a current child custody case. I shared with them what I could recall from the prior evening’s telephone conversation and asked them to explain what was going on. They provided me with the details of a custody case presently in court in which child abuse had been alleged and in which the validity of the medical record was being contested. The clinic director held a copy of a page taken

from the child’s medical record that detailed the physical, laboratory, and radiologic findings of one of the children in the custody dispute. The clinical findings read like a page out of Helfer and Kempe’s textbook, The Battered Child Syndrome. The radiologic descriptions could have been taken directly from Caffey’s Pediatric X-Ray Diagnosis and included terms such as “corner fractures” and “bucket handle” lesions. Although much of the terminology was appropriate, the organization of the note, the use of language, and the flow of the narrative clearly indicated that the note had not been written by a physician. The bogus nature of the record was confirmed when it was determined that none of the laboratory studies and x-rays referred to in the note had been performed. As the various elements of the story were pieced together, it became clear that someone had doctored the medical record to support an allegation of maternal child abuse. This was achieved simply by securing hospital progress note forms, entering the false historical, physical, and laboratory data, and bolstering the account with suitable language from appropriate textbook discussions on the subject of child abuse. The papers were then forwarded to the record room and dutifully added to the patient’s existing chart. The true identity of the midnight caller remains a question to this day. However, the father in this case was described to me as a major figure in high New York circles with many important friends, and I suspect the caller was one of them. My scientific interests in the field of child abuse grew from simple intellectual curiosity. In my early years as a pediatric radiologist, I was struck by the unique character of certain skeletal injuries found in cases of abuse, particularly those encountered in young children. One infant had sustained a fatal head injury and also manifested the classic metaphyseal lesions described by one of the fathers of pediatric radiology, John Caffey. Caffey speculated regarding the basic morphologic alterations and their significance, but provided no pathologic basis for his views. When the infant in question died, I called my friend and colleague, Brian Blackbourne, then the Chief Medical Examiner of the Commonwealth of Massachusetts, and asked him if he would be willing to remove the injured bones so that we might examine them further. He resected the injured metaphyseal regions and we subsequently subjected the specimens to high-detail radiography performed by radiologic technologist Patricia Belanger, with the help of physicist Andrew Karellas. To assist in the analysis of the histologic material, we

sought the aid of anatomist Sandy Marks, an expert in bone structure, growth, and repair. The radiologic–histopathologic correlations that grew from these collaborative efforts over the ensuing years have increased our understanding of both the fundamental structural alterations of skeletal injury and the mechanical factors involved in their production. From these studies, our interest expanded to encompass the wide array of inflicted injuries involving the entire skeleton, the viscera, and the central nervous system. The first edition of Diagnostic Imaging of Child Abuse was an attempt to collect these imaging observations in a single detailed resource that also addressed various related technical, social, and legal issues designed to assist in the imaging evaluation of suspected child abuse. In the second edition, published in 1998, additional imaging patterns of abuse and neglect were described. The evolution of cross-sectional imaging techniques offered new perspectives on familiar physical injuries and revealed additional unusual manifestations of child maltreatment. Perhaps the most stunning insights were gained by the application of magnetic resonance imaging to inflicted central nervous system injuries. The broadening of the imaging spectrum and the advances in our understanding of inflicted injuries are reflected in the substantial growth of the core imaging chapters in this third edition. The incorporation of color imagery has enhanced Andrew Rosenberg’s new discussion of the structure, growth, and development of bone as well as the pathologic basis of skeletal injury. Color photomicrographs are also liberally employed in the following chapters complementing the imaging features of various fracture patterns. The first edition contained a single chapter devoted to differential diagnosis. The second expanded the array to four chapters. The differential diagnosis of abuse has gained even greater importance in the medical and legal environments, and the discussion has been expanded to six chapters, with special attention given to metabolic bone disease. Given the advances in our understanding and imaging complexities of abusive head and spinal trauma, an entire section of six chapters has been devoted to the clinical, biomechanical, and imaging features of these often devastating injuries. The imaging of child abuse draws the members of the Radiology team into the larger societal realm in ways that can pose unique challenges for even the most seasoned professional. Alice Newton, a Child Abuse Pediatrician and

Amy Tishelman, a child psychologist working with our Child Protection Team offer special information and advice to imaging professionals on dealing with possible victims of abuse/neglect and their families. In the first of three legal chapters, Sandeep K. Narang MD, JD covers the principal legal requirements in the area of child abuse, with an emphasis on those materials relevant to radiologists. In a revised chapter Martha Coakley JD, former Chief of the Middlesex County Child Abuse Prosecution Unit and Attorney General of the Commonwealth of Massachusetts, familiarizes the reader with the US court system, providing guidance to physicians in negotiating their way through the potentially daunting task of testifying to the details of imaging findings in court. In this edition, I have again offered my personal perspective on the role that radiologists play in assisting investigative and other legal authorities in resolving cases of suspected abuse. Although there is no substitute for actual personal experience, it is hoped that some of my own observations and recommendations may give the reader an idea of how to deal with the judicial system. Finally, Andrew Karellas PhD, Srinivasan Vedantham PhD, and Robert V. Mulkern PhD, provide technical discussions to aid in understanding modern diagnostic imaging examinations. Patricia Kleinman MPH, RT, then defines the role of quality assurance in diagnostic radiology and details the standard skeletal survey examination for suspected child abuse. Because this volume is directed toward a radiologic audience, the reader can be assured that every effort has been made to provide a comprehensive and reliable discussion of the body of knowledge in this specialized field. It is hoped that colleagues in pediatrics, orthopedics, surgery, and other primary care disciplines caring for children may find this text useful in their practices. Professionals in the fields of child protection, law enforcement, and the legal community should also find this work an authoritative resource. As the spectrum of imaging alterations expands, so do the complex issues entailed in the differentiation of child abuse from its imitators. Although a great deal has been learned since Caffey’s original description, there is still much to be discovered, particularly with respect to the biomechanics of inflicted injury. Physicians and other professionals practicing in this field may seek to simplify matters, taking extreme positions that reflect either an overly zealous approach to diagnosing abuse or an unwillingness to consider

abuse in all but the most flagrant cases. The most effective approach to diagnosis is one based on thoughtful and measured acquisition of data that are carefully analyzed in light of one’s knowledge and experience. With the third edition of Diagnostic Imaging of Child Abuse, I have tried to provide a thorough review of the subject and, with the assistance of my esteemed coauthors, equip the reader with the tools to serve the best interests of children. Paul K. Kleinman MD

Acknowledgments Many fine individuals contributed to the first and second editions of Diagnostic Imaging of Child Abuse, and their efforts were acknowledged in those volumes. As with all scientific texts that focus on conditions that we do not fully understand, it is a work-in-progress. Each volume builds upon its predecessor, and thus any expression of gratitude for the current edition must also include those who helped bring the earlier editions to life. I have expressed those appreciations in the prior editions, but wish to again give special praise to my former assistant Kathy Delongchamp, who provided extraordinary clerical and administrative support for both the first and second editions. These exercises take their toll on the family life and test the strength of the bonds that connect us. This project has taken over four years to complete and without the guidance, support, and profound understanding provided by my dear wife Patricia, this most daunting and frustrating of tasks might well have been abandoned long ago. The work not only invaded our home life: the dreaded laptop was with us on the beach, at all our get-aways, and on all forms of transportation – including the sailboat. Her commitment to the care and well-being of children, ever-present in her own distinguished career, has fostered her support, informal and formal (see Chapter 30), for this text. Another strong woman who has shepherded this work from inception to completion is my current administrative assistant, Susan Ivey. Her intellect and unrelenting personal commitment to the goals of this enterprise have ensured that all the material included in the 3rd edition will be of the highest quality. Putting together and maintaining the integrity of the raw materials of this text – reams of pages, thousands of images with countless annotations, innumerable references – as well as keeping track of all the materials submitted by our esteemed, but often idiosyncratic, contributors, is a truly remarkable accomplishment. She shares the credit for any good that comes from this monumental effort. More than ever, I have depended on my contributors to guarantee that we

have delved into all the facets and nuances of the problem – from the microscopic skeletal alterations through the diagnostic imaging of abuse and its mimics – and into the broader societal context with all the vagaries of current medico-legal proceedings. In an environment where we are all more connected to our work and personal time is in short supply, the contributors to this edition have poured their precious time and effort into this project, and to them I also say thank you. Of necessity, the case material illustrated in this book has been drawn from many sources. As with the earlier editions, I have attempted to acknowledge these important contributors; again, special thanks to Mike Thomason for his many interesting and elegantly imaged cases. He is the consummate scholar / clinical radiologist. In an era of bottom-line-driven publishing, a monograph on a subject of great public health importance, but with a focused audience, may not receive attention from publishing houses that is commensurate with the book’s potential value to the community. I wish to thank Deborah Russell, formerly of Cambridge University Press, for believing in this text, and for fostering our collaboration. I also thank the Cambridge University Press in-house team and all their affiliates for their efforts throughout this long journey. This book has been written during my tenure at Boston Children’s Hospital and I thank all my radiology colleagues for their encouragement and support, especially during those chaotic deadline-driven periods. This precious work has been fostered at this remarkable institution and I cannot think of a more suitable place at which to write a text dedicated to the health and well-being of all children. Paul K. Kleinman MD

List of acronyms Acronym

Description

1,25D2

1,25-dihydroxyvitamin D, active form of vitamin D

18F-NaF

PET

Fluorine 18-labeled sodium fluoride PET

25(OH)D-1-alphahydroxylase

25-Hydroxyvitamin D-1-alpha-hydroxylase

25D

25-Hydroxyvitamin D

2D

Two dimensional

2D-FT

2D Fourier transform

3D

Three dimensional

3D-FT

3D Fourier transform

99mTc

Technetium-99m methylene diphosphonate

MDP

AAP

American Academy of Pediatrics

AAPM

American Association of Physicists in Medicine

AccT

Accidental head trauma

ACR

American College of Radiology

ACTH

Adrenocorticotropic hormone

ADC

Apparent diffusion coefficient

AEC

Automatic exposure control

AHIMA

American Health Information Management Association

AHT

Abusive head trauma

AJR

American Journal of Roentgenology

ALL

Acute lymphoblastic leukemia

ALL

Anterior longitudinal ligament

ALT

Alanine aminotransferase

ALTE

Apparent life-threatening event

AML

Acute myelogenous leukemia

AP

Anteroposterior

aSDH

Acute SDH

ASL

Arterial spin labeling

AST

Aspartate aminotransferase

ATP

Adenosine triphosphate

AVF

Arteriovenous fistula

AVM

Arteriovenous malformation

BBB

Blood brain barrier

BESSI

Benign enlargement of the subarachnoid spaces in infancy

BMC

Bone mineral content

BMD

Bone mineral density

BMI

Body mass index

BO

Magnetic field strength

BW

Bandwidth

CAP

Child Abuse Pediatrician

CARES

Child Abuse Reporting Experience Study

CaSR

Calcium-sensing receptor

CAT

Computed axial tomography

CCJ

Costochondral junction

CDC

Centers for Disease Control

CECT

Contrast-enhanced computed tomography

CF

Capital femur

CHESS

Chemical shift selective suppression

CHH

Cartilage hair hypoplasia

CI

Confidence interval

CML

Classic metaphyseal lesion

CNS

Central nervous system

COJ

Chondro-osseous junction

CPR

Cardiopulmonary resuscitation

CPS

Child Protective Services

CPT

Child Protection Team

CR

Computed radiography

CR/DR

Computed radiography/digital radiography

cSDH

Chronic subdural hematoma

CSF

Cerebrospinal fluid

CSVT

Cerebral sinovenous thrombosis

CT

Computed tomography

CTA

CT angiography

CTDI

CT dose index

CTDIvol

Volume CTDI

CTV

CT venography

D2

Vitamin D2 (ergocalciferol)

D3

Vitamin D3 (cholecalciferol)

DAI

Diffuse axonal injury

DBCL

Dural border cell layer

DCE

Dynamic contrast-enhanced

DDH

Developmental dysplasia of the hip

Deff

Effective Dose

DI

Dentinogenesis imperfecta

DIR

Double inversion recovery

DLP

Dose length product

DNA

Deoxyribonucleic acid

DP

Dural venous plexus

DQE

Detective quantum efficiency

DR

Digital radiography

DSA

Digital subtraction angiography

DT

Digital tomosynthesis

DTI

Diffusion tensor imaging

DTPA

Diethyl-triamine-penta-acetic acid

DTT

Diffusion tensor tractography

DWI

Diffusion-weighted imaging

DXA

Dual-energy X-ray absorptiometry

EBM

Evidence-based medicine

EBR

Evidence-based radiology

ECG

Electrocardiogram

ECMO

Extracorporeal membrane oxygenation

ED

Emergency department

EDH

Epidural hemorrhage or hematoma

EI

Exposure indicator

EMR

Electronic medical record

EMS

Emergency Medical Services

EPI

Echo planar imaging

ER

Emergency room

ETE

Effective echo time

18F

Radioactive fluorine-18

F-FDG

2-deoxy-2-fluoro-D-glucose

FA

Fractional anisotropy

FAST

Focused assessment with sonography for trauma

FE

Finite element

FIESTA

Fast imaging employing steady state acquisition

FIRES

Febrile infection-related epilepsy syndrome

FLAIR

Fluid-attenuated inversion recovery

fMRI

Functional MRI

F-PET or 18F-PET or 18F-NaF PET

Fluorine 18-labeled sodium fluoride PET

fps

Frames per second

FS

Fat staturated

FSE

Fast spin echo

FSEIR

Fast SE with inversion recovery

FT

Fourier transform

FTT

Failure to thrive

GA1

Glutaric Aciduria Type 1

GCS

Glasgow Coma Score

GE

Gradient echo

GI

Gastrointestinal

GM-CFU

Granulocytic-macrophage colony-forming unit

GRE

Gradient recalled echo

GT

Greater trochanter

Gy

Gray

1H-MRS

Hydrogen-1 MR spectroscopy

HC

Head circumference

HLH

Hemophagocytic lymphohistiocytosis

HIE

Hypoxic ischemic encephalopathy

HII

Hypoxic ischemic injury

HIPAA

Health Insurance Portability and Accountability Act

HSAN

Hereditary sensory and autonomic neuropathies

HSV

Herpes simplex virus

HU

Hounsfield unit

HUS

Head ultrasound

HVL

Half-value layer

hZPC

Histologic ZPC

ICI

Intracranial injury

ICRP

International Commission on Radiological Protection

ICU

Intensive care unit

IDH

Intradural hematoma

IOS

Interoccipital synchondrosis

IPV

Intimate partner violence

IQ

Intelligence quotient

ISOD

Isolated sulfite oxidase deficiency

ITP

Immune thrombocytopenic purpura

IU

International units

IV

Intravenous

IVC

Inferior vena cava

IVH

Intraventricular hemorrhage

IVP

Intravenous pyelogram

JCAHO

Joint Commission for the Accreditation of Hospital Organizations

J/kg

Joules per kilogram

keV

Kilo electron volts

kVp

Peak kilovoltage

LCH

Langerhans cell histiocytosis

LDH

Lactate dehydrogenase

LP

Lumbar puncture

lp/mm

Line pairs per millimeter

LPO

Left posterior oblique

LSDI

Line scan diffusion imaging

LT

Left

mA

Milliamps

M-CFU

Macrophage colony-forming units

MD

Mean diffusivity

MD

Metaphyseal dysplasias

MDCT

Multi-detector CT

MDP

Methylene diphosphonate

MELAS

Myopathy encephalopathy lactic acidosis and stroke-like episodes

MHE

Multiple hereditary exostoses

MIM

Mendelian Inheritance in Man

MIP

Maximum intensity projection

MIP

Multiplanar reconstruction

MPGR

Multiplanar gradient recalled

MPR

Multiplanar reformation

MR

Magnetic resonance

MRA

MR angiography

MRI

Magnetic resonance imaging

MRS

MR spectroscopy

MRV

MR venogram

MSBP

Munchausen syndrome by proxy

MTF

Modulation transfer function

MVA

Motor vehicle accident

NAA

N-acetylaspartate

NECT

Noncontrast-enhanced CT

NEX

Number of excitations

NF1

Neurofibromatosis type 1

NIH

National Institutes of Health

NMDA

N-methyl-D-aspartate

NMR

Nuclear magnetic resonance

OI

Osteogenesis imperfecta

OMIM

Online Mendelian Inheritance in Man

OPG

Osteoprotegerin

OR

Odds ratio

OSH

Outside hospital

PA

Posteroanterior

PASL

Pulsed arterial spin labeling

PCASL

Pseudo-continuous arterial spin labeling

PCD

Programmed cell death

PCPCS

Pediatric Cerebral Performance Category Scale

PD

Proton density

PET

Positron emission tomography

PHI

Protected health information

PITS

Parent–infant traumatic stress syndrome

PMMA

Polymethyl-methacrylate

PNET

Primitive neuroectodermal tumor

PO

Intake by mouth

PPV

Positive predictive value

PTH

Parathyroid hormone

PTHrP

Placental parathyroid-related protein

QA

Quality assurance

QALY

Quality-adjusted life years

QC

Quality control

QCT

Quantitative CT

rad

Radiation absorbed dose

RANK

Receptor activator for nuclear factor κβ

RANKL

RANK ligand

RBC

Red blood cell

RCT

Randomized controlled trial

RF

Radio-frequency

RH

Retinal hemorrhage

RMRP

RNA component of mitochondrial RNA processing endoribonuclease

RPO

Right posterior oblique

rZPC

Radiologic ZPC

SAH

Subarachnoid hemorrhage

SAS

Subarachnoid space

SBS

Shaken baby syndrome

SCALP

Skin, Connective subcutaneous tissue, Aponeurotica, Loose avascular connective tissue between the aponeurotica and the pericranium, Pericranium

SCIWORA

Spinal cord injury without radiographic abnormality

SD

Subdural

SD

Standard deviation

SDH

Subdural hematoma

SDH

Subdural hemorrhage

SDHy

Subdural hygroma

SE

Spin echo

SH

Salter–Harris

SH

Subperiosteal hemorrhage

SID

Source-to-image distance

SIDS

Sudden infant death syndrome

SIS

Second impact syndrome

SMD

Spondylometaphyseal dysplasias

SMPTE

Society for Motion Picture and Television Engineers

SNR

Signal-to-noise ratio

SPACE

3D T2 turbo spin echo with variable flip angle (Sampling Perfection with Application optimized Contrasts)

SPBC

Subperiosteal bone collar

SPECT

Single photon emission CT

SPGR

Spoiled gradient recalled echo

SPGR FS

Spoiled gradient recalled echo fat-saturated

SPGR MR

Spoiled gradient recalled echo MR

SPNB

Subperiostial new bone

SPNBF

Subperiosteal new bone formation

SPR

Society for Pediatric Radiology

SPR

Superior pubic ramus

SS

Skeletal survey

SSDE

Size-Specific Dose Estimates

SSDHI

Spontaneous subdural hemorrhage in infants

SSFSE

Single-shot fast spin echo

STIR

Short tau inversion recovery

SUID

Sudden unexpected infant death

Sv

Sieverts, a unit designating the equivalent dose

SWI

Susceptibility-weighted imaging

T1WI

T1-weighted image

T2WI

T2-weighted image

“TBBD”

“Temporary brittle bone disease”

TBI

Traumatic brain injury

TE

Echo time

TFT

Thin-film transistor

TI

Inversion time

TNF

Tumor necrosis factor

TOF

Time of flight

TR

Repetition time

TrueFISP

True fast imaging with steady state free precession

TSE

Turbo spin echo

UGI

Upper gastrointestinal

US

Ultrasound

VDR

Vitamin D receptor

VKDB

Vitamin K deficient bleeding

VL

Ventral lateral

VSD

Ventricular septal defect

VWD

Von Willebrand disease

WB-MRI

Whole-body MRI

WI

Weighted image

ZPC

Zone of provisional calcification

Introduction Paul K. Kleinman Diagnostic Imaging of Child Abuse, third edition, ed. Paul K. Kleinman. Published by Cambridge University Press. © Paul K. Kleinman 2015.

Definition of child abuse There is a wide range of views among professionals as to what is an acceptable definition of child abuse. The lack of universally accepted terminology to characterize the fundamental elements of this condition illustrates the difficulty in developing a precise definition. The battered child syndrome seemed to be an apt characterization of the injuries described in early reports; however, the term implies that an infant or child is hit with a fist, foot, or blunt object (1). Some injuries are inflicted in this manner, but most occur by indirect forces that develop as the child is grabbed by the trunk or an extremity, is shaken, slammed, or thrown. Although assailants may be unaware of the ultimate consequences of their actions, the abusive event generally implies a willful assault on a child at the hands of a person entrusted with their care. The term “nonaccidental injury” characterizes the condition by what it is not, rather than by what it is. It requires a reliable definition of what constitutes an accident and implies that if an injury is not due to an accident, it is due to abuse. Some authors link abuse to intentionality (2–4). Intent is often included in legal standards; the notion is a complex one and is not easily applied to the clinical setting by most physicians dealing with traumatic injuries. On occasion, euphemisms and confusing terms such as “trauma-X” are employed to hide the diagnosis from the victim’s family or other caretakers, and such terminology may actually hinder initial contacts with these parties as well as undermine the trust that must be established for optimal intervention and treatment. What constitutes an abusive act is best understood in terms of behavior

patterns that are generally exhibited by reasonable and prudent caretakers (5, 6). Although definitions of abuse built upon this type of standard may create difficulties for state authorities in developing child abuse legislation (4), understanding injuries in terms of the types of forces customarily employed in child rearing is fundamental to assessing the significance of an injury in an actual case. A number of definitions have been offered to characterize child maltreatment – none are perfect and universally applicable to this complex disorder. The Child Abuse Prevention and Treatment Act (CAPTA), (42 U.S.C. §5101), as amended by the CAPTA Reauthorization Act of 2010, retained the existing definition of child abuse and neglect as, at a minimum: Any recent act or failure to act on the part of a parent or caretaker which results in death, serious physical or emotional harm, sexual abuse or exploitation; or an act or failure to act, which presents an imminent risk of serious harm (7, 8). In June 2005, the American Board of Pediatrics accepted a petition to begin a new pediatric subspecialty, certified by the Board (9, 10). Although the leaders of the field who succeeded in winning formal recognition of this discipline acknowledged that there is no perfect term to characterize the condition, the name Child Abuse Pediatrics was chosen for the subspecialty. Although alternative terms will likely persist, particularly outside of North America, “child abuse” and “child maltreatment” are the preferred terms used throughout this text.

Incidence and demographics There is a vast literature on the epidemiology of the global issue of child maltreatment, and the increasing awareness of this public health problem, particularly in developing nations, is encouraging (11, 12). This review will be limited to the epidemiology of the problem in the United States. Based on mandated reports, the US Department of Health and Human Services estimates that 686,000 children were victims of maltreatment in 2012 (13). A 2014 study found that annual rates of confirmed child

maltreatment dramatically understate the cumulative number of children confirmed to be maltreated during childhood (14). Forty-nine states reported a total of 1593 child maltreatment fatalities. Fatalities are concentrated in infants with a death rate for children aged less than 1 year of 18.83 per 100,000, falling relatively rapidly to a rate of 0.98 per 100,000 at age 5 years (13). The National Child Abuse and Neglect Data System (NCANDS) defines “child fatality” as the death of a child caused by an injury resulting from abuse or neglect or where abuse or neglect was a contributing factor. Based on their data, an estimated 1570 children died from abuse and neglect nationally in 2011. This translated to a rate of 2.10 children per 100,000 children in the general population and an average of 4 children dying every day from abuse or neglect (15, 16). Children less than than 1 year of age accounted for 42.4% of fatalities; children less than 4 years of age accounted for four-fifths (81.6%) of fatalities. Childbearing at an early age is strongly associated with infant homicide (17). It is widely acknowledged that there is significant under-reporting of child abuse in general and specifically for child abuse fatalities, and that the actual incidence of abuse and neglect is higher than the official statistics indicate (18–22). The International Classification of Diseases and coding on death certificates are particularly unreliable (19, 23–26). The Fourth National Incidence Study of child abuse and neglect (NIS-4) is the single most comprehensive source of information about the current incidence of child maltreatment in the United States (27). The National Incidence Study (NIS) is a congressionally mandated, periodic effort of the US Department of Health and Human Services. The Keeping Children and Families Safe Act of 2003 (P.L. 108–36) mandated the NIS-4, which collected data in 2005 and 2006. The NIS not only includes children who were investigated by Child Protective Service (CPS) agencies, it also obtains data on other children who were not reported to CPS or who were screened out by CPS without investigation. These additional children were recognized as maltreated by community professionals. Thus, the NIS estimates include both abused and neglected children who are in the official CPS statistics and those who are not. The NIS-4 employed a sentinel survey methodology in which community

professionals or “sentinels” represent all staff of agencies from 122 counties that have contact with children and families (27). The participating sentinels in the NIS-4 were 10,791 professionals in 1094 sentinel agencies. They submitted data forms on any children they encountered who were maltreated during the study data period. The NIS-4 collected 6208 completed data forms from sentinels and 10,667 completed forms on the investigation outcomes and the abuse and neglect involved in cases sampled at participating CPS agencies. The NIS applies definitional standards that include not only those children who have been harmed, but also those whom the reporting sentinel felt were “endangered.” The number of children who experienced Harm Standard physical abuse in the year spanning 2005–2006 was estimated at 323,000 in the NIS-4 compared to an estimated 381,700 from the 1993 NIS-3 data (a 15% decrease in number and a 23% decline in the rate). The number of physically abused children based on the endangerment standard was estimated at 476,600, compared to an estimated 614,100 children in NIS-3 (a 22% decrease in number, a 29% decline in the rate). The significance of this apparent fall in the incidence of physical abuse has been the subject of considerable interest (28, 29). One multicenter study actually shows an increase in pediatric admissions for physical abuse and high-risk traumatic brain injury and has tied them to recent macroeconomic trends (30), while another has shown little effect of the recent recession on the rates of abuse and neglect (31). As with the earlier studies, the NIS-4 found that rates of maltreatment for black children were significantly higher than those for white and Hispanic children; racial, ethnic, and socioeconomic disparities in the reporting and incidence of child abuse are a subject of ongoing interest and study (27, 30, 32–38). It is evident that infants and young children are at substantial risk for serious physical harm from abusive acts, and they constitute the majority of children who die from their inflicted injuries. Skeletal injuries are present in most infant abuse fatalities and the great majority of these fractures are in a healing phase at the time of death (39). Young children may sustain significant skeletal, abdominal, and central nervous system injuries without clinical findings to indicate abuse, and abuse is often not considered, even when clinical features are present to suggest this diagnosis. The prevalence of injuries that have the highest specificity for abuse is greatest in infants and young children (39–43). It is clear from the literature that diagnostic imaging

plays a central role in the evaluation of suspected physical abuse in infants and young children.

Diagnostic imaging of child abuse: past, present, and future Skeletal injury has been a component of child maltreatment with documented cases as early as Ancient Egypt (44). The modern medical concept of child abuse has its origins with Caffey’s seminal description of long bone fractures associated with subdural hematomas (SDHs) (45). He formulated his early concepts regarding the association and the mechanisms of injury of SDHs and inflicted skeletal injury from earlier reports by Snedecor and others (46, 47) and by Ingraham and associates (48, 49). Although his initial report made only a brief mention of the possibility of “intentional ill treatment” of the victims, Caffey expressed the clear conviction in conferences, lectures, and personal communications that the findings which he noted were manifestations of maltreatment by custodians (45, 50, 51). Notably, as early as 1957 he expressed strong opinions regarding the nature of the skeletal findings he characterized as traumatic lesions: The diagnosis of traumatic injury to infants and children is of more than academic interest, especially when the injuries are repeated and when the traumatic origin is denied by parents or other caretakers. The correct early diagnosis of injury may be the only means by which the abused youngsters can be removed from their traumatic environment and their wrongdoers punished. Correct early diagnosis of injury by the radiologist may be lifesaving to some of these otherwise helpless youngsters, or it may prevent permanent crippling injuries to others. Interestingly, he added: Early diagnosis may also prevent or stop unwarranted expensive medical investigations which ultimately prove embarrassing to the attending physician, when the true story of simple trauma becomes known (52).

Silverman played a crucial role in developing the concept of “unrecognized trauma in infants” and acknowledged the important contribution of Ambroise Tardieu in the Rigler lecture of 1971 (50, 53). Ambroise Tardieu, a French physician described the clinical manifestations of inflicted injuries in children in 1860, well before the discovery of x-rays. Silverman advocated the use of the “Syndrome of Ambroise Tardieu” to describe the modern concept of the entity. The contributions of these two authors are embodied in the “Syndrome de Silverman–Ambroise Tardieu,” terminology that was used by some authors as recently as 1994 (54). In the years following Caffey’s 1946 article, many authors expanded the concept of inflicted skeletal injuries and their association with SDHs in children (52, 53, 55–65). In 1962, Kempe collaborated with Silverman and others in a landmark article that developed the notion of the “battered child syndrome,” and brought it to a wide medical audience (1, 66). In the early 1970s, the introduction of the concept of violent shaking greatly enhanced the understanding of the pathology and dynamics of physical assaults on infants (Fig. I.1) (67–69).

Figure I.1 The shaken infant. (Illustrated by Laura Perry MD, based on descriptions by assailants. With permission from Kleinman PK. Diagnostic imaging in infant abuse. Review article. AJR. 1990;155:703–12.) With further developments in radiography and the advent of nuclear imaging, sonography, computed tomography (CT), and magnetic resonance imaging (MRI), a vast array of imaging abnormalities due to abuse and neglect were described. These reports have not only served to catalogue the various manifestations of inflicted injury, but correlations with surgical and autopsy findings have provided valuable insights into the mechanisms responsible for these injuries. Currently, radiologists have a wide range of choices of imaging modalities to evaluate cases of suspected abuse. The results of these imaging examinations often form the basis of a diagnosis of abuse and are frequently offered as evidence in legal cases. Furthermore,

radiologists may play a role in the activities of child fatality review teams (70). It is increasingly recognized that society pays a high economic cost in caring for abused children, as well as those at risk for injury (71, 72). A substantial portion of the hospital expenses relates to diagnostic imaging studies (73–75). The twenty-first century brings with it the hope that a heightened awareness of child maltreatment by professionals and the public at large will spur further interest in defining the entire spectrum of physical alterations and their causal mechanisms. The ultimate reduction in morbidity and mortality from abuse will rest in large part on prevention measures and early detection. An effective public health approach to the problem is predicated on a thorough understanding of the pathologic features and the mechanisms underlying inflicted injuries in infants and children. Diagnostic imaging is fundamental to the acquisition of this knowledge and can play an important role in the formulation of public health policy.

Diagnostic challenges of child abuse Because most forms of domestic abuse tend to be cyclic, there is a high risk of repetitive injury, particularly in infants and young children. A missed diagnosis carries the risk that a child will be subjected to further assaults (76– 82). In infants, these attacks tend to escalate in severity and culminate with life-threatening central nervous system injury (39). Imaging strategies for suspected abuse are, therefore, formulated to minimize the risk of a missed diagnosis. On the other hand, overzealous efforts by professionals who are ill-prepared to differentiate child abuse from other conditions can have a profoundly negative impact on children and their families. To date, general screening programs for physical abuse have had mixed results and efforts to develop valid screening instruments and programs for at-risk children are needed (83). The fundamental role of diagnostic imaging in cases of suspected abuse is much the same as with other medical conditions. The diagnostic process is characterized by gathering facts through appropriate imaging studies, integrating these findings with clinical and laboratory data, consultation with colleagues, and the formulation of a diagnosis based on knowledge and

expertise. This process is predicated on a thorough understanding of the varied manifestations of child abuse and its imitators on modern diagnostic imaging studies.

Organization of the book Skeletal injuries are the most common physical alterations identified on imaging studies in cases of abuse, and certain fractures carry a high diagnostic specificity. The presence of these strong indicators of abuse in cases with nonspecific clinical and imaging findings often provides the level of certainty required to arrive at a secure diagnosis. Section I of this book deals with the imaging features of inflicted skeletal injury, followed by the various differential diagnoses which may be entertained in cases of suspected abuse. The concept of evidence-based medicine (EBM) has been used and abused in discussions of the differential diagnosis of child maltreatment, and Dr. Christopher Greeley’s chapter on EBM in the context of the abused child seeks to sharpen the reader’s focus on how to critically evaluate the relevant literature. The important issue of dating fractures is addressed, providing the parameters of fracture healing with a goal towards defining the strengths and limitations of radiography in the timing of skeletal injury. Current recommended skeletal imaging strategies are provided and the section concludes with a discussion of postmortem skeletal imaging. Section II addresses the all-important field of abusive head and spinal trauma, the leading cause of maltreatment fatalities in infants and young children. Dr. Gary Hedlund heads a team of experts in the clinical, biomechanical, and neuroimaging aspects of inflicted head and spinal injuries. The differential diagnoses and the imaging strategies are woven into these discussions. Section III covers the imaging features of inflicted visceral trauma, including the imaging approach to these usually serious injuries. Miscellaneous forms of abuse and neglect have protean manifestations, and because there is considerable overlap with classic visceral injuries, these topics are considered together. Section IV places diagnostic imaging in a societal context. A presentation of the factors at work during the complex and sensitive interactions among imaging professionals, abused children, and their families sets the stage for a

discussion of the legal issues that arise once care and protection, or criminal proceedings have begun. The section concludes with the author’s perspective on this challenging, and often daunting, subject. Diagnostic imaging is rooted in basic technical, physical, and biologic principles, which must be fully understood to obtain optimal studies to properly identify and characterize imaging alterations. Section V provides the fundamental principles of diagnostic imaging to professionals who may be unfamiliar with these techniques and addresses risk considerations which accompany studies employing ionizing radiation. This section concludes with a discussion of quality assurance. An imaging department may be equipped with modern and sophisticated imaging modalities and staffed by expert pediatric radiologists, but if the imaging chain is of suboptimal quality, radiologic interpretation may be significantly compromised.

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Section I Skeletal trauma

The skeleton: structure, growth and development, and basis of skeletal injury

Chapter 1

Andrew E. Rosenberg Diagnostic Imaging of Child Abuse, third edition, ed. Paul K. Kleinman. Published by Cambridge University Press. © Paul K. Kleinman 2015.

Introduction Skeletal structure and function Bone structure Woven and lamellar bone Cortical bone Cancellous bone Periosteum and perichondrium Vascular and nerve supply Bone cells Osteoblast lineage Osteoclasts Skeletal growth and development: bone formation, growth, modeling, and remodeling Enchondral ossification and growth plate cartilage Intramembranous ossification Modeling and remodeling Sites vulnerable to trauma in developing long bones Summary

Introduction This chapter focuses on the purpose and composition of the skeleton, bones, and bone tissue, and their formation and maturation. Providing the basis for understanding the inherent weaknesses and susceptibility of the immature

infant skeleton to physical injury, this information also builds the foundation for comprehending the morphologic expression of the trauma and the body’s response to the associated tissue damage.

Skeletal structure and function The skeletal system is vital to life. It plays an essential role in mineral metabolism, movement, protection of viscera, endocrine regulation of critical biologic processes (energy metabolism, male phenotype and fertility, ion homeostasis), and the storage and nourishment of hematopoietic marrow. To accommodate these demands the skeletal system is complex and composed of 206 organs, namely, the individual bones of the body, and a variety of different cell and tissue types (Fig. 1.1). Bones are intricate living structures that have the unique capacity to undergo constant remodeling throughout life. This special biology forms the foundation of its growth and development, its ability to change its structure, function, and metabolism in response to biomechanic and systemic requirements, and its remarkable proficiency in repairing itself, often completely, in the setting of skeletal injury (1).

Figure 1.1 Proximal femur from an older child demonstrating the cortex, medullary cavity, growth plates, apophysis, and articular surface. Tan-white and smooth-surfaced, bones are the hardest and strongest structures of the body, being as strong as cast iron but one-third of the weight as a result of their adaptive architecture. Comparatively lightweight, rigid but not brittle, reinforced, generally asymmetric, and hollow, bones are designed to have a relatively high tensile strength, and maximum strength-to-weight ratio. These characteristics are derived from the substance of bones – all are composed of bone tissue – a specialized type of connective tissue that is a unique biphasic blend of inorganic or mineral component – calcium hydroxyapatite – and organic constituents – the cells and the proteins they synthesize.

Bones vary greatly in size and shape and these features form the basis of the classification of individual bones. The most prominent group of bones are tubular, both long and short (Fig. 1.1), and the other types include flat (bilaminar plates) and cuboid bones. Anatomically, tubular bones are further subdivided into the epiphysis, the metaphysis, and the diaphysis (Fig. 1.2) (2). The epiphysis extends from the base of the articular surface to the beginning point of significant narrowing of the bone. The metaphysis embodies the region of bone that displays a prominent reduction in diameter, and the diaphysis or shaft extends from the base of one metaphysis (the point where decrease in bone diameter ceases) to the base of the opposing metaphysis. During growth and development the metaphysis is composed of the cartilaginous growth plate also known as the physis and the adjacent primary and secondary spongiosa and the surrounding cortex. The medical and forensic determination of skeletal age and the prediction of ultimate size utilize the degree of maturation of the physes, the amount and localization of bone ossification, the formation and dimensions of the secondary ossification centers, and the degree and amount of remodeling (see below).

Figure 1.2 Femur from a fetus showing the epiphysis, metaphysis, and diaphysis. Bones are covered externally by a periosteum. The periosteum is anchored to the cortex, which in turn houses the medullary canal that contains variable

amounts of cancellous or trabecular bone, fatty and hematopoietic marrow, blood vessels, and nerves. The quantity and arrangement of cortical and cancellous bone is directly related to the biomechanical requirements of each bone. For example, long bones that are exposed to the largest torsional and load-bearing forces and flat bones that serve a protective function, such as the skull, are composed roughly of 80–100% cortical bone and 0–20% cancellous bone. In contrast, bones that transmit predominately weight-bearing forces, such as the vertebral bodies, consist of 80% cancellous bone and 20% cortical bone. The trabeculae of cancellous bone are arranged according to the lines of stress to which they are exposed.

Bone structure Woven and lamellar bone Bone tissue is categorized into woven and lamellar types based on the organization of its main structural protein – type I collagen fibers. In woven bone, the collagen fibers are arranged in a seemingly haphazard feltwork, while in lamellar bone they are deposited in parallel arrays (Fig. 1.3).

Figure 1.3 Outer portion of cortex composed of lamellar bone (white

arrow) that has superiosteal reactive woven bone (black arrow) on its surface. The type I collagen fibers in the woven bone are oriented in a weave, whereas those in the underlying cortex are arranged in parallel array. The osteocytes in the woven bone are more numerous and larger than those in the lamellar bone. Woven bone is fabricated during periods of rapid bone growth or formation. It composes parts of the developing skeleton during embryogenesis and portions of bones in the growing infant and adolescent. It may also be the predominant type of bone that is formed in a variety of reactive (fracture-callus, infection-involucrum) and neoplastic (Codman’s triangle, matrix of bone-forming neoplasms) conditions. In the adult, woven bone is always pathologic, except at tendoligamentous insertion sites, where small amounts of woven bone are often present. Histologically, woven bone is hypercellular, and the osteocytes and their lacunae are large and appear to be distributed in a haphazard fashion as the long axes of the cells parallel the differing orientation of the neighboring collagen fibers (Fig. 1.3). Overall, this structural organization enables woven bone to resist forces equally in all directions and facilitates rapid formation, mineralization, and resorption. These factors explain why woven bone is weaker, less rigid, and more flexible than lamellar bone. Normally, the entire mature skeleton is composed solely of lamellar bone. In contrast to woven bone, lamellar bone is synthesized more slowly, is less cellular, and the osteocytes and their lacunae are smaller and distributed amongst the regularly oriented collagen lamellae, giving it a more orderly appearance (Fig. 1.3). Since the mineral and collagen fibers are wellorganized and intimately bound to one another, lamellar bone has greater rigidity and tensile strength and less elasticity than woven bone.

Cortical bone Cortical bone is composed of dense compact bone, and its thickness depends on its location and mechanical requirements (Fig. 1.4). Cortices are thickest in regions exposed to large torsional forces, such as the central portion of the diaphysis, and thinnest where the transmission of torsional forces is smallest, as seen adjacent to articular surfaces, within vertebral bodies, and adjacent to

the subperiosteal bone collar (SPBC), which borders the physis (3, 4).

Figure 1.4 Cortical bone is dense and compact; note the foramen for the nutrient artery. Mature cortical bone is composed of three different architectural lamellar patterns: circumferential, concentric, and interstitial (Fig. 1.5). The circumferential lamellae form outer and inner envelopes to the cortex and consist of several subperiosteal and endosteal layers that are oriented parallel to the long axis of the bone. They are the first cortical lamellae to be deposited, and in young individuals comprise almost the entire cortex. As mechanical stresses on the bone increase with age, many of the circumferential lamellae (except for several lamellae just beneath the periosteum and along the endosteum) are replaced by the concentric lamellae of the haversian systems. Haversian systems, or osteons, are initially created by osteoclastic resorption of the circumferential lamellae, and this process usually begins on the endosteal surface of the cortex, and less frequently on the periosteal surface. The accrual of layers of concentric bone over time reduces the diameter of the haversian canal so that in the end it is small and

contains nutritional blood vessels and nerve twigs (Fig. 1.5). Together, these elements define a haversian or osteonal system.

Figure 1.5 Histology of haversian system composed of the canal and its contents, concentric lamellae, osteocytes and the surface lining osteoblasts. The canaliculi containing osteocyte cell processes are prominent. Mature haversian canals are long and cylindrical, range from 25 to 125 μm in diameter (average 50 μm), and are widest nearest the medullary cavity. They form an intricate, branching, spiraling, and interconnecting network that courses throughout the cortex. The number of haversian systems in a particular bone is variable and is determined by age, the amount of mechanical stress and weight the bone is subjected to over time, and other biologic and genetic factors. Filling the spaces between the haversian systems is the interstitial bone. The interstitial lamellae represent the remnants of concentric lamellae of previously formed haversian systems that have become partially destroyed by osteoclastic activity. Interstitial lamellae are irregular, geometric-shaped units of lamellar bone that help “glue”, or anneal haversian systems to one another – this arrangement is important in maintaining cortical integrity. As the bone

is subjected to varying forces and remodeling, newly formed haversian systems replace pre-existing interstitial lamellae and older haversian systems subsequently become newly created interstitial lamellae.

Cancellous bone Cancellous bone is fenestrated, and is situated within the medullary cavity (Figs 1.6, 1.7). It consists of interconnecting plates and struts of trabecular bone, and its total surface area is very large, which facilitates remodeling, and the ability of the skeleton to respond rapidly to the metabolic demands of the body. Bone trabeculae are deposited according to lines of mechanical stress to provide support and distribute large weight-bearing forces along a variety of different pathways. Consequently, cancellous bone is most abundant in the weight-bearing ends of bones, such as the epiphyses and metaphyses of long bones and vertebral bodies, whereas it is present in only small quantities in the mid diaphysis of tubular bones.

Figure 1.6 Cancellous bone is composed of interconnecting plates of trabeculae creating a large surface area for cell activity.

Figure 1.7 Trabeculae composed of the lamellae that are oriented in the same direction as the trabeculae.

Periosteum and perichondrium The periosteum consists of a thin layer of tan-white connective tissue that covers the outer surface of all cortices. Where this layer of tissue overlies cartilage, such as that of the growth plate and adjacent immature epiphysis, it is known as the perichondrium. In children the periosteum is relatively loosely attached to the cortex, whereas in adults it is firmly anchored. The periosteum and perichondrium is constructed of an outer fibrous layer and an inner cellular or cambium (osteogenic) layer and these layers are most apparent during periods of rapid bone growth in children. The cambium layer is composed of fibroblasts, osteo- and chondro-progenitor cells, and developing osteoblasts and chondroblasts (Fig. 1.8). Generally, the number of progenitor cells present depends on the age of the child and the amount of bone cell activity in any particular region; they are especially numerous during periods of active bone formation. In contrast, in adults the periosteum appears largely as a fibrous layer that contains fibroblasts and broad collagen fibers that are continuous with those of the joint capsule, tendons, and muscle fascia. Collagen fibers of tendoligamentous structures pierce the periosteum and become anchored in the bone (Sharpey’s fibers).

Figure 1.8 Fetal periosteum is composed of an outer fibrous layer containing collagen, and an inner cellular region known as the cambium (osteogenic) layer.

Vascular and nerve supply Bones are very vascular and receive their blood supply from three main sources: (a) large nutrient arteries (one to two per bone); (b) metaphyseal and epiphyseal vessels; and (c) periosteal vessels. Nutrient arteries enter long bones in the diaphysis, traverse the cortex through foramina, and divide into ascending and descending branches within the medullary cavity. Smaller branch arteries, arterioles, capillaries, venules, and veins traverse the medullary cavity, nourish the fatty and hematopoietic marrow, and extend into haversian canals, where they supply the inner two-thirds of the cortex. At the ends of growing bones, small arteries give rise to a rich bed of capillary

loops adjacent to the bases of the growth plates. The epiphyseal and metaphyseal vessels access bone through small apertures and provide blood flow to regions of the epiphysis and metaphysis in the mature skeleton and to the secondary centers of ossification during active enchondral ossification. The periosteal vessels are small and are believed to nourish the outer third of the cortex. The venous drainage system of bone is composed of medullary sinusoids that empty into a central venous sinus, which merges with nutrient veins. Nonmyelinated nerves that are derived from the autonomic nervous system are the main source of innervation of bones, and their function is to control blood flow. Larger nerve branches are usually associated with arterial vessels, whereas small groups of fibers can be found adjacent to vessels in haversian systems. Nerves supplying the periosteum contain sensory elements and are responsible for the generation of bone pain.

Bone cells The cells of bone are of different types and include the osteoblast lineage, osteoclast lineage, fibroblasts, adipocytes, smooth muscle cells found in vessel walls, endothelium, axonal processes, Schwann cells, and the hematopoietic elements. The cells responsible for the formation and remodeling of bone tissue are the osteoblast and osteoclast lineages.

Osteoblast lineage Osteoprogenitor cells are derived from tissue-bound mesenchymal stem cells located in the peri-anlage tissue of the fetus, the periosteum, the haversian and volkman canals, and the medullary cavity. Osteoprogenitor cells are primitive committed mesenchymal cells that produce offspring that develop into osteoblasts. The process of osteoblast differentiation and maturation is complex and involves a variety of molecules and signaling pathways (5–14). Morphologically, the osteoprogenitor cells have the features of spindle cells, and do not have any distinguishing histologic characteristics. Osteoblasts are responsible for the production, transport, and arrangement of most of the components of the organic bone matrix (osteoid). Importantly, they also regulate matrix mineralization, and use autocrine and paracrine mechanisms to influence the activity of neighboring bone cells. Osteoblasts

have a lifespan that ranges from months to many years, and their metabolic state is reflected in their morphology. Osteoblasts actively synthesizing bone are polyhedral, have abundant cytoplasm that is in intimate contact with the bone-forming surface, and their nuclei are polarized away from the matrix surface (Fig. 1.9). As their synthetic activity diminishes, they become more attenuated and elongate (spindle-shaped) and remain as a cellular lining covering all bone surfaces (Fig. 1.10).

Figure 1.9 Metabolically active osteoblasts line woven bone trabeculae. The large osteoblasts have abundant cytoplasm and the nuclei tend to be oriented away from the bone-forming surface.

Figure 1.10 Quiescent osteoblasts, known as surface lining cells, covering trabeculae. Osteoblasts enveloped by bone matrix are known as osteocytes (Fig. 1.5), and they are the most numerous cell type of the osteoblast lineage (15). The number, size, shape, and position of osteocytes vary according to the type of bone they inhabit. In woven bone, they are numerous, large, and plump, and are comparatively fewer in number, smaller, and more elongate in lamellar bone (Fig. 1.3). Osteocytes reside in lacunar spaces that house the cell body, nucleus, and surrounding scant cytoplasm. Osteocytes have numerous long and delicate cytoplasmic processes that extend beyond the lacuna, and traverse the matrix through small channels termed canaliculi (Fig. 1.5). This arrangement creates a very large surface area of contact between the osteocyte and the matrix and extracellular fluid that bathes each cell. Osteocyte cell processes connect to those of neighboring osteocytes and to surface osteoblasts via gap junctions. Gap junctions are specialized to facilitate the transfer of small molecules and biologically generated electrical potentials from one cell to another. In this manner, osteocytes communicate with one another and form a complex and integrated network throughout bone tissue. The repertoire of biologic activity possessed by osteocytes helps them

maintain bone tissue, and allows bone to be responsive to the mechanical and metabolic requirements of the body. As mechanosensory cells they translate mechanical forces into biologic activity (16–18). The detection of physical forces stimulates osteocytes to produce and release intercellular messengers that target surface lining cells, precursor cells, and osteoclasts (16–19). These cells, in turn, respond by remodeling the bone regionally as the structure and mass of the bone is altered according to the demands of the external physical environment. Osteocytes also generate and respond to microfluxes in ion concentrations and mediate the exchange of calcium and other ions between the bone matrix and extracellular fluid. In certain conditions, they may even be able to rapidly release calcium and phosphorus from the mineralized matrix by a process termed osteocytic osteolysis, and this manifests histologically as enlarged lacunar spaces (20). Additionally, osteocytes produce fibroblast growth factor-23, a hormone essential in the regulation of serum phosphorus as it modulates the reabsorption of this element in the renal tubule (17).

Osteoclasts Osteoclasts are multinucleated cells responsible for the resorption of bone and cartilage. The matrix they break down must be mineralized for the process to be initiated and completed. Osteoclasts are mobile cells that have a lifespan of only several weeks. By the time they are recognizable by light microscopy they are fully differentiated and biologically active and reside within resorption pits (Howship’s lacunae) formed by their digestion of mineralized bone matrix (Fig. 1.11).

Figure 1.11 Three multinucleated osteoclasts reside in their respective resorption pits, which appear as scallops on the bone surface. Osteoclasts are 40–100 μm in diameter and are polarized, with one portion of the cell membrane intimately attached to the bone and the remainder exposed to the extracellular fluid in its microenvironment. The cytoplasm in the vicinity of the resorbing surface is rich in lysosomes containing a variety of enzymes, and when their contents are released into the resorption pit, the actual process of bone digestion begins. Once osteoclast activity concludes and the cell moves to another targeted site, macrophages migrate into the base of the resorption pit and break down the organic remnants. Osteoclasts are derived from mononuclear, hematopoietic progenitor cells of the granulocytic-macrophage colony-forming (GM-CFU) and macrophage colony-forming units (M-CFU) (21). The process of formation and activation of osteoclasts is controlled by a paracrine system that includes the receptor activator for nuclear factor κβ (RANK), RANK ligand (RANKL), and osteoprotegerin (OPG) (22–25). RANK is a member of the tumor necrosis factor (TNF) family of receptors expressed mainly on cells of macrophage/monocytic lineage, such as preosteoclasts. When this receptor binds its specific ligand (RANKL), which

is expressed by osteoblasts and marrow stromal cells through cell-to-cell contact, a series of signal cascades is activated and osteoclastogenesis is initiated. Another member of the TNF family of receptors that can block the actions of RANKL, is OPG, a soluble protein produced by a number of tissues, including bone, hematopoietic marrow cells, and immune cells. OPG inhibits osteoclastogenesis by acting as a decoy receptor that binds to RANKL, thus blocking the interaction of RANK with RANKL. The communication between bone cells and these molecules permits osteoblasts and stromal cells to control osteoclast development. This ensures the tight coupling of bone formation and resorption vital to the success of the skeletal system and provides a mechanism for a wide variety of biologic mediators (hormones, cytokines, and growth factors) to influence the homeostasis of bone tissue.

Skeletal growth and development: bone formation, growth, modeling, and remodeling Beginning in the embryo until the stage that adult stature is attained, the bones of the body undergo a significant increase in size, refinement of shape, and enhancement of contour. Being rigid, bone cannot grow interstitially and only enlarges by the apposition of new bone on its surface. In contrast, cartilage has the capacity for both appositional and interstitial growth; it increases its substance and enlarges in all dimensions by adding new cells that elaborate freshly synthesized extracellular matrix internally, and on its surfaces. These characteristics of bone and cartilage form the foundation of the two major processes of formation and growth of the skeleton known as enchondral and intramembranous ossification. In enchondral ossification a cartilage model is replaced by bone and in intramembranous ossification bone tissue is formed directly by precursor cells residing in a membranous layer of fibrous tissue.

Enchondral ossification and growth plate cartilage The increase in length of tubular bones in embryos and prepubertal children occurs as growing cartilage is replaced by bone, with the majority of the growth derived from the cartilage anlage (cartilage model of the future bone) and growth plate (physis). The cartilage anlage originally develops in the

early stages of embryogenesis from mesenchymal cells that form cellular condensations at the sites of future bones (26, 27). These mesenchymal cells differentiate into chondrocytes that produce a cartilage model or anlage of the forthcoming bone (Fig. 1.12). This process commences at a specific time for individual bones, and the temporal sequence of anlage formation is the same in all humans. Surrounding the newly formed cartilage anlage are several layers of mesenchymal cells that form the perichondrium, which gives rise to progenitor cells that differentiate into chondrocytes (Fig. 1.12). Subsequently, a specific portion of the perichondrium transforms into periosteum to initiate ossification. This process first occurs in the mid portion of the cartilaginous shaft where mesenchymal stem cells in the perichondrium begin to produce a layer of osteoblasts that deposit a collar of woven mineralized bone on the surface of the cartilage model. This anatomic site is known as the primary center of ossification (Fig. 1.13).

Figure 1.12 Cartilage anlage composed of hyaline cartilage. The perichondrium covers the surface of the structure.

Figure 1.13 Cartilage anlage of a metacarpal containing a primary center of ossification in an early stage of development. In the primary center the chondrocytes are hypertrophied and surrounded peripherally by a very thin layer of woven bone. Concurrently, the chondrocytes in the interior of the cartilaginous shaft that are encased by the periosteal shell of bone begin to hypertrophy and swell (Figs. 1.13, 1.14). Apoptosis ensues and the surrounding matrix mineralizes. During this time the periosteal vessels give rise to a capillary network that, with the aid of osteoclastic (chondroclastic) resorption, penetrates the woven bone of the primary center of ossification into the mineralized cartilage. The capillaries are the precursors to the future nutrient vessels and are accompanied by pluripotent mesenchymal cells that give rise to immature osteoprogenitor and osteoclast progenitor cells.

Figure 1.14 Primary center of ossification that has recently formed. A delicate layer of bone rimmed by osteoblasts covers the central region of hypertrophied chondrocytes. Osteoclasts derived from this tissue continue to bore into the cartilaginous core of the bone leaving residual longitudinally oriented struts of matrix. These bars of cartilage act as scaffolding for newly formed bone deposited by osteoblasts originating from mesenchymal stem cells. Composed of a central cartilaginous core covered by a layer of woven bone, these first trabeculae form the primary spongiosa. Progressive digestion of cartilage creates spaces that coalesce and form the medullary cavity (Fig. 1.15). The medullary cavity is initially filled with loose connective tissue, but eventually becomes occupied by varying amounts of fat and hematopoietic elements. This complex process of cartilage replacement by bone progresses toward both ends as the bone lengthens.

Figure 1.15 Well-formed primary center of ossification moving towards both ends of the bones creating a medullary cavity. In most long bones, a similar process develops subsequently in the epiphysis, and this region is known as the secondary center of ossification (Fig. 1.16). In the secondary center of ossification the maturation and replacement of the cartilage anlage is identical to that which occurs in the diaphysis, except that the maturation proceeds from the center centrifugally, toward the periphery. This means that the growing area of the secondary center is, at first, a sphere. Continual growth of the primary and secondary centers of ossification results in the mergence of their reserve zones. As this occurs, a horizontal plate of bone is deposited along the base of the secondary center, which demarcates it from the primary center of ossification; henceforth, the centrifugal growth of the epiphysis becomes hemispheric. The cartilage located at the base of the true articular cartilage is responsible for progressive epiphyseal enlargement, and it has the architectural organization of growth plate cartilage. Variation in the subarticular growth results in concordance of the shapes of the ends of articulating bones. The epiphysis receives its nutrition primarily from blood vessels within the bone and its adjacent periosteum, whereas the true articular cartilage is nourished by synovial fluid.

Figure 1.16 Secondary center of ossification has developed in the epiphysis. Growth is occurring in a centrifugal fashion. A secondary-like center of ossification also appears in the apophyseal cartilage, located on the surface of the bone (Fig. 1.1). It is responsible for the formation of apophyseal bone – some examples are the iliac crests, the greater and lesser trochanters of the femur, and the humeral and tibial tuberosities. Once the plate of bone that separates the secondary and primary centers of ossification from one another is deposited, the final form of the growth plate is attained. The periphery of the physis is encircled by perichondrium known as the ring of Lacroix and it merges with the periosteum adjacent to the metaphysis and with the perichondrium that surrounds the epiphysis (Fig. 1.17) (28). This structure helps protect against injury and provides precursor cells for lateral expansion of the growth plate. The anatomic zone that extends from the junction of the epiphyseal cartilage and the reserve zone of the growth plate to the junction of the proliferative and hypertrophic zone, where there is frequently a subtle increase in diameter of the physis, is called “the groove of Ranvier” (Fig. 1.17) (3, 26). The appearance of the groove

varies according to the specific growth plate anatomic region.

Figure 1.17 Perichondrium extends from the epiphysis to the base of the growth plate where it merges with the periosteum. The portion that spans the growth plate is known as the ring of Lacroix and beneath it is the SPBC. The anatomic zone that extends from the junction of the epiphyseal cartilage and the reserve zone of the growth plate to the junction of the proliferative and hypertrophic zone, where there is frequently a subtle increase in diameter of the physis, is called “the groove of Ranvier.” The perichondrium adjacent to the distal portion of the growth plate deposits an encompassing rim of bone known as the subperiosteal bone collar (SPBC) (Fig. 1.18) (3). The length of the SPBC is variable; in one study of a 3-month-old infant the lateral SPBC of the distal tibia measured 2.5 mm and medially it was 1.7 mm long (29). The SPBC acts as a lateral buttress providing mechanic support to the physis and often has a distinct step-off with the obliquely oriented metaphyseal cortex with which it is in contiguity (3, 4, 30, 31). Radiographic visualization of the SPBC is a normal finding in

children between the ages of one month and two years (3). The natural stepoff contour at its junction with the metaphyseal cortex should not be mistaken for a fracture; sometimes it may appear as a small bony spur that hugs the periphery of the growth plate (32).

Figure 1.18 Magnified region of Fig. 1.17. The SPBC forms beneath the periosteum and borders the lateral aspect of the growth plate that supports it. The SPBC merges with the adjacent metaphyseal cortex. The growth plate with its inherent chondrocyte proliferation, matrix elaboration, and hypertrophy in the direction of bone growth are the primary determinants of linear bone enlargement (2). This process is coordinated, and tightly regulated by secreted growth factors (Table 1.1) that stimulate chondrocyte-specific transcription factors (SOX9, GLI2/2, and RUNX2), and systemic hormones (Table 1.2), all of which interact to orchestrate and ensure the continuous elongation and eventual closure of the physis (2, 26, 33–37). Table 1.1

Autocrine and paracrine growth factors that regulate the

growth plate Insulin-like growth factor 1 and 2 Indian hedgehog WNT Bone morphogenic proteins Fibroblast growth factors Vascular endothelial growth factor C-type naturietic peptide Transforming growth factor beta Glycosylphosphatidylinositol Table 1.2 Systemic hormones that regulate the growth plate Growth hormone Thyroid hormone Parathyroid hormone-related protein Estrogen Testosterone Glucocorticoids

In the growth plate the chondrocytes are arranged in merging regions that correspond to different stages of chondrocyte proliferation and maturation (Fig. 1.19). As the cells pass through different stages of their lifespan they do not literally move within the matrix but mature in the position they occupy when first formed. The stages of maturation are reflected in their morphology and these features form the basis of their division into different zones including: (a) a region of resting or reserve chondrocytes located nearest the ends of the bone; (b) a region of proliferating chondrocytes that become arranged in spiral columns; (c) a region of chondrocyte hypertrophy; (d) a region of chondrocyte apoptotic necrosis and matrix mineralization; and (e) a region of cartilage resorption by osteoclasts.

Figure 1.19 Well-formed growth plate extending from the superior aspect of the zone of proliferation and including the zones of hypertrophy and

mineralization. The primary spongiosa are in continuity with the base of the plate. The chondrocytes in the reserve zone are relatively small, round, or oval, surrounded by abundant matrix, and those at its base give rise to those that form the zone of proliferation. The chondrocytes in the zone of proliferation are flattened, undergo cell division, become arranged in spiral columns, and elaborate extracellular matrix (26). In the zone of hypertrophy the chondrocytes enlarge with the cytoplasmic volume increasing 10 times (26), resulting in a transverse diameter of up to 30 μm, and the cells model the surrounding matrix as they increase in size (Fig. 1.20) (2). In the zone of mineralization or calcifying cartilage (sometimes considered a sub-region of the hypertrophic zone), the chondrocytes secrete matrix vesicles that are derived from the cell membrane, and they control mineralization of the surrounding extracellular matrix (2, 26, 38). Three to five longitudinally oriented chondrocytes are associated with the calcified matrix, and this area measures approximately 90–150 μm in length (39). This mineralized region of the physis has also been designated the histologic zone of provisional calcification (hZPC) (40). As the matrix mineralizes the chondrocytes undergo rapid necrosis in the last row of lacunae before the ossification front. This process is associated with the release of cytokines, which attracts the ingrowth of endothelial-lined blood vessels and osteoclasts that tunnel into the mineralized matrix, digesting the transverse septae of matrix that separates the chondrocytes from one another (Fig. 1.21). As a result, the vertically oriented intercolumnar struts of mineralized cartilage remain (2, 34, 35); their orientation is determined by the pre-existing columnar arrangement of the chondrocytes in the proliferative and hypertrophied zones and parallels the long axis of the bone (Figs 1.19–1.21). These struts of cartilage become the scaffolding for newly deposited bone.

Figure 1.20 Undecalcified section of the base of the growth plate. The zone of hypertrophy contains enlarged chondrocytes and merges with the zone of mineralization in which the intervening cartilage matrix is calcified and appears dark purple in this micrograph. Osteoclasts resorb portions of cartilage leaving behind struts that act as the scaffolding for osteoblasts, which deposit newly formed bone that is pink in this image. The structures that contain the cartilage cores covered by bony surfaces adjacent to the growth plate are known as the primary spongiosa.

Figure 1.21 Decalcified section of the base of the growth plate showing osteoclasts resorbing portions of the zone of mineralization. This process is vital for the formation of the primary spongiosa. The amount of marrow space surrounding the primary spongiosa is limited in quantity. In a growing long bone the rate of resorption of mineralized cartilage at the chondro-osseous junction (COJ) is balanced by the rate of chondrocyte proliferation in the zone of proliferation. Studies in the rat have shown that chondrocytes spend an average of 4 days in the proliferating zone and at least 48 hours in the zone of hypertrophy (41). The analogous time course in humans is unknown, but experimental studies have shown that up to eight chondrocytes in an individual column of chondrocytes undergo necrosis per day in rapidly growing rat bones (42), and that five or six die per day in fourweek-old pigs (41). Growth of bones in humans and pigs are known to be similar to one another; therefore, it is reasonable to estimate that in newborn humans 4–7 chondrocytes undergo necrosis per day per column of chondrocytes. Studies have found that in the costochondral junction (CCJ) of

newborn infants there are 12.6 ± 1.0 chondrocytes per column, and of these 39.6 ± 6.9% are proliferating chondrocytes, and that the number of chondrocytes per column decreases with age (43). The rate of growth differs for each physis and is greatest in the growth plate of the distal femur, followed by that of the proximal tibia. Generally, the faster the growth rate of the physis, the greater the contribution of growth is derived from cell hypertrophy and the smaller the contribution is from matrix synthesis (35). In diseases in which mineralization of the cartilage is delayed (e.g., rickets), removal of the cartilage is impaired, and the zone of hypertrophy becomes massively and irregularly thickened. While most tubular long bones have two epiphyseal growth plates, other bones (such as the ribs and some of the phalanges, carpals, tarsals, metacarpals, and metatarsals) have only a single physis. Once enchondral ossification is underway in the growth plate, the primary spongiosa becomes well developed and measures approximately 250 µm in longitudinal dimension (Figs. 1.19–1.21) (39). It is estimated that 60% of the zone of calcified cartilage is resorbed by osteoclasts and 40% is preserved in the form of the cartilage cores of the primary spongiosa (44, 45). The fact that these calcified cartilage cores are in continuity with the zone of calcification of the growth plate which interdigitates and merges with the remaining cartilage mass of the growth plate is thought to help protect the growth plate from side slippage (46). The marrow spaces between the individual newly formed trabeculae of the primary spongiosa are relatively limited in quantity (Figs 1.19–1.21) and this impacts the radiographic appearance of this anatomic region. For it is mainly the combination of the mineralized cartilage in the primary spongiosa and the adjacent zone of mineralization of the growth plate that produces the discrete homogeneous opacity along the COJ known as the radiologic ZPC (rZPC) (Fig. 1.22) (40). The rZPC has been measured to be 416 µm long by high-resolution micro-CT or less than 1 mm in length by plain radiography (29, 47). This contrasts with the hZPC dimension of 118 µm. The discordant radiologic and histologic dimensions of the ZPC have been studied in depth in fetal piglets (40).

Figure 1.22 Micro-CT with histologic correlate of the region of the left distal tibial COJ. Composite showing the histology of the lateral half of the tibia as well as the coronal micro-CT reformatted image of the medial half of the bone illustrating the spatial relationship of the physis and the rZPC. Note the rZPC corresponds histologically to the densely staining cartilage rich region of the metaphyseal primary spongiosa (curved arrow). Low power photomicrograph of the boxed area demonstrates the SPBC and the rZPC spatially localized in the histologic section. (Reprinted with permission from Tsai A, McDonald AG, Rosenberg AE, Gupta R, Kleinman PK. Highresolution CT with histopathologic correlates of the classic metaphyseal lesion of infant abuse. Pediatr Radiol. 2014;44(2):124–40.) The fate of the primary spongiosa is either complete osteoclastic resorption or continued deposition of bone on their surfaces while the cartilage is being resorbed (39). These growing trabeculae are known as the secondary spongiosa, and they are comparatively larger in size and fewer in number, and there is an associated increase in the volume of the intervening marrow space. The region that encompasses the relatively abrupt change from the primary to secondary spongiosa is the trabecular transition zone (Fig. 1.23) (29, 40).

Figure 1.23 Histologic correlate of rZPC showing the region of the COJ. Note the sharp transition in density and thickness of the longitudinal bony trabeculae within the metaphysis (dashed line), which corresponds spatially to the metaphyseal margin of the rZPC in the trabecular transition zone. (Reprinted with permission from Tsai A, McDonald AG, Rosenberg AE, Gupta R, Kleinman PK. High-resolution CT with histopathologic correlates of the classic metaphyseal lesion of infant abuse. Pediatr Radiol. 2014;44(2):124–40.) Dramatic changes also occur in the cortex during this time period of rapid growth. Increase in bone diameter is accompanied by subperiosteal bone deposition and bone resorption along the endosteum so that the cortical thickness remains proportionally uniform and the medullary cavity enlarges. The bone that first forms the cortex is woven in nature; but within the first several years of life, the fabricated bone is lamellar in architecture. Variation in the rate of formation and resorption alters the shape of the bone, and this process is most pronounced in the region just distal to the base of the growth plate, known as the “cut back” zone. The “cut back” zone, which forms the metaphysis, contains numerous subperiosteal osteoclasts that reduce the diameter of the bone to that of the diaphysis, and this results in “funnelization” of the bone. The metaphysis is defined as the widened end of a long bone, situated between the physis and the diaphysis (Fig. 1.2). This region contains

abundant trabecular bone composed of the primary and secondary spongiosa in children and mature lamellar trabeculae in the adult. The demarcation between the end of the physis and the beginning of the metaphysis is defined as the last intact transverse septum along the base of each physeal cartilage cell column. In contrast, the demarcation between the metaphysis and the diaphysis is less discrete, corresponding roughly to where the funneling of the metaphysis ceases. The cortex of the metaphysis is thin relative to that of the diaphysis. In the diaphysis, the cortical thickness is maintained or increases by appositional new bone formation. During growth and development, the diameter of the diaphysis continues to enlarge and in specific sites becomes asymmetric. This process is dynamic and responsive to mechanical forces, and not only determines the eventual diameter of the bone, but controls the thickness and contour of the cortex, and the arrangement of the trabeculae. The expanding medullary cavity becomes largely free of spicules of cancellous bone in much of the diaphysis and becomes filled with adipose tissue and hematopoietic marrow. Conditions altering the balance of bone formation and resorption may cause abnormally thickened or significantly thinned (osteoporotic) cortices. A variety of hormones regulate bone growth, and their concentrations cause the growth spurt that occurs during puberty. As this process waxes and wanes chondrocyte proliferation decreases, however, maturation and bone formation proceed. This eventually leads to complete enchondral ossification and, at this time, the growth plate is considered closed and all additional bone growth is appositional (34). Cessation of growth of the secondary centers of ossification occurs in a similar fashion. However, a remnant of mineralized growth cartilage, which is the tidemark cartilage, persists at the base of the articular surface (Fig. 1.24). It is demarcated from the true articular cartilage by a thin undulating layer of more densely mineralized matrix, known as the tidemark (Fig. 1.24). The biologic potential of the tidemark cartilage persists as increases in hormones, such as growth hormone in the setting of acromegaly, can reactivate the process of enchondral ossification and produce additional growth in the adult. In normal circumstances, however, the vestige of the growth cartilage remains dormant, and functions as an anchor of the true articular cartilage to the subchondral bone plate (Fig. 1.24).

Figure 1.24 End of a large long bone containing true articular cartilage and at its base is the tidemark cartilage. The undulating purple line is the tidemark and it delineates the true articular cartilage from the tidemark cartilage, which is the remnant of growth plate-like cartilage. The tidemark cartilage is anchored to the underlying bone.

Intramembranous ossification The fibrous membrane rich in osteoprogenitor cells that is the basis of intramembranous ossification develops from the mesenchymal condensations in the embryo, and the periosteum in the fetus, child, and adult (48). The osteoprogenitor cells produce offspring that differentiate into mature osteoblasts that deposit bone matrix. Large portions of the flat bones of the skull, including the frontal, parietal, occipital, and temporal bones, form by this process. Also, since the cortices of all bones are largely created by osteoblasts derived from the periosteum, all bones, in at least some part, are formed by intramembranous ossification. Growth of membranous bone

occurs only by apposition of new bone, and the medullary cavities are created and maintained by endosteal osteoclastic activity. In the case of fracture callus, bone formation may occur both via intramembranous and enchondral ossification.

Modeling and remodeling The processes of bone formation and resorption are tightly coupled, and their balance determines skeletal mass at any point in time (49, 50). As the skeleton grows and enlarges (undergoes modeling) during childhood and young adulthood, bone formation predominates, whereas after the third or fourth decades of life bone resorption prevails. The breakdown and renewal of bone fundamental to the formation and maintenance of the skeleton is called remodeling. Remodeling is a dynamic process involving the removal and replenishment of both cortical and trabecular bone; it continues throughout life to maintain bone mass, skeletal integrity, and skeletal function (49, 50). This process is complex and at least partially controlled by the interplay of different organ systems, including the peripheral sympathetic nervous system (51), and by mechanically induced microdamage. It depends on the integrated actions of osteoblasts, osteocytes, reversal cells, and osteoclasts (52), and, in adults, is responsible for turning over approximately 10% of the skeleton on an annual basis (49, 50).

Sites vulnerable to trauma in developing long bones Growing bones are composed of an admixture of tissues of differing consistencies and quantities; therefore, they are susceptible to trauma. Although any portion of long bones may fracture, the metaphyseal– epiphyseal region is a distinctive site of injury in children. A region of fracture susceptibility to shear strains in the young infant is the trabecular transition zone (29, 40). In this zone, the density of bone-covered mineralized cartilage of the primary spongiosa is greater than that of the adjacent secondary spongiosa, providing a potential plane of trabecular failure when exposed to excessive mechanical loads. After infancy, the location of fractures shifts to involve the physeal cartilage, because of the concurrent increase in thickness of the juxtaphyseal metaphyseal bony trabeculae, which enhances its physical strength relative to the adjacent growth plate (53).

A closely related site of vulnerability of the infant metaphysis lies near the SPBC (Figs 1.17, 1.18) (29, 32, 54, 55). Fractures through the trabecular transition zone are limited from extending directly to the periphery by the thick bony collar that surrounds this region. Thus, planar fractures involving the trabecular transition zone characteristically extend to the bone surface at the junction of the SPBC and the metaphyseal cortex (Figs. 1.17, 1.18), resulting in the varied radiographic appearances of the classic metaphyseal lesion (CML) of infant abuse (32, 54, 55), an injury that will be discussed in depth in subsequent chapters.

Summary The skeleton is a complex structure that plays a variety of different roles crucial to life. It is composed of many individual bones that are constructed of proteins, minerals, and the cells specific to bone, namely, the families of osteoblasts and osteoclasts. Bones form through enchondral and intramembranous ossification, and these processes are complex and tightly regulated by molecular genetics and cell-signaling pathways. Understanding the structure of the skeleton and its growth and development provides the foundation to understand its susceptibility to trauma and the pathology induced by injury and tissue damage.

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Chapter 2

Skeletal trauma: general considerations

Paul K. Kleinman, Andrew E. Rosenberg and Andy Tsai Diagnostic Imaging of Child Abuse, third edition, ed. Paul K. Kleinman. Published by Cambridge University Press. © Paul K. Kleinman 2015.

Introduction Epidemiology and distribution of skeletal injuries Long bone injuries Subperiosteal new bone formation Long bone shaft fractures The CML Background Prevalence Histologic studies Radiologic–pathologic correlates Radiographic projection Fracture extent Anatomic site Age of the injury Radiologic correlates of healing Conclusions and mechanisms of injury Salter–Harris injuries and epiphyseal separations

Introduction Fractures are common injuries in abused children, second only to cutaneous bruising (1). Although fundamental to the documentation of abuse, the fractures are rarely life-threatening and few result in long-term deformity. Specific types of fractures are known to be associated with abuse, and their recognition is important for their accurate identification and in understanding their significance.

Many reports of unexplained subdural hematomas (SDHs) in infants had appeared before Caffey’s historic 1946 article, but it was only after he associated these lesions with certain patterns of skeletal injury that the modern medical entity of child abuse was formulated (2). In a sense, recognition of the role of skeletal injuries in child abuse became the catalyst for the surge of interest in child maltreatment after Caffey’s original description. In the years that followed, most reports of child abuse focused mainly on the radiologic alterations associated with the skeletal trauma (3–14). The confident documentation of skeletal injury, facilitated by characteristic radiologic alterations, provided investigators the opportunity to study the multiple facets of child abuse. Eventually, the blend of the clinical and the radiologic findings led Kempe, Silverman, and others to bring these associations to the status of the “battered child syndrome” (15). Skeletal injury figured prominently in the early concepts of the battered child syndrome. As the definitions of child abuse expanded to include neglect, sexual abuse, and a variety of other unusual forms of maltreatment, the percentage of abused children with fractures in large series has decreased (16). Workers in the field of abuse and neglect may now encounter skeletal injury in only a minority of patients. Ironically, this trend may have had the consequence of de-emphasizing the importance of rigorously documenting the nature and extent of skeletal injury in cases of suspected abuse. In physically abused infants and young children, skeletal injuries remain common findings, often in the absence of overlying bruising, and may in fact be the only indications of inflicted injury (17–19). It is a tragedy when a child suffers further injuries, or a sibling or other child at risk is abused because of failure to document earlier abusive episodes. A number of studies indicate that the diagnosis of abuse may be missed when young children present with fractures, and that some will go on to sustain more serious, sometimes fatal inflicted injuries (20–24). Given an increasingly complex and adversarial legal environment, cases satisfying the medical requirements for a diagnosis of physical abuse are regularly challenged in the courtroom, often with novel and unsupported hypotheses (see Chapter 13). The presence of skeletal injury may provide the necessary evidence to support a legal determination of child maltreatment. This public health issue demands that all professionals dealing with suspected abuse possess some familiarity with these skeletal injuries as

well as an understanding of their diagnostic value.

Epidemiology and distribution of skeletal injuries Fractures are relatively common in childhood and most are accidental. Jones and others found that approximately 50% of children suffered at least 1 fracture, most often at the wrist/forearm, between the age of 5 and 18 years (25). Fractures become less common with decreasing age and nonambulatory status (1, 26, 27). Abusive injuries are most common in toddlers and infants, and this pattern is most evident in early infancy (28). Krishnan et al. examined the patterns of osseous injuries and psychosocial factors affecting victims of child abuse. They found that 48% of the children were first-born and 67% of parents were unemployed. Of the alleged abuser, the mother was known to be responsible in 50% of cases. In 10% of cases, the parent responsible for the injury admitted to the offence at the time of presentation at the hospital (29). Since the clinical and imaging assessments, as well as the diagnostic criteria for suspected abuse utilized in published studies vary considerably, it is difficult to establish a precise estimate of the prevalence of fractures in maltreated children. The matter is further confounded by the fact that skeletal injury commonly forms the basis of a diagnosis of abuse, and inclusion of fractures as a diagnostic criterion for abuse introduces significant bias into the calculation of prevalence estimates. Thus, the reported frequencies of fractures in cases of abuse vary widely, from 9 to 55% (30–39). Centers with large orthopedic services may see greater proportions of abused children with fractures, and studies that fail to differentiate neglect and sexual assaults from cases of physical abuse are likely to show smaller percentages of fractures (40). What is clear from early reports is that skeletal injuries are much more common in the younger age groups (30, 32). Recent estimates suggest that approximately one-third of abused children have fractures, and these injuries occur predominantly in infants ( skull (26%) > upper extremity/scapula/clavicle (20%) > ribs/sternum (20%); 1–2 years: skull

(31%); upper extremity/scapula/clavicle (31%) > lower extremity (23%) > ribs/sternum (9%). Table 2.2 Fractures due to abuse Age