Electromyography and Neuromuscular Disorders: Clinical-Electrophysiologic-Ultrasound Correlations [4th Edition] 9780323758307, 9780323758291, 9780323661805

Table of contents :
Electromyography and Neuromuscular Disorders: Clinical-Electrophysiologic-Ultrasound Correlations......Page 2
Copyright......Page 3
Foreword......Page 4
Preface to the Fourth Edition......Page 5
Preface to the Third Edition......Page 7
Preface to the Second Edition......Page 8
Preface to the First Edition......Page 10
Dedication......Page 11
Acknowledgments......Page 12
1 - Approach to Nerve Conduction Studies, Electromyography, and Neuromuscular Ultrasound......Page 13
LOCALIZATION OF THE DISORDER IS THE MAJOR AIM OF THE ELECTRODIAGNOSTIC STUDY......Page 14
Assessing the Degree of Axonal Loss Versus Demyelination has Implications for Severity and Prognosis......Page 15
Neuromuscular Junction Localization......Page 16
CARDINAL RULES OF NERVE CONDUCTION STUDIES AND ELECTROMYOGRAPHY......Page 17
NEUROMUSCULAR ULTRASOUND......Page 19
Motor Neuron Disease......Page 20
CARDINAL RULES OF NEUROMUSCULAR ULTRASOUND......Page 21
ANATOMY......Page 23
PHYSIOLOGY......Page 26
CLASSIFICATION......Page 31
RECORDING......Page 32
MOTOR CONDUCTION STUDIES......Page 35
Duration......Page 36
Conduction Velocity......Page 37
Peak Latency......Page 38
Conduction Velocity......Page 39
Lesions Proximal to the Dorsal Root ­Ganglion Result in Normal Sensory Nerve Action Potentials......Page 40
Proximal Stimulation: Normal Temporal Dispersion and Phase Cancellation......Page 42
Use Supramaximal Stimulation......Page 44
Axonal Loss......Page 45
Demyelination......Page 47
Conduction Block......Page 48
Myopathy......Page 50
Neuromuscular Junction Disorders......Page 51
4 - Late Responses......Page 53
F RESPONSE......Page 54
F Response Procedure......Page 55
The F Estimate......Page 56
H REFLEX......Page 58
AXON REFLEX......Page 61
BLINK REFLEX PROCEDURE......Page 64
PATTERNS OF ABNORMALITIES......Page 66
NORMAL NEUROMUSCULAR JUNCTION PHYSIOLOGY......Page 69
Modeling Slow Repetitive Nerve Stimulation......Page 70
REPETITIVE NERVE STIMULATION IN THE ELECTROMYOGRAPHY LABORATORY......Page 72
Exercise Testing in the Electromyography Laboratory......Page 73
Temperature Must Be Controlled......Page 74
Nerve Selection......Page 75
Decrement and Increment Calculation......Page 76
Repetitive Nerve Stimulation Protocol......Page 77
Routine Ulnar Conduction Study: Pseudo–Conduction Block Between the Wrist and Below-­Elbow Sites......Page 79
Ulnar Conduction Study: Proximal Martin-­Gruber Anastomosis and Pseudo–Conduction Block Between the Below-­Elbow and Above-­Elbo.........Page 80
Ulnar Conduction Study Recording the First Dorsal Interosseous: Pseudo-­Conduction Block Between the Wrist and Below-­Elbow Site.........Page 81
Routine Median Motor Study: Increased Compound Muscle Action Potential Amplitude Proximally......Page 83
Martin-­Gruber Anastomosis and Carpal Tunnel Syndrome: Positive Proximal Deflection (“Dip”) and Factitiously Fast Conduction Vel.........Page 84
ACCESSORY PERONEAL NERVE......Page 85
Miscellaneous Anatomic Variations......Page 86
Temperature......Page 90
Age......Page 92
Electrode Impedance and Noise......Page 93
Filters......Page 95
Stimulus Artifact......Page 96
Cathode Position: Reversing Stimulator Polarity......Page 98
Supramaximal Stimulation......Page 99
Co-­Stimulation of Adjacent Nerves......Page 100
Electrode Placement for Motor Studies......Page 102
Antidromic Versus Orthodromic Recording......Page 103
Distance Between Recording Electrodes and Nerve......Page 105
Limb Position and Distance Measurements......Page 106
Limb Position and Waveform Morphology......Page 107
Latency Measurements: Sweep Speed and Sensitivity......Page 109
9 - Basic Statistics for Electrodiagnostic Studies......Page 111
BAYES’ THEOREM AND THE PREDICTIVE VALUE OF A POSITIVE TEST......Page 114
LIKELIHOOD RATIOS......Page 116
MULTIPLE TESTS AND THE INCREASING RISK OF FALSE POSITIVES......Page 117
Key Points......Page 119
Distal Distance......Page 120
Key Points......Page 121
Key Points......Page 122
Distal Distance......Page 123
Key Points......Page 124
Key Points......Page 125
Stimulation Site......Page 126
Key Points......Page 127
Distal Distance......Page 129
Recording Sites......Page 130
Recording Site......Page 131
Stimulation Site......Page 132
Key Points......Page 133
Upper Extremity......Page 134
Craniobulbar......Page 135
Key Points......Page 136
Recording Site......Page 137
Key Points......Page 138
Key Points......Page 140
Stimulation Site......Page 141
Key Points......Page 142
Recording Site......Page 143
Key Points......Page 144
Nerve Conduction Studies of the Lower Extremity: Normal Adult Values......Page 145
EQUIPMENT......Page 146
TYPICAL NEEDLE EMG EXAMINATION (BOX 12.1)......Page 148
Cross-­Section Anatomy Key Points......Page 150
Cross-­Section Anatomy Key Points......Page 153
Cross-­Section Anatomy Key Points......Page 157
Cross-­Section Anatomy Key Points......Page 160
Cross-­Section Anatomy Key Points......Page 163
Cross-­Section Anatomy Key Points......Page 166
Cross-­Section Anatomy Key Points......Page 169
Cross-­Section Anatomy Key Points......Page 173
Cross-­Section Anatomy Key Points......Page 176
Cross-­Section Anatomy Key Points......Page 179
Cross-­Section Anatomy Key Points......Page 182
Cross-­Section Anatomy Key Points......Page 185
Cross-­Section Anatomy Key Points......Page 188
Cross-­Section Anatomy Key Points......Page 191
Cross-­Section Anatomy Key Points......Page 195
Cross-­Section Anatomy Key Points......Page 199
Cross-­Section Anatomy Key Points......Page 202
Cross-­Section Anatomy Key Points......Page 206
Cross-­Section Anatomy Key Points......Page 209
Cross-­Section Anatomy Key Points......Page 212
Cross-­Section Anatomy Key Points......Page 215
Cross-­Section Anatomy Key Points......Page 218
Cross-­Section Anatomy Key Points......Page 221
Cross-­Section Anatomy Key Points......Page 225
Cross-­Section Anatomy Key Points......Page 230
Cross-­Section Anatomy Key Points......Page 234
Cross-­Section Anatomy Key Points......Page 238
Morphology......Page 241
INSERTIONAL ACTIVITY......Page 244
SPONTANEOUS ACTIVITY: ABNORMAL MUSCLE FIBER POTENTIALS......Page 245
Positive Sharp Waves......Page 246
Complex Repetitive Discharges......Page 248
Fasciculation Potentials......Page 250
Doublets, Triplets, and Multiplets......Page 251
Myokymic Discharges......Page 252
Neuromyotonic Discharges......Page 253
Rest Tremor......Page 254
PHYSIOLOGY......Page 257
MORPHOLOGY......Page 258
Duration......Page 259
Amplitude......Page 260
STABILITY......Page 261
FIRING PATTERN (ACTIVATION, RECRUITMENT, INTERFERENCE PATTERN)......Page 262
Chronic Axonal Loss......Page 267
Acute......Page 268
Central Nervous System Disorders......Page 269
Axonal Loss Lesions......Page 272
Demyelinating Lesions......Page 273
IMPORTANT NEUROPATHIC PATTERNS......Page 274
Axonal Loss: Acute......Page 275
Demyelination (Slowing and Conduction Block): Single Proximal Lesion......Page 276
Demyelination (Slowing and Conduction Block): Single Distal Lesion......Page 277
MYOPATHIC LESIONS......Page 278
NEUROMUSCULAR JUNCTION LESIONS......Page 279
Upper Motor Neuron Lesion......Page 280
Mononeuropathy: Localizing......Page 281
Chronic Demyelinating Polyneuropathy With Secondary Axonal Changes: Uniform Slowing......Page 282
Radiculopathy......Page 283
Neuromuscular Junction: Postsynaptic Disorders......Page 284
Myopathy With Denervating Features......Page 285
Pure Motor Loss on Nerve Conduction Studies......Page 286
Localizing a Mononeuropathy by Needle EMG: Issues and Limitations......Page 287
NEUROMUSCULAR ULTRASOUND HISTORY......Page 290
BASIC PHYSICS OF ULTRASOUND......Page 291
OPTIMIZING THE IMAGE......Page 294
Tendon......Page 298
Arteries and Veins......Page 299
Skin and Subcutaneous Tissue......Page 300
Cartilage......Page 301
Anisotropy......Page 302
Posterior Acoustic Enhancement......Page 303
Reverberation Artifact......Page 304
ULTRASOUND LIMITATIONS......Page 305
18 - Neuromuscular Ultrasound of Mononeuropathies......Page 307
APPEARANCE OF NORMAL NERVE......Page 308
Measurements......Page 309
Ganglion Cysts......Page 314
Bone Fragments and Callus......Page 315
Tenosynovitis and Synovial Hypertrophy......Page 317
Tumor......Page 318
Hematomas and Blood Vessel Abnormalities......Page 321
Patterns of Muscle Denervation......Page 323
DEMYELINATING POLYNEUROPATHIES......Page 325
Charcot-­Marie-­Tooth Polyneuropathy......Page 326
Chronic Acquired Demyelinating Polyneuropathies......Page 327
Acute-­Onset Chronic Inflammatory Demyelinating Polyneuropathy......Page 328
DIABETIC POLYNEUROPATHY......Page 329
MOTOR NEURON DISEASE......Page 330
MYOPATHY......Page 331
ANATOMY......Page 335
CLINICAL......Page 337
DIFFERENTIAL DIAGNOSIS......Page 339
Nerve Conduction Studies......Page 340
Median-­Versus-­Ulnar Palm-­to-­Wrist Mixed Nerve Studies......Page 341
Median Second Lumbrical-­Versus-­Ulnar Interossei Distal Motor Latencies......Page 342
Wrist-­to-­Palm Versus Palm-­to-­Digit Sensory Conduction Velocity (Segmental Sensory Conduction Studies Across the Wrist)......Page 343
Inching Across the Wrist and Palmar Stimulation......Page 344
Electromyographic Approach......Page 347
Special Situation: EDX Studies After Carpal Tunnel Release......Page 348
ULTRASOUND CORRELATIONS......Page 349
Nonlocalizing Median Neuropathy......Page 353
Persistent Symptoms or Recurrent Symptoms After Carpal Tunnel Release Surgery......Page 354
COMMON ANOMALIES......Page 355
Ganglion Cyst......Page 356
Neuroma in Continuity......Page 357
Tumors......Page 358
Thickened Epineurium and Intraneural Scar......Page 359
DETAILED ANATOMY AT THE ANTECUBITAL FOSSA......Page 370
Ligament of Struthers Entrapment......Page 371
ANTERIOR INTEROSSEOUS NERVE SYNDROME......Page 372
Nerve Conduction Studies......Page 373
Proximal Median Nerve......Page 374
Anterior Interosseous Nerve......Page 378
ANATOMY......Page 384
CLINICAL......Page 385
DIFFERENTIAL DIAGNOSIS......Page 386
Differential Slowing: Flexed Versus Extended Elbow Conduction Techniques......Page 388
Short Segment Incremental Studies (“Inching”)......Page 391
Mixed and Sensory Nerve Conductions......Page 392
Dorsal Ulnar Cutaneous Sensory Study......Page 393
Nerve Conduction Study Pitfalls......Page 395
ULTRASOUND CORRELATIONS......Page 397
CLINICAL......Page 414
DIFFERENTIAL DIAGNOSIS......Page 416
Ulnar Motor Studies Recording the First Dorsal Interosseous......Page 417
Short Segment Incremental Studies......Page 418
Comparison of the Various Electrophysiologic Tests in Ulnar Neuropathy at the Wrist......Page 419
Electromyographic Approach......Page 420
ULTRASOUND CORRELATIONS......Page 422
ANATOMY......Page 429
Deep Branch......Page 431
Posterior Interosseous Neuropathy......Page 432
DIFFERENTIAL DIAGNOSIS......Page 433
ELECTROPHYSIOLOGIC EVALUATION......Page 434
Nerve Conduction Studies......Page 435
Anatomic Considerations of Some Radial-­Innervated Muscles on Needle EMG......Page 437
ULTRASOUND CORRELATIONS......Page 438
ANATOMY......Page 453
Peroneal Neuropathy at the Fibular Neck......Page 455
ETIOLOGY......Page 456
Nerve Conduction Studies......Page 457
Electromyographic Approach......Page 458
ULTRASOUND CORRELATIONS......Page 460
CLINICAL......Page 471
DIFFERENTIAL DIAGNOSIS......Page 472
Nerve Conduction Studies......Page 473
ULTRASOUND CORRELATIONS......Page 474
CLINICAL......Page 480
Nerve Conduction Studies......Page 481
Electromyographic Approach......Page 482
ULTRASOUND CORRELATIONS......Page 483
Trigeminal Nerve......Page 490
Facial Neuropathy......Page 492
Trigeminal Neuropathy......Page 493
Nerve Conduction Studies......Page 494
Nerve Conduction Studies and Blink Reflex......Page 495
Electromyographic Approach......Page 496
CLINICAL......Page 502
Key Question No. 2: Which Fiber Types Are Involved (Motor, Large Sensory, Small Sensory, Autonomic)?......Page 503
Key Question No. 5: Is There a Family History of Polyneuropathy?......Page 505
Special Situations in Axonal Polyneuropathy: The Use of the Sural/Radial Amplitude Ratio in Mild Polyneuropathy......Page 507
Diabetes......Page 508
DEMYELINATING POLYNEUROPATHY......Page 509
Guillain-­Barré Syndrome (GBS)......Page 510
Electrophysiology......Page 511
Charcot-­Marie-­Tooth Neuropathy......Page 512
Electrophysiology......Page 513
Prognosis......Page 514
Electrophysiology......Page 515
Nerve Conduction Studies......Page 516
Electromyographic Approach......Page 517
ULTRASOUND CORRELATIONS......Page 518
Classic Amyotrophic Lateral Sclerosis......Page 537
Primary Lateral Sclerosis......Page 538
Cervical/Lumbar Stenosis......Page 539
Inclusion Body Myositis......Page 540
Mimics of Primary Lateral Sclerosis......Page 541
Nerve Conduction Studies......Page 542
Electromyographic Approach......Page 545
ULTRASOUND CORRELATIONS......Page 546
31 - Atypical and Inherited Motor ­Neuron Disorders......Page 552
Paralytic Poliomyelitis and Postpolio Syndrome......Page 553
Retrovirus-­Associated Motor Neuron Disorders......Page 554
X-­Linked Bulbospinal Muscular Atrophy (Kennedy Disease)......Page 555
Adult-­Onset Hexosaminidase A Deficiency (Late-­Onset Tay-­Sachs Disease)......Page 556
Monomelic Amyotrophy......Page 557
Delayed Radiation-­Induced Motor Neuron Syndrome......Page 559
Nerve Conduction Studies......Page 560
Electromyographic Approach......Page 561
ETIOLOGY......Page 569
Nerve Conduction Studies......Page 570
Superficial Peroneal SNAP and L5 Radiculopathy: The Rare Exception......Page 573
Electromyographic Approach......Page 574
TIME COURSE IN RADICULOPATHY......Page 576
ABERRANT REINNERVATION AND THE “BREATHING ARM”......Page 577
It May Be Difficult to Localize a Radiculopathy to a Single Root Level......Page 578
If the Sensory Nerve Root Is Predominantly Affected, the Electromyographic Study Will Be Normal......Page 579
Abnormal Paraspinal Muscles Are Useful in Identifying a Radiculopathy but Not the Segmental Level of the Lesion......Page 581
There May Be Few or No Electromyographic Abnormalities in Spinal Stenosis......Page 582
Fibrillation Potentials in the Paraspinal Muscles Do Not Necessarily Imply Radiculopathy......Page 583
ANATOMY......Page 589
CLINICAL......Page 590
Lateral Cord Plexopathy......Page 591
Neuralgic Amyotrophy......Page 592
Postoperative Brachial Plexopathy......Page 593
Thoracic Outlet Syndrome......Page 594
Nerve Conduction Studies......Page 595
Electromyographic Approach......Page 598
Neurogenic Thoracic Outlet Syndrome......Page 599
Neuralgic Amyotrophy......Page 600
Brachial Plexopathy......Page 602
Neuralgic Amyotrophy......Page 607
Clinical......Page 618
Clinical......Page 621
Electrodiagnosis......Page 622
Electrodiagnosis......Page 623
Electrodiagnosis......Page 624
Clinical......Page 625
Electrodiagnosis......Page 626
ULTRASOUND CORRELATIONS......Page 627
Special Considerations: Musculocutaneous, Suprascapular, and Spinal Accessory Nerves......Page 628
Obturator Nerve......Page 634
CLINICAL......Page 635
Retroperitoneal Hemorrhage......Page 636
Postpartum Plexopathy......Page 639
Diabetic Amyotrophy......Page 640
Electrophysiologic Evaluation......Page 641
Nerve Conduction Studies......Page 642
Electromyographic Approach......Page 643
ULTRASOUND CORRELATIONS......Page 644
CLINICAL......Page 653
ETIOLOGY......Page 655
Piriformis Syndrome......Page 656
Nerve Conduction Studies......Page 657
Special Studies on Suspected Piriformis Syndrome......Page 658
Electromyographic Approach......Page 659
ULTRASOUND CORRELATIONS......Page 660
Example: Sciatic Neuropathy Secondary to a Bone Fragment......Page 661
MYASTHENIA GRAVIS......Page 666
Clinical......Page 667
Nerve Conduction Studies......Page 668
Repetitive Nerve Stimulation......Page 669
Single-­Fiber Electromyography......Page 670
Clinical......Page 673
Electrophysiologic Evaluation......Page 674
Clinical......Page 675
CONGENITAL MYASTHENIC SYNDROMES......Page 676
38 - Myopathy......Page 687
CLINICAL......Page 688
Nerve Conduction Studies......Page 689
Spontaneous Activity in Myopathies......Page 690
Motor Unit Action Potential Analysis in Myopathies......Page 691
Polymyositis and Dermatomyositis......Page 693
Inclusion Body Myositis......Page 694
Late-­Onset Acid Maltase Deficiency (Pompe Disease)......Page 695
ULTRASOUND CORRELATIONS......Page 696
39 - Myotonic Muscle Disorders and Periodic Paralysis Syndromes......Page 705
Prolonged Exercise Test......Page 706
Myotonic Dystrophy......Page 708
Clinical......Page 709
Electrophysiologic Evaluation......Page 711
Electrophysiologic Evaluation......Page 712
Electrophysiologic Examination......Page 713
Paramyotonia Congenita......Page 714
Clinical......Page 715
Clinical......Page 716
Electrophysiologic Examination......Page 717
OTHER CONDITIONS ASSOCIATED WITH MYOTONIA AND PERIODIC PARALYSIS......Page 718
DIFFERENTIAL DIAGNOSIS OF NEUROLOGIC WEAKNESS IN THE ICU......Page 725
ELECTRODIAGNOSTIC STUDIES IN THE ICU: TECHNICAL ISSUES......Page 727
Low or Absent Motor Responses With Normal Sensory Responses......Page 729
Decreased Activation......Page 731
NERVE CONDUCTION AND ELECTROMYOGRAPHIC PROTOCOL IN THE INTENSIVE CARE UNIT......Page 732
ULTRASOUND CORRELATIONS......Page 733
MATURATION ISSUES......Page 741
TECHNICAL ISSUES......Page 743
APPROACH TO THE CHILD AS A PATIENT......Page 744
ULTRASOUND CORRELATIONS......Page 746
BASICS OF ELECTRICITY......Page 749
Ohm’s Law......Page 750
Kirchhoff’s Laws......Page 751
Resistors in Parallel......Page 752
Direct Current and Alternating Current......Page 753
Capacitance......Page 754
Inductance......Page 756
WAVEFORMS, FREQUENCY ANALYSIS, AND FILTERING......Page 757
Low-­Frequency (High-­Pass) Filters......Page 758
High-­Frequency (Low-­Pass) Filters......Page 759
PRACTICAL IMPLICATIONS FOR ELECTRODIAGNOSTIC STUDIES......Page 760
ELECTRICAL ISSUES......Page 763
Central Lines and Electrical Wires......Page 765
Implanted Pacemakers and Cardioverter-­Defibrillators......Page 766
PNEUMOTHORAX......Page 767
BLEEDING......Page 768
Coexistent Medical Conditions......Page 769
Needle Electromyography and Patients at Risk of Bleeding......Page 770
INFECTION......Page 771
ULTRASOUND CORRELATIONS......Page 772
SUMMARY......Page 773
Palmar Mixed Nerve Studies......Page 775
Phrenic Motor Studya......Page 776
Motor Studies......Page 777
Late Responsesa......Page 778
Mean Motor Unit Action Potential Duration Based on Age and Muscle Group......Page 779
Pediatric Normalsa......Page 780

Citation preview

Fourth Edition

Electromyography and Neuromuscular Disorders CLINICAL-­ELECTROPHYSIOLOGIC-­ULTRASOUND ­CORRELATIONS

David C. Preston, MD Professor of Neurology Case Western Reserve University School of Medicine Program Director, Neurology Residency Vice Chairman, Department of Neurology University Hospitals Cleveland Medical Center Cleveland, Ohio

Barbara E. Shapiro, MD, PhD Associate Professor of Neurology Case Western Reserve University School of Medicine University Hospitals Cleveland Medical Center Cleveland, Ohio

Elsevier 1600 John F. Kennedy Blvd. Ste 1600 Philadelphia, PA 19103-­2899 ELECTROMYOGRAPHY AND NEUROMUSCULAR DISORDERS: CLINICAL-­ELECTROPHYSIOLOGIC-­ULTRASOUND CORRELATIONS, FOURTH EDITION

ISBN: 978-­0-­323-­66180-­5

Copyright © 2021 by Elsevier, Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein).

Notice Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds or experiments described herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made. To the fullest extent of the law, no responsibility is assumed by Elsevier, authors, editors or ­contributors for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Previous editions copyrighted 2013, 2005, and 1998. Library of Congress Control Number: 2020931444

Senior Acquisitions Editor: Melanie Tucker Content Development Specialist: Lisa Barnes Publishing Services Manager: Catherine Albright Jackson Senior Project Manager: Doug Turner Designer: Renee Duenow Printed in Canada Last digit is the print number:  9  8  7  6  5  4  3  2  1

ix

Foreword Electromyography (EMG) is a relatively new test. When I started my residency training at the Mayo Clinic in 1973 with Drs. Ed Lambert and Jasper Daube, it was not widely available, and the equipment was rudimentary. The machines were based on vacuum tube technology, were large and cumbersome, took up most of the room, and had to be tweaked and calibrated. Filters had to be set manually for each patient as well as each test. Heating lamps were not necessary because the heat alone from these machines in a small room was enough to keep patients warm and make the neophyte trainee perspire, especially when the instructor entered the room. Since then, much has changed. New technology has produced compact, microchip-­based, and highly accurate and reliable machines. Gains and filters are available at the touch of a button. Moreover, fostered by the efforts of pioneers such as Lambert, Daube, and many others, there has been an explosion of knowledge in the field of EMG and clinical neurophysiology. As a result, we now know a great deal about the neurophysiologic findings in many diseases of the peripheral nervous system. Indeed, for those of us in the day-­to-­day practice of clinical neuromuscular diseases and clinical neurophysiology, EMG and related electrophysiologic studies can be an enormous help in diagnosis and management. Most of us regard EMG as the single most useful test in clarifying the differential diagnosis of an obscure neuromuscular problem, second only to the clinical examination. We all pay lip service to the concept that the EMG is an extension of the clinical examination and best used in conjunction with a careful clinical examination. In practice, however, there are many occasions when this rule is violated, and there has been a trend lately to develop “clinical neurophysiologists” who practice in the laboratory and have little clinical experience. This is a dangerous approach, because

although EMG and related tests are a powerful and sensitive technology, they are also subject to interpretive error. As such, they must always be evaluated in light of careful consideration of the clinical findings by an experienced clinician. Improperly interpreted or performed EMG tests can lead to useless diagnostic tests and dangerous treatments. On virtually a weekly basis, patients are referred to my clinic because of tests done improperly or misinterpreted in the light of the clinical findings. Thus there is a need for publications that continue to teach the clinical approach to neurophysiology. Although several excellent texts cover the technical and, to some extent, clinical aspects of EMG, this book by Preston and Shapiro is unique in its emphasis on clinical and EMG correlation. The book amply and clearly covers the technical aspects, but its strength lies in its emphasis on clinical/neurophysiologic correlation, a hands-on, interactive approach for the reader, and a style that most closely approximates how a clinical neurophysiologist thinks when approaching a complicated patient. The authors’ discussion of potential pitfalls in testing is also most helpful. The authors’ admonition that, when in doubt, the examiner should stop stimulating and needling, retake the history, and repeat the clinical examination bears repeating to every trainee in every program. This text will be a positive and important addition to the EMG literature. It will be helpful to trainees in EMG and should also be useful as a refresher to experienced electromyographers. I congratulate Drs. Preston and Shapiro on an excellent book. I’m jealous: I wish I had written it. John J. Kelly Jr., MD Chief, Department of Neurology Deputy Director, Cooper Neurological Institute Camden, New Jersey

Dr. Kelly’s most recent position is Chair Emeritus, Department of Neurology, George Washington University, Washington, DC.

xi

Preface to the Fourth Edition Since the publication of this book in 1997, followed by the second and third editions in 2005 and 2012, respectively, we continue to be profoundly gratified by the overwhelmingly positive reception it has received. It has been humbling as we have traveled throughout the country and parts of the world to have so many physicians remark how much they have valued the text (not to mention wanting to have their picture taken with us). The main purpose of the text remains the same as the previous editions: to create a textbook that integrates electrodiagnostic studies and neuromuscular disorders in a practical and concise manner, always remembering the important principle that nerve conduction studies and electromyography (EMG) are an extension of the clinical examination. As the intention of this text was, and remains, to convey basic and essential information and the vast majority of the basic and essential information has not changed since the third edition, the question arises, why do a fourth edition? First, writing a fourth edition has allowed us to update many chapters, especially those that deal with clinical disorders, with new insights from recent medical literature. Second, we were able to add additional tables and figures that have further improved the text. Third, one of the major improvements in the previous edition was the inclusion of cross-­ sectional anatomy of the muscles used for needle EMG. The idea in that edition was that, to really master the needle EMG, one needs to be able to think three dimensionally— not only to know where the muscle is but to also know what other muscles are nearby and, even more importantly, what other important vascular structures and nerves are nearby that one needs to avoid. This addition of the cross-­sectional anatomy foreshadowed the major reason for doing a fourth edition—the addition of neuromuscular ultrasound correlations. Since the third edition of this text, much has changed in the field of neuromuscular medicine. The value of neuromuscular ultrasound has become well-­established, and its use will undoubtedly expand in the future. Neuromuscular ultrasound is a natural complement to electrodiagnostic (EDX) studies. Just as EDX studies are best performed by neuromuscular physicians, neuromuscular ultrasound studies are also best performed by neuromuscular physicians, who are very familiar with peripheral nerve and muscle anatomy and are well acquainted with the associated clinical disorders. Neuromuscular ultrasound has many advantages. It is painless and safe, with no side effects. It is dynamic: one can visualize nerves, muscles, and tendons as a limb is moved either actively or passively to help understand the relationship between the nerves and muscles examined and their surrounding structures. Knowing neuromuscular ultrasound improves one’s ability to perform EDX studies; indeed, we believe that our knowledge of peripheral nerve and muscle anatomy has more than doubled since starting to perform neuromuscular ultrasound. Research in neuromuscular

ultrasound has greatly expanded, with several thousand peer-­ reviewed articles published each year. Neuromuscular ultrasound workshops are offered by several professional societies and universities. It is being incorporated into many neuromuscular and EMG fellowships and into some residencies. Our text is not meant to be a substitute for a comprehensive textbook on neuromuscular ultrasound. Rather, we highlight the basics of neuromuscular ultrasound and many of its most useful features as a complement to EDX testing. In this edition, we include three new chapters: (1) “Fundamentals of Neuromuscular Ultrasound,” (2) “Neuromuscular Ultrasound of Mononeuropathies,” and (3) “Neuromuscular Ultrasound of Polyneuropathy, Motor Neuron Disease, and Myopathy.” In addition, almost all the clinical chapters now include new sections on Ultrasound Correlations. There are hundreds of new figures in these chapters and sections. Almost all the ultrasound figures purposely include the native ultrasound image alongside an annotated image to facilitate learning of the material. We refer the reader to several excellent textbooks and manuscripts on ultrasound and neuromuscular disorders in the suggested readings. It is important to emphasize that neuromuscular ultrasound does not and will not replace EDX testing but is complementary to it. EDX testing assesses the physiology of nerve and muscle, which ultrasound cannot do, and often localizes the problem. In contrast, ultrasound is an imaging test that can not only often localize the problem but also add some specific diagnostic information that EDX studies cannot detect. Once the information from the EDX study is known, ultrasound can then be used in a directed manner to obtain important additional structural and dynamic information. Like the previous editions, this text is meant to provide a single resource for those physicians training in or practicing electrodiagnostic studies. However, it can now also be used to learn the basics of neuromuscular ultrasound and how ultrasound can be used to complement the EDX study. In the future, we expect electromyographers will be referring more patients for neuromuscular ultrasound or performing ultrasound studies themselves. This text will help in both situations. From our perspective of teaching for more than 30 years on post-­graduate, residency, and fellowship levels, we feel that if one can master the fundamentals in this book, one should have all the basic concepts and information needed to competently understand and interpret electrodiagnostic studies. Likewise, one will understand the most important uses of neuromuscular ultrasound as an adjunct to EDX studies and how to interpret ultrasound studies. Nevertheless, with all the information presented in this text regarding the performance of EDX and ultrasound studies, there remains no substitute for hands-­on experience guided by

xii Preface to the Fourth Edition

supervision. The continued goal of this text is to present material in an easily understandable and logical manner. We have often commented to our students that with knowledge of anatomy, physiology, and neurologic localization, the practice of electrodiagnostic studies makes sense. With the addition of ultrasound correlation, it now makes even more sense. We hope that with the information contained in this

text, one can sit down with a patient, take a history, perform a physical examination, and use the appropriate electrodiagnostic studies, with ultrasound if indicated, to reach the most accurate and complete diagnosis. David C. Preston Barbara E. Shapiro

xiii

Preface to the Third Edition Since the publication of this book in 1997, followed by the second edition in 2005, we have been profoundly gratified by the continued overwhelmingly positive reception it has received from physicians, both in training and in practice. It has become one of the key resources for residents and fellows who are learning electrodiagnostic testing and clinical neuromuscular disorders. The goal of the first edition was to create a textbook that integrated electrodiagnostic studies and neuromuscular disorders in a practical and concise manner, always remembering the important principle that nerve conduction studies and electromyography (EMG) are an extension of the clinical examination. In the second edition, the companion CD of EMG waveforms was added so that the reader could have the benefit of being able to see and hear examples of classic EMG waveforms. The second edition was also expanded in the number of chapters and the breadth of information, adding chapters on Pediatric EMG, Electricity and Electronics, EMG in the ICU, Iatrogenic Electrodiagnosis, and Statistics for EMG studies. As the intention of this text was, and remains, to convey basic and essential information, and the vast majority of the basic and essential information has not changed, the question again arises, “why do a third edition?” The reasons are multifactorial. First, the authors now read many of our neurology journals and an increasing number of books on our iPads and other similar devices. We also now use these devices to connect to our electronic medical record, and look up drug information and a host of medical information. It therefore makes sense for a third edition to be both in print and completely electronic. Although it is difficult for many of us to think about replacing books with electronic media, this is clearly where the world is moving, led by our students, residents, and fellows in training. Second, writing a third edition gave us the opportunity to review the medical literature since 2005 on all the topics in the text, especially the chapters that deal with clinical disorders. Since the publication of the second edition there have been significant advances in understanding the genetics, pathophysiology, and treatment of many neuromuscular conditions, and these are included in the third edition. In addition, some electrodiagnostic techniques have been improved and other new ones described that are included in this third edition of the book. Third, with advances in publishing, we have now greatly improved the figures and color has been added to many

of them. Most of the photographs are now in color. Being strong believers in “a picture is worth a thousand words,” we have added over 100 new figures and photos, and others have been updated. In addition, one of the major improvements in the third edition has been the inclusion of cross-­ sectional anatomy of the muscles used for needle EMG. To really master the needle EMG, one needs to be able to think three dimensionally – not only where the muscle is, but what other muscles are nearby and, even more important, what other important vascular structures and nerves are nearby that one needs to avoid. To this end, we adapted cross-­sectional line drawings from the outstanding work of Eycleshymer and Schoemaker published in 1911. Each individual drawing was scanned and then oriented to the position used for EMG. The muscle of interest was shaded red and, likewise, all major nerves, veins, arteries and tendons were color coded. Finally, a life size image of a conventional needle EMG was placed in the correct orientation used for EMG. Thus, each muscle used for needle EMG now has a photo showing its correct insertion point along with its relevant cross-­sectional anatomy at that location. Like the first and second editions, this text is meant to provide a single resource for those physicians training in or practicing electrodiagnostic studies. From our perspective of teaching for over 20 years, on a post-­graduate, residency, and fellowship level, we feel that if one can master the fundamentals in this book, one should have all the basic concepts and information one needs to competently understand and interpret electrodiagnostic studies. Although a great deal of information is presented regarding the performance of studies, there remains no substitute for hands-­on experience under supervision. However, for the recognition and interpretation of EMG waveforms, the videos now published on the web should make this much easier to master. The continued goal of this text is to present material in an easily understandable and logical manner. The authors have often commented to their students that with knowledge of anatomy, physiology, and neurologic localization, the practice of electrodiagnostic studies makes sense. We hope that with the information contained in this text, one can sit down with a patient, take a history, perform a physical examination, and use the appropriate electrodiagnostic studies to reach a diagnosis. DCP BES

xv

Preface to the Second Edition Since the publication of the first edition of this book in 1997, we have been gratified by the overwhelmingly positive reception it has received from physicians, both in training and in practice. The goal of the first edition was to create a textbook that integrated electrodiagnostic studies and neuromuscular disorders in a practical and concise manner, always remembering the important principle that nerve conduction studies and electromyography (EMG) are an extension of the clinical examination. As this text is intended to convey basic and essential information, the question arises, “why do a second edition?” The authors acknowledge that no new muscles have been discovered in the human body over the past six years. Likewise, PCR and genetic tests have failed to identify any new nerves. Although much of the basic information in the fields of electrodiagnostic studies and neuromuscular disorders has not changed, we have written this second edition to improve and expand on many topics. First and most important, needle electromyography relies upon the proper interpretation of waveforms in real-­ time. While one can read about waveforms until they are blue in the face, it is very difficult to appreciate the audio and visual qualities of a waveform unless one can see and hear it. For the last fifteen years, we have collected video examples of classic EMG waveforms from a variety of patients. Two years after the publication of the first edition of this book, we introduced a companion videotape of common EMG waveforms. With new digital technology, we have now been able to digitize these video waveforms and put them on a companion CD which accompanies this book. Thus, in this second edition, the reader can view the CD on any computer, and watch and hear every common and classic EMG waveform. Because all the waveforms are digital, the reader can freeze or replay any waveform at any time. The textbook description and discussion of each waveform are now greatly enhanced by the companion CD. Since the publication of the first edition there have been significant advances in some neuromuscular conditions, and these are included in the second edition. Some new disorders have been described, among them paralytic poliomyelitis caused by the West Nile virus. In addition, several new techniques that have been described and validated in the electrodiagnosis of neuromuscular conditions are included in this second edition of the book. For instance, the electrodiagnosis of ulnar neuropathy at Guyon’s canal has significantly improved over the past few years, and several new techniques that are useful in making this diagnosis are included in this second edition. We spent a considerable amount of time thinking of better ways to present complex material in a logical and concise manner for this second edition of the book. Being strong believers in “a picture is worth a thousand words,” we have added many new figures, and others have been updated.

Indeed, we have added or updated more than 175 figures to the first edition of the book. We have improved the book in several other ways. First, we have expanded many of the clinical chapters, and in some cases separated them into new chapters, including median neuropathy at the wrist, proximal median neuropathy, ulnar neuropathy at the wrist, ulnar neuropathy at the elbow, amyotrophic lateral sclerosis, and atypical motor neuron disorders. All of the clinical chapters follow the same format that was used in the first edition, first presenting the important anatomic and clinical aspects of the disorder, followed by a discussion of the relevant electrodiagnostic studies. Each chapter ends with example cases based on actual patients, illustrating many important clinical and electrodiagnostic teaching points. In addition, in section three we have added a new chapter on basic statistics for electrodiagnostic studies, discussing several basic statistical concepts that every electromyographer needs to know in order to properly interpret a study. The first edition was divided into six separate sections. This new edition has been expanded to eight. The first new section deals with EMG in Special Clinical Settings, including the approach to electrodiagnostic studies in the intensive care unit, and the approach to electrodiagnostic studies in the pediatric patient. In the last several years, electromyographers are called upon more frequently to perform EMG studies in the intensive care unit to evaluate patients with profound weakness. New clinical disorders and electrodiagnostic techniques to evaluate these disorders have been extensively reported over the last several years and are reflected in this new edition. We have included a discussion of pediatric EMG because of its own unique set of challenges and techniques that differ from adult studies. The other new section deals with the basics of electricity and electronics, in addition to the potential risks and complications of electrodiagnostic studies. Some knowledge of electricity and electronics is extremely helpful in understanding electrodiagnostic studies. From a practical point of view, this knowledge is also very helpful in understanding and correcting many of the technical problems that arise in the everyday practice of electrodiagnostic medicine. The latter chapter arose from a continuing medical education course which we were asked to give at an annual meeting of the American Association of Electrodiagnostic Medicine, which was followed up as a review article in the journal Muscle and Nerve. Although nerve conduction studies and EMG are usually well tolerated and in most patients have minimal side effects, there are potential risks and complications, especially in certain patient populations. It is essential that all physicians performing these studies are aware of these potential risks and complications, albeit rare, and follow simple protocols to minimize them.

xvi Preface to the Second Edition

Like the first edition, this text is meant to provide a single resource for those physicians training in or practicing electrodiagnostic studies. From our perspective of teaching for many years, both on a post-­graduate and residency level, we feel that if one can master the fundamentals in this book, one should have all the basic concepts and information one needs to competently understand and interpret electrodiagnostic studies. Although a great deal of information is presented regarding the performance of studies, there is no substitute for hands-­on experience under supervision. However, it is our hope that with the companion CD as part of the textbook, the recognition and interpretation of EMG waveforms will be easier to master.

Finally, the goal of this text is to present material in an easily understandable and logical manner. The authors have often commented to their students that with knowledge of anatomy, physiology, and neurologic localization, the practice of electrodiagnostic studies makes sense. We hope that with the information contained in this text, one can sit down with a patient, take a history, perform a physical examination, and use the appropriate electrodiagnostic studies to reach a diagnosis. DCP BES

xvii

Preface to the First Edition This text is written primarily for clinicians who perform and interpret nerve conduction studies and electromyography (EMG), as well as for physicians who use the results of these electrodiagnostic studies to evaluate patients with peripheral nervous system disorders. Nerve conduction studies and EMG are best considered an extension of the clinical examination. Indeed, these studies cannot be properly planned, performed, or interpreted without knowing the patient’s symptoms and findings on the clinical examination. Numerous nerves and literally hundreds of muscles can be studied. To study them all would be neither practical for the electromyographer, nor desirable for the patient. In every case, the study must be individually planned, based on the clinical differential diagnosis, and then modified as the study progresses and further information is gained. The electromyographer needs to perform the studies necessary to both confirm and exclude certain diagnoses while minimizing the amount of patient discomfort. Most often, nerve conduction studies and EMG can successfully localize the lesion, provide further information about the underlying pathophysiology, and assist in assessing the disorder’s severity and temporal course. Although there are many excellent textbooks on electrodiagnosis and several superb references on clinical neuromuscular disorders, few integrate the two in a practical and concise manner. The approach we take in this text parallels our teaching program developed for the EMG fellowships and neurology residencies at the Brigham and Women’s Hospital and the Massachusetts General Hospital in Boston. The book is divided into six fundamental sections. Section One covers the overall practical approach to a patient in the EMG laboratory, followed by a review of the basic anatomy and neurophysiology that every electromyographer needs to understand. Section Two discusses the fundamentals of nerve conductions, including motor, sensory, and mixed nerve studies, as well as late responses, blink

reflexes, and repetitive nerve stimulation studies. In Section Three, important technical factors and artifacts are discussed, including the anomalous innervations. Section Four discusses the practical details of performing the most commonly used nerve conduction studies. In Section Five, the focus changes to needle EMG. After discussing the overall approach to the needle EMG, the anatomy of the bulbar, upper extremity, and lower extremity muscles is reviewed in detail. The last two chapters in this section cover the approach to the needle EMG examination, including the assessment of spontaneous activity and the analysis of motor unit action potentials. Section Six, Clinical–Electrophysiologic Correlations, forms the core of the text. After an overview of the important patterns, all of the major peripheral nervous system conditions are discussed, from both the clinical and the electrophysiologic points of view. Included are the mononeuropathies, polyneuropathies, motor neuron diseases, radiculopathies, plexopathies, disorders of the neuromuscular junction and muscle, and the myotonic and periodic paralysis disorders. At all times, the text integrates the important basic clinical and electrophysiologic points. In Chapters 16–32, clinical cases and their respective nerve conduction and EMG data are presented. Each case example is that of an actual patient taken from our EMG teaching file during the past 10 years. The authors appreciate that some specific techniques and normal values may vary from laboratory to laboratory. Nevertheless, the goal of this book is to present a logical approach in the EMG laboratory that combines the clinical and electrophysiologic evaluations of a patient with a disorder of the peripheral nervous system. DCP BES

xix

Dedication

To our daughters, Hannah and Abigail.

xxi

Acknowledgments The authors are indebted to their mentors in clinical neurophysiology: Drs. John J. Kelly, Jr., Eric L. Logigian, and Bhagwan T. Shahani. Dr. Bashar Katirji, our friend and colleague for more than 20 years, has been an inspiration and a great partner in teaching, research, and patient care in clinical neuromuscular disorders and electrophysiology. In addition, the authors wish to thank their colleagues, technologists, and present and former Neuromuscular and EMG fellows at the University Hospitals Cleveland Medical Center, the Brigham and Women’s Hospital, and the Massachusetts General Hospital. The contributions of Dale Preston, Thayer Preston, and Richard (Zack) Zydek to the photography are greatly appreciated. A special thanks to our friend, colleague, and mentor, Dr. Martin A. Samuels, who was instrumental in

the early parts of our academic and publishing careers. Then there are a host of individuals whose books, presentations, courses, and research ignited our passion in neuromuscular ultrasound. Among them are Drs. Francis O. Walker, Michael S. Cartwright, Lisa D. Hobson-­Webb, Jeff Strakowski, Lucia Padua, Stefano Bianchi, Carlo Martinoli, Andrea J. Boon, Leo Visser, Craig M. Zaidman, Antonios Kerasnoudis, H. Stephan Goedee, James B. Caress, and Joon Shik Yoon. At Elsevier, Melanie Tucker, Lisa Barnes, and Doug Turner were instrumental in bringing the fourth edition into print and electronic forms. And of course we will always be grateful to our dear friend, Susan Pioli, who has been there since the inception of this book and was instrumental in bringing the first and second editions to publication.

SECTION I • Overview of Nerve Conduction Studies and Electromyography

Approach to Nerve Conduction Studies, Electromyography, and Neuromuscular Ultrasound Electrodiagnostic (EDX) studies play a key role in the evaluation of patients with neuromuscular disorders. In selected cases, the additional use of neuromuscular ultrasound (U/S) can add key complementary anatomical and diagnostic information. EDX studies include nerve conduction studies (NCSs), repetitive nerve stimulation, late responses, blink reflexes, and needle electromyography (EMG), in addition to a variety of other specialized examinations. NCSs and needle EMG form the core of the EDX study. They are performed first and usually yield the greatest diagnostic information. NCSs and needle EMG are complementary and, therefore, are always performed together and in the same setting. Performed and interpreted correctly, EDX studies yield critical information about the underlying neuromuscular disorder and allow other laboratory and diagnostic tests, including neuromuscular U/S, to be used in an appropriate and efficient manner. Sometimes, the information gained from EDX studies leads to specific medical or surgical therapy. For example, a patient with a peripheral neuropathy clinically, who is subsequently found to have an acquired demyelinating neuropathy with conduction blocks on EDX studies, most often has a potentially treatable condition. Indeed, the value of EDX studies has been validated in several large case studies. In the most recent study by Lindstrom and colleagues, they analyzed data from 1414 consecutive patients and found that EDX studies either changed or confirmed the diagnosis in 52% and 47% of cases, respectively. Even more impressive was that EDX studies resulted in a change in patient management in 63% of patients. In practice, EDX studies serve as an extension of the clinical examination and should always be considered as such. Accordingly, a directed neurologic examination should always be performed before EDX studies to identify key clinical abnormalities and establish a differential diagnosis. With numerous nerves and literally hundreds of muscles available, it is neither desirable for the patient nor practical for the electromyographer to study them all. In each case, the study must be individualized, based on the neurologic examination and differential diagnosis, and modified in real time as the study progresses and further information is gained. NCSs and EMG are most often used to diagnose disorders of the peripheral nervous system (Fig. 1.1, Box 1.1). These include disorders affecting the primary motor neurons (anterior horn cells), primary sensory neurons (dorsal root ganglia), nerve roots, brachial and lumbosacral plexuses,

1

peripheral nerves, neuromuscular junctions (NMJs), and muscles. In addition, these studies may provide useful diagnostic information when the disorder arises in the central nervous system (CNS) (e.g., tremor or upper motor neuron weakness). Occasionally, information from the EDX study is so specific that it suggests a precise etiology. In most cases, however, the exact etiology cannot be defined based on EDX studies alone. It is in some of these cases that neuromuscular U/S is most useful. Neuromuscular U/S, the use of U/S to study the peripheral nerves and muscles, is often able to suggest the precise etiology of the disease, such as chronic inflammatory demyelinating polyneuropathy (CIDP) when a particular pattern of nerve enlargement is seen or inclusion body myositis when a particular pattern of muscle involvement is present. EDX studies provide an initial aid in defining the disorder, giving several key pieces of information, which in some cases can be further refined with neuromuscular U/S.

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0XVFOH Fig. 1.1  Elements of the peripheral nervous system. Note that the primary motor neuron resides within the spinal cord, whereas the primary sensory neuron, the dorsal root ganglion, lies outside the spinal cord. The dorsal root ganglion is a bipolar cell. Its proximal process forms the sensory nerve root; the distal process becomes the peripheral sensory nerve.

1

2

SECTION I  Overview of Nerve Conduction Studies and Electromyography

Box 1.1  Peripheral Nervous System Disorders: Localization and Major Categories

Motor Neuronopathy

Neuropathy

Amyotrophic lateral sclerosis and its variants Spinal muscular atrophy Infectious (poliomyelitis, West Nile virus) Focal motor neuron disease (monomelic amyotrophy) 

Pattern Mononeuropathy • Entrapment • Trauma Mononeuritis multiplex Polyneuropathy  Primary nerve pathology Demyelinating Axonal  Primary fiber type involvement Sensorimotor Motor Sensory 

Sensory Neuronopathy Autoimmune Paraneoplastic Toxic Infectious 

Radiculopathy Macroscopic Disk herniation Spondylosis Neoplasia Hemorrhage Abscess  Microscopic Infarction Infectious Inflammatory Neoplastic Demyelinating 

Neuromuscular ­Junction Disorders

Plexopathy

Myopathy

Radiation induced Neoplastic Entrapment Diabetic Hemorrhagic Inflammatory 

Inherited Muscular dystrophy Congenital Metabolic  Acquired Inflammatory Toxic Endocrine Infectious

Postsynaptic Myasthenia gravis Toxic Congenital  Presynaptic Lambert-­Eaton myasthenic syndrome Botulism Toxic Congenital 

LOCALIZATION OF THE DISORDER IS THE MAJOR AIM OF THE ELECTRODIAGNOSTIC STUDY

The principal goal of every EDX study is to localize the disorder. The differential diagnosis is often dramatically narrowed once the disorder has been localized. Broadly speaking, the first order of localization is whether the disorder is neuropathic, myopathic, a disorder of neuromuscular transmission, or a disorder of the CNS. For example, in patients with pure weakness, EDX studies can be used to localize whether the disorder is caused by dysfunction of the motor neurons/axons, NMJs, or muscles or if it has a central etiology. The pattern of nerve conduction and especially EMG abnormalities usually can differentiate among these possibilities and guide subsequent laboratory investigations. For example, a patient with proximal muscle weakness may have spinal muscular atrophy (i.e., a motor neuron disorder), myasthenic syndrome (i.e., a NMJ disorder), or polymyositis (i.e., a muscle disorder) among other conditions, including those with central etiologies (e.g., a parasagittal frontal lesion). EDX studies can easily differentiate among these conditions, providing key information to guide subsequent evaluation and treatment, which differ markedly among these diseases. Once the localization is determined to be neuropathic, myopathic, or a disorder of the NMJ or of the CNS, EDX studies can usually add other important pieces of information to localize the problem further (Fig. 1.2). For instance, the differential diagnosis of a patient with weakness of the hand and numbness of the fourth and fifth fingers includes lesions affecting the ulnar nerve, lower brachial plexus, or C8-­T1 nerve roots. If EDX studies demonstrate an ulnar neuropathy at the elbow, the differential diagnosis is limited to a few conditions, and further diagnostic studies can be directed in a more intelligent manner. In this situation, for instance, there is no need to obtain a magnetic resonance

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Fig. 1.2  Possible localizations determined from the electrodiagnostic study. CNS, Central nervous system; NMJ, neuromuscular junction.

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Chapter 1 • Approach to Nerve Conduction Studies, Electromyography, and Neuromuscular Ultrasound 3

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imaging (MRI) scan of the cervical spine to assess a possible cervical radiculopathy because the EDX studies demonstrated an ulnar neuropathy at the elbow as the source of the patient’s symptoms. This is a situation where neuromuscular U/S may be particularly useful, able to precisely localize the lesion and help assess for anatomic etiologies. In a patient with a CNS disorder who is mistaken as having a peripheral disorder, the EDX study often correctly suggests that the localization is central. For example, transverse myelitis may mimic Guillain-­Barré syndrome, or a small acute cortical stroke may occasionally mimic the pattern of a brachial plexopathy or mononeuropathy. In settings such as these, the EDX study is often the first test to suggest that the correct localization is central rather than peripheral.

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Fig. 1.3  Key electrodiagnostic findings in a neuropathic localization.

Neuropathic is probably the most common localization made on EDX studies. Neuropathic literally means a disorder of the peripheral nerves. However, in common usage, it includes the primary sensory and motor neurons as well. EDX studies are particularly helpful in neuropathic conditions. First, in conjunction with the history and examination, they can usually further localize the disorder to the neurons, roots, plexus, or peripheral nerve. In the case of peripheral nerves, further localization is usually possible to a single nerve (mononeuropathy), multiple individual nerves (mononeuropathy multiplex), or all nerves (polyneuropathy). In the case of a single nerve, the exact segment of nerve responsible for the problem may be localized in some cases. In the case of neuropathic lesions, EDX studies often yield further key information, including the fiber types involved, the underlying pathophysiology, and the temporal course of the disorder (Fig. 1.3).

Conversely, predominantly motor or predominantly sensory neuropathies are rare and suggest a much more limited set of disorders. For instance, a patient with numbness in the hands and feet and diminished reflexes may be diagnosed with a peripheral neuropathy. However, if EDX studies demonstrate abnormal sensory nerve conductions with completely normal motor nerve conductions and needle EMG, then the differential diagnosis changes from a peripheral neuropathy to a pure sensory neuropathy or neuronopathy, which has a much more limited differential diagnosis. Second, EDX studies often can define whether the underlying pathophysiology is demyelination or axonal loss. Although most demyelinating neuropathies have some secondary axonal loss and many axonal loss neuropathies have some secondary demyelination, EDX studies usually can differentiate between a primary demyelinating and a primary axonal neuropathy. Because EDX studies usually can make this differentiation quickly and noninvasively, nerve biopsy is essentially never required to make this determination. Furthermore, the differentiation between primary axonal and primary demyelinating pathology is of considerable diagnostic and prognostic importance, especially in the case of polyneuropathies. Most polyneuropathies are associated with primary axonal degeneration, which has an extensive differential diagnosis. In contrast, the number of true electrophysiologic primary demyelinating neuropathies is extremely small. They are generally subdivided into those that are inherited and those that are acquired (e.g., Charcot Marie Tooth [CMT] vs. CIDP). EDX studies can typically make that determination as well. The finding of an unequivocal primary demyelinating polyneuropathy on EDX studies often leads quickly to the correct diagnosis and, in the case of an acquired demyelinating polyneuropathy, often suggests a potentially treatable disorder. 

Information About the Fiber Types Involved and the Underlying Nerve Pathophysiology can be Gained, Which Then Further Narrows the Differential Diagnosis In the case of neuropathic disorders, the involved fiber types and the underlying pathology can usually be determined. First, EDX studies are more sensitive than the clinical examination in determining which fiber types are involved: motor, sensory, or a combination of the two. Sensorimotor polyneuropathies are common and suggest a large differential diagnosis.

Assessing the Degree of Axonal Loss Versus Demyelination has Implications for Severity and Prognosis A nerve that has sustained a demyelinating injury often can remyelinate in a very short time, usually weeks. However, if there has been substantial axonal loss, whether primary or secondary, the prognosis is much more guarded. The rate of axonal regrowth is limited by the rate of slow axonal transport, approximately 1 mm per day. Clinically, axonal loss

Neuropathic Localization

4

SECTION I  Overview of Nerve Conduction Studies and Electromyography

lesions can rarely be differentiated from demyelinating ones, especially in the acute setting. For example, in a patient who awakens with a complete wrist and finger drop, the etiology usually is compression of the radial nerve against the spiral groove of the humerus. However, the paralysis could result from either conduction block (i.e., demyelination) or axonal loss, depending on the severity and duration of the compression. Clinically, both conditions appear the same. Nevertheless, if the injury is due to axonal loss, it has a much worse prognosis and a longer rehabilitation time to recovery than a similarly placed lesion that is predominantly demyelinating in nature. EDX studies can readily differentiate axonal loss from demyelinating lesions.  Assessment of the Temporal Course can Often be Made For neuropathic conditions, there is an orderly, temporal progression of abnormalities that occurs in NCSs and needle EMG. A combination of findings often allows differentiation among hyperacute (less than 1 week), acute (up to a few weeks), subacute (weeks to a few months), and chronic (more than a few months) lesions. The time course suggested by the EDX findings may alter the impression and differential diagnosis. For example, it is not uncommon for a patient to report an acute time course to his or her symptoms, whereas the EDX studies clearly indicate that the process has been present for a longer period of time than the patient has been aware of. Conversely, the temporal course described by the patient may impact the interpretation of the EDX findings. For instance, the finding of a normal ulnar sensory nerve action potential recording the little finger, in a patient with numbness of the little finger, has very different implications depending on the time course of the symptoms. If the symptoms are truly less than 1 week in duration, the normal ulnar sensory response could indicate an ulnar neuropathy (with wallerian degeneration yet to have been completed), a proximal demyelinating lesion, or a lesion at the level of the nerve root or above. On the other hand, if the symptoms have been present for several weeks or longer, the same finding would indicate either a proximal demyelinating lesion or a lesion at the level of the nerve root or above. These temporal changes underscore the electromyographer’s need to know the clinical time course of symptoms and signs to ensure an accurate interpretation of any electrophysiologic abnormalities. 

Myopathic Localization In the case of myopathic (i.e., muscle) disease, EDX studies can also add key information to further define the condition (Fig. 1.4). First, the distribution of the abnormalities may suggest a diagnosis: are they proximal, distal, or generalized? Most myopathies preferentially affect the proximal muscles. Few myopathies, such as myotonic dystrophy type I, affect distal muscles. Some very severe myopathies (e.g., critical illness myopathy) can be generalized. In rare myopathies, there is prominent bulbar weakness; accordingly, EDX abnormalities may be most prominent in the bulbar muscles. Most myopathies are fairly symmetric; the finding of asymmetry either clinically and/or on EDX studies

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can be very helpful in narrowing the differential diagnosis. For example, inclusion body myositis may present asymmetrically, whereas polymyositis and dermatomyositis do not. Second, the presence of spontaneous activity on needle EMG is helpful in limiting the differential diagnosis and suggesting certain underlying pathologies. Most myopathies are bland, with little or no spontaneous activity. However, myopathies that are inflammatory, necrotic, and some that are toxic or dystrophic may be associated with active denervation. In addition, other myopathies may have prominent myotonic discharges at rest. The presence of myotonic discharges in a myopathy markedly narrows the differential diagnosis to only a few possible disorders. Last is the issue of the temporal course. Although this determination is more challenging than with neuropathic lesions, in some myopathies, a determination can be made if the myopathy is acute, subacute, or chronic, a finding that again narrows the differential diagnosis. 

Neuromuscular Junction Localization Disorders of the NMJ are distinctly uncommon. However, when they occur, EDX studies not only help in identifying them but can also add other key pieces of information (Fig. 1.5). First is the distribution of the abnormalities on EDX

Chapter 1 • Approach to Nerve Conduction Studies, Electromyography, and Neuromuscular Ultrasound 5

testing: are they proximal, bulbar, or generalized? For instance, myasthenia gravis preferentially affects oculobulbar muscles and then proximal muscles on EDX studies, whereas myasthenic syndrome is a generalized disorder on EDX studies, although clinically it has a predilection for proximal muscles. Broadly speaking, the underlying pathology can be divided into presynaptic and postsynaptic disorders. EDX studies are usually very good at making this determination. Myasthenia gravis is the prototypic postsynaptic disorder, whereas myasthenic syndrome and botulism target the presynaptic junction. Last is the issue of the etiology of the NMJ disorder, whether it is acquired or inherited. Almost all NMJ disorders are acquired. However, there are rare inherited NMJ disorders. In some of these, there may be unique findings on EDX testing that suggest one of these rare disorders. 

PATIENT ENCOUNTER Every EDX study begins with a brief history and directed physical examination (Box 1.2). This point cannot be overemphasized! Some may (incorrectly) argue that the history and clinical examinations are not part of the EDX examination and that the EDX study needs to stand on its own. Nothing could be further from the truth. One is not expected to perform the same detailed history and physical examination that is done in the office consultation setting. However, before starting every study, the EDX physician must know some basic facts:    • What are the patient’s symptoms? • How long have they been going on? • Is there any important past medical history (e.g., diabetes, history of chemotherapy, etc.)? • Is there muscle atrophy? • What is the muscle tone (normal, decreased, or increased)? • Is there weakness, and, if so, where is it and how severe is it? • What do the reflexes show (normal, decreased, or increased)? • Is there any loss of sensation, and, if so, what is the distribution; what modalities are disturbed (e.g., temperature, pain, vibration, etc.)?    The duration, type, and distribution of symptoms, along with the physical examination, help determine the differential diagnosis, which in turn is used to plan the EDX studies. The EDX study is planned only after the differential diagnosis is determined. For instance, the EDX evaluation of a patient with slowly progressive proximal weakness is very different from that of a patient with numbness and tingling of the fourth and fifth fingers. In the former case, the differential diagnosis includes disorders of the anterior horn cell, motor nerve, NMJ, or muscle. In the latter case, the differential diagnosis includes an ulnar neuropathy at its various entrapment sites, a lower brachial plexus lesion, or cervical radiculopathy. The EDX plan includes which nerves and muscles to study and whether specialized tests, such as repetitive nerve stimulation, may be helpful. The study can

Box 1.2  Patient Encounter 1. Take a brief history and perform a directed physical examination. 2. Formulate a differential diagnosis. 3. Formulate a study based on the differential diagnosis. 4. Explain the test to the patient. 5. Perform the nerve conduction studies and modify which nerve conduction studies to add, based on the findings as the test proceeds. 6. Perform the needle electromyography study and modify which additional muscles to sample, based on the findings as the test proceeds.

always be amended as the testing proceeds. Before beginning, however, one should first explain to the patient in simple terms what the test involves. Many patients are very anxious about the examination and may have slept poorly or not at all the night before the EDX study. Simple explanations, both before the test begins and while it is ongoing, can greatly reduce a patient’s anxiety. After the test is explained to the patient, the NCSs are performed first, followed by the needle EMG. Indeed, one needs the findings on the NCSs to adapt the needle EMG strategy accordingly and to interpret the needle EMG findings correctly. For instance, active denervation in the abductor digiti minimi (an ulnar, C8–T1 innervated muscle) has a completely different interpretation depending on whether the ulnar motor and sensory NCSs are abnormal or not (ulnar neuropathy in the former, a radiculopathy or motor neuron disease in the latter). A proper balance must be maintained among obtaining a thorough study, collecting the necessary information to answer the clinical question, and minimizing patient discomfort. If performed correctly, nearly all NCSs and needle EMG can be completed within 1–1.5 hours. Rarely, a longer study is needed if specialized tests such as repetitive nerve stimulation are performed in addition to the standard studies. There clearly is a limit to what most patients can tolerate. The electromyographer should always remember the Willy Sutton rule concerning robbing banks: “Go where the money is.” If there is any question as to whether a patient will tolerate the entire examination, the study should begin with the area of interest. For instance, in the patient with numbness and tingling of the fourth and fifth fingers, ulnar motor and sensory studies should be done first. Likewise, needle EMG examination of the ulnar-­innervated muscles, as well as the C8–T1 non-­ulnar–innervated muscles, are of most interest in such a patient. Plan and consider which NCSs and needle examination of which muscles should be performed first, in case the patient can tolerate only one or two nerve conductions or examination of only a few muscles by EMG. 

CARDINAL RULES OF NERVE CONDUCTION STUDIES AND ELECTROMYOGRAPHY

EDX studies rely on the physician’s ability to pay meticulous attention to technical details during the study while

6

SECTION I  Overview of Nerve Conduction Studies and Electromyography

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Fig. 1.6  Cardinal rules of nerve conduction studies and electromyography. EDX, Electrodiagnostic; EMG, electromyography; NCS, nerve conduction study.

keeping in mind the bigger picture of why the study is being performed. As more data are obtained, the study must be analyzed in real time and the test altered as needed. Analysis of online results gives the electromyographer the opportunity to modify the strategy as the testing proceeds, an opportunity that is lost once the patient has left the laboratory. The following cardinal rules of EDX studies should always be kept in mind while an EDX study is being performed (Fig. 1.6):    1. NCSs and EMG are an extension of the clinical examination. NCSs and EMG cannot be performed without a good directed clinical examination. Every examination must be individualized based on the patient’s symptoms and signs and the resulting differential diagnosis. If marked abnormalities are found on electrophysiologic testing in the same distribution where the clinical examination is normal, either the clinical examination or the electrophysiologic testing must be called into question. One usually finds that the better the clinical examination, the better the differential diagnosis, and thus, the more clearly directed the EDX studies will be. 2. When in doubt, always think about technical factors. EDX studies rely upon collecting and amplifying very small bioelectric signals in the millivolt and microvolt range. Accomplishing this is technically demanding; many physiologic and nonphysiologic factors can significantly interfere with the accuracy of the data. Accurate NCSs and EMG depend on intact equipment (e.g., EMG machine, electrodes, and stimulator), and on correct performance of the study by the electromyographer. Technical problems can easily lead to absent or abnormal findings. Failure to recognize technical factors that influence the EDX study can result in type I errors (i.e., diagnosing an

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abnormality when none is present) and type II errors (i.e., failing to recognize an abnormality when one is present). Although both are important, type I errors are potentially more serious (e.g., the patient is labeled with an abnormal EDX study result, such as neuropathy, when the “abnormality” on the EDX testing is simply due to unrecognized technical errors). Such faulty diagnoses can lead to further inappropriate testing and treatment. If there is an unexpected abnormal EDX finding that does not fit the clinical examination, the lack of a clinical-­electrophysiologic correlation should suggest a technical problem. For instance, if a routine sural nerve sensory conduction study shows an absent potential but the patient has a normal sensory examination of the lateral foot (i.e., sural territory), one should suspect a technical problem (e.g., improper electrode or stimulator placement or too low of a stimulus intensity). If the data are not technically accurate, then correct data interpretation can never occur, either at the time of the study or later by the treating physician. 3. When in doubt, reexamine the patient. This is essentially an extension of cardinal rule number 1. In the example given with rule number 2, if the sural sensory response is absent after all possible technical factors have been corrected, the clinician should reexamine the patient. If the patient has clear loss of vibration at the ankles, there is less concern about an absent sural sensory response. If the patient’s sensory examination is normal on reexamination, the absent sensory response does not fit the clinical findings, and technical factors should be investigated further. 4. EDX findings should be reported in the context of the clinical symptoms and the referring diagnosis. In every study, electrophysiologic abnormalities must be correlated with the clinical deficit.

Chapter 1 • Approach to Nerve Conduction Studies, Electromyography, and Neuromuscular Ultrasound 7

Because electrophysiologic studies are quite sensitive, it is not uncommon for the electromyographer to discover mild, subclinical deficits of which the patient may not be aware. For example, a diabetic patient referred to the EMG laboratory for polyneuropathy may show electrophysiologic evidence of a superimposed ulnar neuropathy but have no symptoms of such. Accordingly, the electromyographer should always report any electrophysiologic abnormality in the context of its clinical relevance so that it can be properly interpreted. 5. When in doubt, do not overcall a diagnosis. Because electrophysiologic tests are very sensitive, mild, subclinical, and sometimes clinically insignificant findings often appear on EDX testing. This occurs partly because of the wide range of normal values, which vary with the nerve and muscle being tested. In addition, there are a variety of physiologic and nonphysiologic factors that may alter the results of both NCSs and EMG, despite attempts to control for them. These factors, often when combined, may create minor abnormalities. Such minor abnormalities should not be deemed relevant unless they correlate with other electrophysiologic findings and, most importantly, with the clinical history and examination. It is a mistake to overcall an electrophysiologic diagnosis based on minor abnormalities or on findings that do not fit together well. Sometimes, the clinical or electrophysiologic diagnosis is not clear-­cut and a definite diagnosis cannot be reached. Occasionally, NCSs and EMG are clearly and definitely abnormal, but a precise diagnosis still cannot be determined. For example, consider the patient whose clinical history and examination suggest an ulnar neuropathy at the elbow. The EDX study often demonstrates abnormalities of the ulnar nerve in the absence of any localizing findings, such as conduction block or slowing across the elbow. Although the referring surgeon usually wants to know whether the ulnar neuropathy is at the elbow, often, the only accurate impression that the electromyographer can give is one of a non-­localizable ulnar neuropathy that is at, or proximal to, the most proximal abnormal ulnar-­ innervated muscle found on EMG. 6. Always think about the clinical-­electrophysiologic correlation. This rule combines all of the earlier rules. One usually can be certain of a diagnosis when the clinical findings, NCSs, and EMG abnormalities all correlate well. Consider again the example of the patient with weakness of the hand and tingling and numbness of the fourth and fifth fingers. If NCSs demonstrate abnormal ulnar motor and sensory potentials associated with slowing across the elbow, and the needle EMG shows denervation and reduced numbers of motor unit potentials in all ulnar-­ innervated muscles and a normal EMG of all non-­ ulnar–innervated muscles, there is a high degree of certainty that the patient truly has an ulnar neuropathy at the elbow, and the electrophysiologic abnormalities are indeed relevant.   

If all three results fit together, the diagnosis is secure. However, if the NCSs and EMG findings do not fit together and, more importantly, if they do not correlate with the clinical findings, the significance of any electrical abnormalities should be seriously questioned. Consider a patient with pain in the arm who has an otherwise normal history and examination. If the NCSs are normal except for a low ulnar sensory potential and the EMG demonstrates only mild reinnervation of the biceps, one should be reluctant to interpret the study as showing a combination of an ulnar neuropathy and a C5 radiculopathy. These mild abnormalities, which are not substantiated by other electrophysiologic findings and do not have clear clinical correlates, may have little to do with the patient’s pain. In such a case, the patient should be reexamined. If no clinical correlate is found, the studies should be rechecked. If the abnormalities persist, they may be noted as part of the impression but interpreted as being of uncertain clinical significance. When performed properly, NCSs and EMG can be very helpful to the referring physician. However, the limitations of EDX studies must be appreciated, technical factors well controlled, and a good differential diagnosis established before each study. Otherwise, the study may actually do a disservice to the patient and to the referring physician by leading them astray by way of minor, irrelevant, or technically induced “abnormalities.” If the cardinal rules of NCSs and EMG are kept in mind, EDX studies are far more likely to be of help to the referring clinician and the patient with a neuromuscular disorder. 

NEUROMUSCULAR ULTRASOUND Over the last several years, neuromuscular U/S has increasingly been used along with EDX studies in the evaluation of patients with various neuromuscular conditions. The use of neuromuscular U/S has grown due to a combination of several factors, including the marked improvement of the resolution and software of U/S machines while the physical size and cost of the machines have gone down. These smaller, portable machines can easily be used and shared among EDX laboratory rooms. Indeed, some manufacturers are working on combined EDX and U/S machines housed in one unit. Hundreds of peer-­reviewed articles on the usefulness of neuromuscular U/S are published each year. Thus, neuromuscular U/S has become a validated, reliable, and important tool in the evaluation of many neuromuscular disorders. Physicians who perform EDX studies are best suited to learn and perform neuromuscular U/S, which is the study of peripheral nerves and muscles. Neuromuscular U/S differs from vascular U/S and musculoskeletal U/S, although there is some overlap. It is essential to emphasize that neuromuscular U/S is complementary to EDX studies; it does not replace EDX studies. The situation is similar to the role that EDX studies and MRI have in the evaluation of radiculopathy. EDX studies are physiologic tests and, as such, yield information about the function of the nerves, nerve roots, and muscles. In contrast, imaging studies show a picture of

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SECTION I  Overview of Nerve Conduction Studies and Electromyography

the nerves, nerve roots, and muscles, but yield no information on the functioning. Thus, for example, whereas EDX studies give information about how well the nerve root is functioning, an MRI can show the nerve roots and whether they appear impinged by a disk, spondylosis, or other structural causes. Likewise, whereas EDX studies may be able to identify an ulnar neuropathy at the elbow, they cannot discern what is causing it. This is where neuromuscular U/S may add critical complementary information to the EDX studies. For example, it may reveal bony spurs and excess callus in the ulnar groove from tardy ulnar palsy, compression of the ulnar nerve in the true cubital tunnel under the humeral-­ulnar aponeurosis, or in some cases a synovial cyst compressing the ulnar nerve, among many possible etiologies. Best used, neuromuscular U/S serves as an extension of the clinical examination and most often of the EDX studies, and should be used as such. Chapters 17, 18, and 19 discuss neuromuscular U/S in greater detail. In addition, many of the later clinical chapters expand on the usefulness of neuromuscular U/S in specific conditions. Similar to EDX studies, there are several general principles of neuromuscular U/S. Each neuromuscular U/S study must be individualized, based on the neurologic examination, the EDX study, and the differential diagnosis, and modified as the study progresses and further information is gained. Its primary use is to add anatomic and pathologic information that complements the EDX study. Among neuromuscular U/S’s many potential uses, the major ones are described in the following sections.

Peripheral Nerve: Mononeuropathy In general, U/S is particularly helpful in many mononeuropathies. Mononeuropathies are commonly caused by entrapment, trauma, and in some cases other structural causes. When the EDX study has localized the problem to one segment of one peripheral nerve (e.g., the median nerve at the carpal tunnel), U/S can confirm the localization by revealing structural changes in the nerve at the involved site. In the case of carpal tunnel syndrome, U/S usually simply adds additional confirmatory evidence of the nerve location, although as we will see later in Chapter 20 on Median Neuropathy at the Wrist, U/S may add more information, especially in postoperative cases or when symptoms recur. In other cases of mononeuropathy, when the EDX study localizes the problem to one nerve but is not able to localize a specific segment, U/S can be particularly useful. This occurs when the pathophysiology is that of axonal loss. In this situation, U/S is particularly helpful as it can often localize the lesion more precisely than EDX studies. Take the example of the patient with a weak grip and numbness involving digit 5. An ulnar neuropathy is considered most likely. The EDX study might show abnormalities limited to the ulnar nerve, but there is no slowing or conduction block across the elbow. Is the lesion at the elbow? Or is it as the wrist, in the forearm, upper arm, or in the lower brachial plexus? U/S can visualize the ulnar nerve from the wrist to

its origin in the lower brachial plexus and assess for structural abnormalities to localize the lesion. Regardless of whether the EDX study can definitely localize the mononeuropathy or not, it is important to know what is causing it. Is it an entrapment from wear and tear? Or from tenosynovitis? Or from compression from a ganglion cyst? Or from a nerve sheath tumor? And the list continues. This is also where U/S may add critical anatomic information about what is causing the mononeuropathy. Performing U/S after EDX studies for a mononeuropathy may result in three different outcomes:    1. It may add no useful information, or 2. It may add important complementary information, or 3. It may be the key to the case.    Unfortunately, one does not know before doing the U/S study which of these three outcomes will be the result. Thus, one can make a strong argument that U/S is a reasonable adjunct to EDX studies for most mononeuropathies. 

Peripheral Nerve: Polyneuropathy The role of neuromuscular U/S in polyneuropathy is most useful when looking for evidence of a hypertrophic (usually meaning demyelinating) polyneuropathy. As will be discussed in Chapter 29 on Polyneuropathy, the vast majority of polyneuropathies display an axonal loss pattern on EDX studies. Very few are primarily demyelinating. However, the presence of demyelination on EDX studies of a polyneuropathy is a critical piece of information, as it markedly narrows the differential diagnosis. Furthermore, in the case of acquired demyelinating polyneuropathies, most are inflammatory (autoimmune) and potentially very treatable. The U/S picture of a chronic demyelinating polyneuropathy is usually that of a hypertrophic neuropathy (from repeated demyelination and remyelination, Schwann cell proliferation, and onion blub formation). EDX studies may be indeterminate in some chronic demyelinating neuropathies. Sometimes, this is due to responses being absent. In others, the EDX criteria for demyelination are not fully met, or the conduction velocities are in the borderline range between axon loss and demyelination. In these cases, presumably the demyelination is not marked enough to call, or the segments of nerve that are demyelinated are not easily assessed by standard EDX studies (e.g., very proximal nerves, plexus, and/or roots). Hence, U/S can be extremely useful in establishing a polyneuropathy as demyelinating. 

Motor Neuron Disease EDX studies in conjunction with the history and physical examination are the cornerstones of diagnosing motor neuron disease. U/S has a limited role in the diagnosis of motor neuron disease, with a couple of notable exceptions. First, U/S is extremely good at detecting fasciculations— better than the clinical examination and needle EMG. The research criteria for the diagnosis of motor neuron disease (and qualification for clinical studies) requires evidence of

Chapter 1 • Approach to Nerve Conduction Studies, Electromyography, and Neuromuscular Ultrasound 9

denervation and reinnervation on EDX studies. However, more recent criteria accept the presence of fasciculations along with reinnervation as evidence of ongoing lower motor neuron loss. Thus, U/S can be very helpful in more easily detecting fasciculations. Second, a diagnostic dilemma often arises in patients with suspected motor neuron disease when they present with a pure lower motor neuron syndrome without any definite upper motor neuron signs. This syndrome is typically designated as the progressive muscular atrophy (PMA) form of motor neuron disease. However, in such patients, the question often remains whether the patient has a motor neuron disorder, such as PMA, or a motor nerve disorder. True motor nerve disorders are rare, but when they occur, they typically mimic PMA. Oftentimes, EDX studies cannot distinguish between these two, especially when conduction blocks are very proximal or motor NCSs are in the borderline range. Motor neuropathies are most often inflammatory and treatable. Variants of CIDP, but more often, multifocal motor neuropathy with conduction block (MMNCB) may present as pure lower motor neuron weakness. In these conditions, U/S may demonstrate hypertrophic nerves, whereas in amyotrophic lateral sclerosis (ALS), PMA, and other motor neuron disorders, nerve size is normal or even small. Thus, U/S should be strongly considered in all patients presenting as a pure lower motor neuron syndrome. 

Myopathy The original reports of using U/S in neuromuscular disorders come from evaluation of young boys with Duchenne muscular dystrophy. Like motor neuron disease, the use of U/S in myopathies is limited, but with a few notable exceptions. First, U/S can easily screen many muscles at one sitting. The pattern formed by which muscles are abnormal and which are spared is increasingly used to help limit the differential diagnosis in myopathies. U/S is much quicker and less expensive than MRI in establishing the pattern of muscle involvement and can screen all four limbs, proximally and distally, in one sitting. Certain myopathies have a characteristic pattern of muscle involvement. For instance, in inclusion body myositis, sparing of the rectus femoris compared to the other quadriceps muscles and the involvement of the forearm finger flexors are both highly suggestive of the diagnosis, in the proper clinical context. Second, U/S may be useful in identifying a muscle site for biopsy. The best yield of a muscle biopsy is in choosing a muscle that is abnormal but not end stage. Needle EMG is often used in this regard, but one then needs to biopsy the muscle on the contralateral side to the muscle identified on needle EMG as the optimal site. If one biopsied the muscle sampled with needle EMG, the biopsy might include the area where the needle had been placed, which could result in inflammation and other injury along the needle track and carries the inherent risk of diagnosing an inflammatory myopathy incorrectly. Using U/S, one can biopsy the specific muscle that was examined and determined to be optimal, without the need to choose the contralateral side. 

CARDINAL RULES OF NEUROMUSCULAR ULTRASOUND

Similar to EDX studies, neuromuscular U/S relies on the physician’s ability to perform and interpret the study correctly and analyze the findings in real time, altering the study as needed. The following cardinal rules of neuromuscular U/S should always be kept in mind when performing a study (Fig. 1.7):    1. Neuromuscular U/S is complementary to the EDX study. As emphasized earlier, EDX assesses the physiologic function of nerve and muscle, whereas U/S imaging of nerve and muscle is used to provide anatomic and, possibly, pathologic etiologic information. These are complementary pieces of information that, when used together, allow more accurate and complete information on the nature of the neuromuscular disorder. 2. Each U/S study should be tailored for the individual patient. Each study must be tailored to the individual patient and differential diagnosis. Properly used, neuromuscular U/S is used after the EDX study is completed to answer specific questions. It is not desirable or practical to image all nerves and all muscles. The specific neuromuscular U/S study done will be different for each patient. 3. Fully evaluate any abnormalities. When any “abnormality” is seen on U/S, one must define it to the fullest extent possible. Always look at the abnormality in at least two planes. Just like MRI, when an “abnormality” is seen on a sagittal image but not on the axial image, it is probably an artifact. Use the color Doppler to look for increased blood flow, which may occur with inflammation, infection, or neoplasia. Check for compressibility and mobility. Note the echogencity (i.e., how bright or how dark the lesion is). Look for the classic U/S findings of posterior acoustic enhancement or shadowing. Then, look closely at the nearby structures: bone, tendon, ligament, and blood vessel. If possible, do a dynamic evaluation and see what happens &DUGLQDOUXOHVRI QHXURPXVFODU86 1HXURPXVFXODU86LV FRPSOHPHQWDU\WR('; VWXGLHV (DFKVWXG\VKRXOGEH WDLORUHG WRWKHLQGLYLGXDOSDWLHQW

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Fig. 1.7  Cardinal rules of neuromuscular ultrasound. EDX, ­Electrodiagnostic; U/S, ultrasound.

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SECTION I  Overview of Nerve Conduction Studies and Electromyography

to the lesion with passive range of motion, or during voluntary contraction of nearby muscles. Take lots of still pictures and movie clips, all of which will help you later in making your determination. 4. When in doubt, think about technical factors, artifacts, and anomalies. U/S has its own set of artifacts and technical factors (see Chapter 17). If not recognized, these can lead to the mistaken impression of pathology when none actually exists. Similar to EDX studies, such faulty diagnoses can lead to inappropriate testing and treatment. In addition, when performing U/S, it is not uncommon to encounter anatomic anomalies of nerve, muscle, and blood vessel. One quickly appreciates that every patient’s anatomy does not necessarily follow the textbook. Sometimes, these anatomic anomalies are actually the cause of the patient’s problem; in other cases, they are simply incidental findings. 5. When in doubt, do not overcall a diagnosis. This general rule is equally applicable to EDX studies and all other laboratory and radiographic tests. It is not uncommon to find minor abnormalities of unclear significance or to misinterpret technical issues as findings. It is a mistake to overcall any diagnosis based on minor abnormalities or findings that do not fit together with the clinical presentation. 6. Always think about the clinical-­electrophysiologic-­ ultrasound correlation. This is simply an extension of the final cardinal rule of EDX. One usually can be certain of a diagnosis when the clinical findings, NCSs, EMG, and U/S abnormalities all correlate well. Consider again the example of the patient with weakness of the hand and tingling and numbness of the fourth and fifth fingers. If NCSs demonstrate abnormal ulnar motor and sensory potentials associated with slowing across the elbow, the needle EMG shows denervation and a reduced number of motor unit potentials in all ulnar-­innervated muscles and a

normal EMG of all non-ulnar–innervated muscles, and the U/S shows an enlarged, hypoechoic ulnar nerve under the humeral-­ulnar aponeurosis at the true cubital tunnel without any other pathology; there is a very high degree of certainty that the patient truly has an ulnar neuropathy at the elbow. In this case, the electrophysiological abnormalities are indeed relevant, with the U/S demonstrating the etiology of the ulnar nerve entrapment at the cubital tunnel.

Suggested Readings Cocito D, Tavella A, Ciaramitaro P, Costa P, Poglio F, Paolasso I, et al. A further critical evaluation of requests for electrodiagnostic examinations. Neurol Sci. 2006;26(6):419–422. Haig AJ, Tzeng HM, LeBreck DB. The value of electrodiagnostic consultation for patients with upper extremity nerve complaints: a prospective comparison with the history and physical examination. Arch Phys Med Rehabil. 1999;80(10):1273–1281. Kothari MJ, Blakeslee MA, Reichwein R, Simmons Z, Logigian EL. Electrodiagnostic studies: are they useful in clinical practice? Arch Phys Med Rehabil. 1998;79(12):1510–1511. Kothari MJ, Preston DC, Plotkin GM, Venkatesh S, Shefner JM, Logigian EL. Electromyography: do the diagnostic ends justify the means? Arch Phys Med Rehabil. 1995;76(10):947–949. Lindstrom H, Ashworth NL. The usefulness of electrodiagnostic studies in the diagnosis and management of neuromuscular disorders. Muscle Nerve. 2018;58(2):191–196. Mondelli M, Aretini A, Greco G. Requests of electrodiagnostic testing: consistency and agreement of referral diagnosis. What is changed in a primary outpatient EDX lab 16 years later? Neurol Sci. 2014;35(5):669–675. Mondelli M, Giacchi M, Federico A. Requests for electromyography from general practitioners and specialists: critical evaluation. Ital J Neurol Sci. 1998;19(4):195–203.

SECTION I • Overview of Nerve Conduction Studies and Electromyography

Anatomy and Neurophysiology for Electrodiagnostic Studies The electromyographer need not have detailed knowledge of all the electrical and chemical events that occur at a molecular level to perform an electrodiagnostic (EDX) study. However, one must have a basic understanding of anatomy and physiology to plan, perform, and properly interpret an EDX study. In the everyday evaluation of patients with neuromuscular disorders, nerve conduction studies (NCSs) and electromyography (EMG) serve primarily as extensions of the clinical examination. For NCSs, one needs to know the location of the various peripheral nerves and muscles so that the stimulating and recording electrodes are properly positioned. For the needle EMG study, knowledge of gross muscle anatomy is crucial for inserting the needle electrode correctly into the muscle being sampled. On the microscopic level, knowledge of nerve and muscle anatomy and basic neurophysiology is required to appreciate and interpret the EDX findings both in normal individuals and in patients with various neuromuscular disorders. In addition, knowledge of anatomy and physiology is crucial to understanding the technical aspects of the EDX study and appreciating its limitations and potential pitfalls.

ANATOMY The strict definition of the peripheral nervous system includes that part of the nervous system in which the Schwann cell is the major supporting cell, as opposed to the

2

central nervous system in which the glial cells are the major supporting cells. The peripheral nervous system includes the nerve roots, peripheral nerves, primary sensory neurons, neuromuscular junctions (NMJs), and muscles (Fig. 2.1). Although not technically part of the peripheral nervous system, the primary motor neurons (i.e., anterior horn cells), which are located in the spinal cord, are usually included as part of the peripheral nervous system as well. In addition, cranial nerves III through XII are also considered to be part of the peripheral nervous system, being essentially the same as peripheral nerves, except that their primary motor neurons are located in the brainstem rather than the spinal cord. The primary motor neurons, the anterior horn cells, are located in the ventral gray matter of the spinal cord. The axons of these cells ultimately become the motor fibers in peripheral nerves. Their projections first run through the white matter of the anterior spinal cord before exiting ventrally as the motor roots. In contrast to the anterior horn cell, the primary sensory neuron, also known as the dorsal root ganglion (DRG), is not found within the substance of the spinal cord itself but rather lies outside the spinal cord, near the intervertebral foramen. The DRG are bipolar cells with two separate axonal projections. Their central projections form the sensory nerve roots. The sensory roots enter the spinal cord on the dorsal side to ascend in either the posterior columns or synapse with sensory neurons in the dorsal horn. The peripheral projections of the DRGs ultimately become the sensory fibers in peripheral nerves. Because the DRGs

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Fig. 2.1  Elements of the peripheral nervous system.  The peripheral nervous system includes the peripheral motor and sensory nerves; their primary neurons, the anterior horn cells, and dorsal root ganglia; the neuromuscular junctions (NMJs); and muscle. The dorsal root ganglion, a bipolar cell located distal to the sensory root, is anatomically different from the anterior horn cell. Consequently, lesions of the nerve roots result in abnormalities of motor nerve conduction studies but do not affect the sensory conduction studies, as the dorsal root ganglion and its peripheral nerve remain intact.

11

12

SECTION I  Overview of Nerve Conduction Studies and Electromyography

lie outside the spinal cord, this results in a different pattern of sensory nerve conduction abnormalities, depending on whether the lesion is in the peripheral nerve or proximal to the DRG at the root level (see Chapter 3). Motor and sensory roots at each spinal level unite distal to the DRG to become a mixed spinal nerve. There are 31 pairs of spinal nerves (8 cervical, 12 thoracic, 5 lumbar, 5 sacral, 1 coccygeal; Fig. 2.2). Each spinal nerve divides into a dorsal and ventral ramus (Fig. 2.3). Unlike the dorsal and ventral nerve roots, the dorsal and ventral rami both contain , &  ,,  ,,,   ,; ;   ;,  ;,, 7

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motor and sensory fibers. The dorsal ramus runs posteriorly to supply sensory innervation to the skin over the spine and muscular innervation to the paraspinal muscles at that segment. The ventral ramus differs, depending on the segment within the body. In the thoracic region, each ventral ramus continues as an intercostal nerve. In the lower cervical to upper thoracic (C5–T1) region, the ventral rami unite to form the brachial plexus (Fig. 2.4). In the mid-­lumbar to sacral regions, the ventral rami intermix to form the lumbosacral plexus (Fig. 2.5). Within each plexus, motor and sensory fibers from different nerve roots intermix to ultimately form individual peripheral nerves. Each peripheral nerve generally supplies muscular innervation to several muscles and cutaneous sensation to a specific area of skin, as well as sensory innervation to underlying deep structures. Because of this arrangement, motor fibers from the same nerve root supply muscles innervated by different peripheral nerves, and sensory fibers from the same nerve root supply cutaneous sensation in the distribution of different peripheral nerves. For instance, the C5 motor root supplies the biceps (musculocutaneous nerve), deltoid (axillary nerve), and brachioradialis (radial nerve), among other muscles (Fig. 2.6). Similarly, C5 sensory fibers innervate the lateral arm (axillary nerve) and forearm (lateral antebrachial cutaneous sensory nerve), in addition to other nerves. All muscles supplied by one spinal segment (i.e., one nerve root) are known as a myotome, whereas all cutaneous

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Fig. 2.3  Nerve roots and rami.  The motor root, originating from anterior horn cells, leaves the cord ventrally, whereas the sensory root enters the cord on the dorsal side. Immediately distal to the dorsal root ganglion, the motor and sensory roots come together to form the spinal nerve. Each spinal nerve quickly divides into a dorsal and ventral ramus. Each ramus contains both motor and sensory fibers. The dorsal rami supply sensation to the skin over the spine and muscular innervation to the paraspinal muscles. The ventral rami continue as intercostal nerves in the thoracic region. In the lower cervical region, the ventral rami fuse to form the brachial plexus. In the mid-­lumbar through sacral segments, the ventral rami intermix to form the lumbosacral plexus.

Chapter 2 • Anatomy and Neurophysiology for Electrodiagnostic Studies 13

areas supplied by a single spinal segment are known as a dermatome (Fig. 2.7). For both myotomes and dermatomes, there is considerable overlap between adjacent segments. Because of the high degree of overlap between spinal segments, a single root lesion seldom results in significant sensory loss and never in anesthesia. Likewise, on the motor side, even a severe single nerve root lesion usually results in only mild or moderate weakness and never in paralysis. For instance, a severe lesion of the C6 motor root causes weakness of the biceps; however, paralysis would not occur because C5 motor fibers also innervate the biceps. In contrast, a severe peripheral nerve lesion usually results in marked sensory and motor deficits because contributions from several myotomes and dermatomes are affected simultaneously. At the microscopic level, nerve fibers are protected by three different layers of connective tissue: the epineurium, perineurium, and endoneurium (Fig. 2.8). The thick epineurium surrounds the entire nerve and is in continuity with the dura mater at the spinal cord level. Within the epineurium, axons are grouped into fascicles, surrounded by perineurium. A final layer of connective tissue, the endoneurium, is present between individual axons. Effectively, a blood-­nerve barrier is formed by the combination of vascular endothelium supplying the nerve and the connective tissue of the perineurium. Together, the three layers of connective tissue give peripheral nerve considerable tensile strength, usually in the range of 20–30 kg. However, the weakest point of a 7UXQNV

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nerve occurs where the nerve roots meet the spinal cord, where the nerve can sustain only 2–3 kg of force. For this reason, nerve root avulsion may occur after a significant trauma and especially after a stretch injury. Analogous to nerve fibers, muscle fibers have a very similar arrangement at the microscopic level with three layers of connective tissue: the epimysium, perimysium, and endomysium (Fig. 2.9). The epimysium surrounds the entire muscle. Within the epimysium, muscle fibers (which are the actual muscle cells) are grouped into fascicles surrounded by the perimysium. The final layer of connective tissue, the endomysium, is present between individual muscle fibers. Muscle fibers are cylindrical and contain the actual muscle fibrils: the structural proteins that are responsible for muscle contraction. When muscle contraction occurs, the force is transmitted most often to a bone to move a joint (occasionally, muscle is connected to other connective tissue or the skin). This connection is most often made by way of a tendon, which is a thick rope-­like piece of connective tissue that is in continuity with the epimysium of the muscle. In some muscles, the contraction is by way of an aponeurosis, which is a large, sheet-­like piece of connective tissue. Most muscles have two tendons, one at their origin (typically proximal and more static) and one at their insertion (typically more distal and more mobile). In some muscles, the tendon originates from inside the muscle, known as an internal or central tendon. 

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Fig. 2.4  Brachial plexus.  The ventral rami of the C5–T1 nerve roots intermix to form the brachial plexus between the neck and shoulder. From the brachial plexus, the major upper extremity peripheral nerves are derived. (From Hollinshead WH. Anatomy for Surgeons, Volume 2: The Back and Limbs. New York: Harper & Row; 1969, with permission.)

14

SECTION I  Overview of Nerve Conduction Studies and Electromyography

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Fig. 2.5  Lumbosacral plexus.  The L1–S4 nerve roots intermix in the pelvis to form the lumbosacral plexus. From this plexus, the individual major peripheral nerves of the lower extremity are derived. (From Mayo Clinic and Mayo Foundation. Clinical Examinations in Neurology. Philadelphia: WB Saunders; 1956, with permission.)

PHYSIOLOGY The primary role of nerve is to transmit information reliably from the anterior horn cells to muscles for the motor system and from the sensory receptors to the spinal cord for the sensory system. Although functionally nerves may seem similar to electrical wires, there are vast differences between the two. At the molecular level, a complex set of chemical and electrical events allows nerve to propagate an electrical signal. The axonal membrane of every nerve is electrically active. This property results from a combination of a specialized membrane and the sodium/potassium (Na+/K+) pump (Fig. 2.10). The specialized axonal membrane is semipermeable to electrically charged molecules (anions

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and cations). The membrane is always impermeable to large negatively charged anions, and it is relatively impermeable to sodium in the resting state. This semipermeable membrane, in conjunction with an active Na+/K+ pump that moves sodium outside in exchange for potassium, leads to concentration gradients across the membrane. The concentration of sodium is larger outside the membrane, whereas the concentration of potassium and larger anions is greater inside. The combination of these electrical and chemical gradients results in forces that create a resting equilibrium potential. At the nerve cell soma, this resting membrane potential is approximately 70 mV negative inside compared with the outside; distally in the axon it is approximately 90 mV negative. The membrane of the axon is lined with voltage-­gated sodium channels (Fig. 2.11). These structures are essentially molecular pores with gates that open and close. For many ion channels, gates open in response to molecules that bind to the channel. In the case of the voltage-­gated sodium channel, the gate is controlled by a voltage sensor that responds to the level of the membrane potential. If current is injected into the axon, depolarization occurs (i.e., the axon becomes more positive internally). Voltage sensors within the sodium channel respond to the depolarization by

Chapter 2 • Anatomy and Neurophysiology for Electrodiagnostic Studies 15

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Fig. 2.7  Dermatomes.  The cutaneous area supplied from one spinal segment (i.e., one sensory nerve root) is known as a dermatome. Despite the apparent simplicity of dermatomal charts, in actuality there is a wide overlap of adjacent dermatomes. Consequently, a nerve root lesion, even if severe, never results in anesthesia but rather results in altered or decreased sensation. (From O’Brien MD. Aids to the Examination of the Peripheral Nervous System. London: Baillière Tindall; 1986.)

Fig. 2.8  Internal peripheral nerve anatomy. Myelinated fibers are recognized as small dark rings (myelin) with a central clearing (axon) in this 1-­micron thick, semi-­thin section of plastic embedded nerve tissue. The endoneurium is present between axons. Axons are grouped into fascicles, surrounded by perineurium (small arrows). Surrounding the entire nerve is the last layer of connective tissue, the epineurium (large arrow).

SECTION I  Overview of Nerve Conduction Studies and Electromyography

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Fig. 2.9  Internal muscle anatomy.  The endomysium is present between muscle fibers. Muscle fibers are grouped into fascicles, surrounded by perimysium. Surrounding the entire muscle is the last layer of connective tissue, the epimysium.

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opening the gate to the channel and allowing sodium to rush into the axon, driven both by concentration and by electrical gradients. Every time a depolarization of 10–30 mV above the resting membrane potential occurs (i.e., threshold), it creates an action potential and a cycle of positive feedback; further depolarization occurs and more sodium channels open (Fig. 2.12). Action potentials are always all-­or-­none responses that then propagate away from the initial site of depolarization. The axon does not remain depolarized for long, however, because the opening of the sodium channels is time limited. Sodium channels have a second gate, known as the inactivation gate. Inactivation of the sodium channel occurs within 1–2 ms. During this time, the membrane is not excitable and cannot be opened (i.e., refractory period). The inactivation gate of the sodium channel has been modeled as a “hinged lid.” From a practical point of view, the refractory period limits the frequency that nerves can conduct impulses. It also ensures that the action potential continues to propagate in the same direction (i.e., the area of

nerve behind the depolarization is refractory when the area ahead is not so that the impulse will continue forward and will not return backward). In addition to sodium channel inactivation, depolarization also results in the opening of potassium channels, which also then drives the membrane voltage in a more negative direction. These factors, along with the Na+/K+ pump, then reestablish the resting membrane potential. The conduction velocity of the action potential depends on the diameter of the axon: the larger the axon, the less resistance and the faster the conduction velocity. For typical unmyelinated axons, the conduction velocity of an action potential is very slow, typically in the range of 0.2– 1.5 m/s. Conduction velocity can be greatly increased with the addition of myelin. Myelin insulation is present on all fast-­conducting fibers and is derived from Schwann cells, the major supporting cells in the peripheral nervous system. Myelin is composed of concentric spirals of Schwann cell membrane (Fig. 2.13). For every myelinated fiber,

Chapter 2 • Anatomy and Neurophysiology for Electrodiagnostic Studies 17

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     Fig. 2.12  Action potential.  When the resting membrane voltage (Vm) is depolarized to threshold, voltage-­gated sodium channels are opened, increasing Na+ conductance (gNa), resulting in an influx of sodium and further depolarization. The action potential, however, is short lived, due to the inactivation of the sodium channels within 1–2 ms and an increase in K+ conductance (gK). These changes, along with the Na+/K+ pump, allow the axon to reestablish the resting membrane potential.









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successive segments are myelinated by single Schwann cells. Each segment of the axon covered by myelin is termed the “internode.” At small gaps between successive internodes, the axon is exposed; these areas are known as the nodes of Ranvier. They are very small, in the range of 1–2 μm in length. Most of the nerve is effectively insulated with myelin, and depolarization occurs by way of saltatory conduction, whereby depolarization occurs only at the nodes of Ranvier. After one node depolarizes, the current essentially jumps to the next adjacent node, and the cycle continues (Fig. 2.14). The physiology of normal saltatory conduction was first shown in a series of elegant experiments on normal animal myelinated nerve fibers, recording along the motor root in very small increments and measuring the current as a function of distance and latency (Fig. 2.15). From an electrical point of view, myelin insulates the internode and reduces the capacitance. A lower capacitance results in less current lost as the action potential travels from node to node. Although more current is needed for saltatory conduction than for continuous conduction, much less

Fig. 2.14  Saltatory conduction.  Myelinated fibers propagate action potentials by way of saltatory conduction. Depolarization only occurs at the small uninsulated areas of membrane between internodes, with the action potential essentially jumping from node to node. Thus, less membrane needs to be depolarized, less time is required, and, consequently, conduction velocity dramatically increases. Most human peripheral myelinated fibers conduct in the range of 35–75 m/s.

nerve membrane must be depolarized. For unmyelinated fibers, depolarization must occur over the entire length of the nerve (i.e., continuous conduction), which takes much more time than in myelinated fibers. In myelinated fibers, the axonal membrane only needs to depolarize at the nodes of Ranvier; the internodes do not depolarize, but rather the action potential jumps over them. As the internode is approximately 1 mm in length and the node of Ranvier is only 1–2 μm in length, markedly less axonal membrane needs to depolarize to propagate an action potential. The lower the total depolarization time, the faster the conduction velocity. In myelinated axons, the density of sodium channels is highest in nodal areas, the areas undergoing depolarization. Myelinated human peripheral nerve fibers typically conduct in the range of 35–75 m/s, far faster than could ever be achieved by increasing the diameter of unmyelinated fibers. Not all human peripheral nerve fibers are myelinated. Unmyelinated fibers, which conduct very slowly (typically 0.2–1.5 m/s), primarily mediate pain, temperature, and autonomic functions. Schwann cells also support these unmyelinated fibers; however, one Schwann cell typically surrounds several unmyelinated fibers, but without the formation of concentric spirals of myelin. When an individual axon is depolarized, an action potential propagates down the nerve. Distally, the axon divides

SECTION I  Overview of Nerve Conduction Studies and Electromyography

into many twigs, each of which goes to an individual muscle fiber. An axon, along with its anterior horn cell and all muscle fibers with which it is connected, is known as a motor unit (Fig. 2.16). Depolarization of all the muscle fibers in a motor unit creates an electrical potential known as the motor unit action potential (MUAP). Analysis of MUAPs is an important part of every needle EMG examination. When an action potential is generated, all muscle fibers in the motor unit are normally activated, again an all-­or-­none response. However, before a muscle fiber can be activated, the nerve action potential must be carried across the NMJ. The $

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Fig. 2.15  Demonstration of saltatory conduction.  Recording of a normal single fiber from an intact ventral root in a rat. (A) Successive records of external longitudinal current recorded from a single fiber as electrodes were moved along a ventral root in steps of 0–2 mm. (B) Lines from each record indicate positions of electrodes with respect to underlying nodes and internodes. (C) Latency to peak of external longitudinal current as a function of distance. Note how the distance/latency graph is a “staircase” configuration. As current proceeds down a normal myelinated axon, the latency (i.e., the conduction time) abruptly increases approximately every 1.0–1.5 mm. This is the depolarization time at the nodes of Ranvier. Conversely, note the flat part of the staircase graph; here the latency stays almost exactly the same despite a change in distance. This is the saltatory conduction jumping from node to node. (From Rasminsky M, Sears TA. Internodal conduction in undissected demyelinated nerve fibres. J Physiol. 1972;227:323–350, with permission.)

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Fig. 2.16  Motor unit.  The motor unit is defined as one axon, its anterior horn cell, and all connected muscle fibers and neuromuscular junctions. A nerve fiber action potential normally always results in depolarization of all the muscle fibers of the motor unit, creating an electrical potential known as the motor unit action potential (MUAP). Analysis of MUAPs is a large part of the needle electromyographic examination.

Chapter 2 • Anatomy and Neurophysiology for Electrodiagnostic Studies 19

sodium and depolarization of the muscle fiber. As is the case with nerve, once threshold is reached, a muscle fiber action potential is created that spreads throughout the muscle fiber. Following the muscle fiber action potential, a complex set of molecular interactions occurs within the muscle fiber, resulting in increasing overlap of the major muscle fiber filaments: actin and myosin, with the final result of muscle shortening, contraction, and generation of force (Fig. 2.18). 

CLASSIFICATION Multiple peripheral nerve classification schemes exist (Table 2.1). Peripheral nerves can be classified based on

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the following attributes: (1) myelinated or unmyelinated, (2) somatic or autonomic, (3) motor or sensory, and (4) diameter. There are several important points to glean from Table 2.1, some of which are directly relevant to clinical EDX testing. First is the direct relationship between fiber diameter and conduction velocity: the larger the diameter, the faster the conduction velocity. The large myelinated fibers are the fibers that are measured in clinical NCSs. Indeed, all routine motor and sensory conduction velocity and latency measurements are from the largest and fastest fibers of the particular peripheral nerve that is being studied. Large-­diameter fibers have the most myelin and the least electrical resistance, both of which result in faster conduction velocities. The small myelinated (Aδ, B) and unmyelinated (C) fibers carry autonomic information (afferent and efferent) and somatic pain and temperature sensations. These fibers are not recorded with standard nerve conduction techniques. Thus, neuropathies that preferentially affect only small fibers may not reveal any abnormalities on NCSs. Second, routine sensory conduction studies typically record cutaneous nerves innervating skin. The largest and fastest cutaneous fibers are the Aβ fibers from hair and skin follicles. Note that the size and conduction velocities of these fibers are similar to those of the muscle efferent fibers from the anterior horn cells that are recorded during routine motor studies. These myelinated fibers have velocities in the range of 35–75 m/s. Third, the largest and fastest fibers in the peripheral nervous system are not recorded during either routine motor or sensory NCSs. These are the muscle afferents, the Aα fibers (also known as Ia fibers), which originate from muscle spindles and mediate the afferent arc of the muscle stretch reflex. These fibers are recorded only during mixed nerve studies in which the entire mixed nerve is stimulated and recorded. Therefore mixed nerve conduction velocities usually are faster than either routine motor or cutaneous sensory conduction velocities because they contain these Ia fibers. Because the Ia fibers have the largest diameter and accordingly the

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20

SECTION I  Overview of Nerve Conduction Studies and Electromyography

Table 2.1  Peripheral Nerve Classification Schemes. Fiber Type(s)

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greatest amount of myelin, they often are affected early by demyelinating lesions such as those found in entrapment neuropathies. For example, in the EDX evaluation of carpal tunnel syndrome, the mixed nerve study from the palm to the wrist often is more sensitive in detecting abnormalities than either the routine motor or sensory conduction study. 

RECORDING All potentials obtained during NCSs and needle EMG result from the extracellular recording of intracellular events from either nerve or muscle. NCSs usually are performed by recording with surface electrodes over the skin, and EMG potentials by recording with a needle electrode placed within the muscle. In both procedures, intracellular electrical potentials are transmitted through tissue to the recording electrodes. The process of an intracellular electrical potential being transmitted through extracellular fluid and tissue is known as volume conduction. Although the theory of volume conduction is complex and beyond the scope of this text, volume-­conducted potentials can be modeled as either near-­field or far-­field potentials. Near-­ field potentials can be recorded only close to their source, and the characteristics of the potential depend on the distance between the recording electrodes and the electrical

source (i.e., the action potential). With near-­field potentials, a response generally is not seen until the source is close to the recording electrodes. The closer the recording electrodes are to the current source, the higher the amplitude. Compound muscle action potentials, sensory nerve action potentials, and MUAPs recorded during routine motor conduction, sensory conduction, and needle EMG studies, respectively, are essentially all volume-­conducted near-­field potentials. Volume-­ conducted, near-­ field potentials produce a characteristic triphasic waveform as an advancing action potential approaches and then passes beneath and away from a recording electrode (Fig. 2.19, top). In practice, most sensory and mixed nerve studies display this triphasic waveform morphology, as do fibrillation potentials and most MUAPs. The electrical correlate of an action potential traveling toward, under, and then away from the recording electrode is an initial positive phase, followed by a negative phase, and then a trailing positive phase, respectively. The first positive peak represents the time that the action potential is first beneath the active electrode; this is the point at which the onset latency should be measured for nerve action potentials. The initial positive peak may be very small or absent with some sensory responses. In that case, the initial negative deflection best marks the true onset of the potential.

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Fig. 2.19  Volume conduction and waveform morphology.  Top, An advancing action potential recorded by volume conduction will result in a triphasic potential that initially is positive, then is negative, and finally is positive again. Bottom, If the depolarization occurs directly beneath the recording electrode, the initial positive phase will be absent, and a biphasic, initially negative potential will be seen. Note that, by convention, negative is up and positive is down in all nerve conduction and electromyographic traces.

If a volume-­ conducted, near-­ field action potential begins directly under the recording electrode, the initial deflection will be negative (Fig. 2.19, bottom). During routine motor NCSs, this is the expected compound muscle action–potential morphology if the active electrode is correctly placed over the motor point (i.e., endplate) of the muscle. There is no advancing action potential, as muscle fiber depolarization begins at the endplate; hence, the waveform has no initial positive deflection. This results in a characteristic biphasic potential with an initial negative deflection (Fig. 2.20, top). If the electrode is inadvertently placed off the motor point, a triphasic potential with an initial positive deflection will be seen (Fig. 2.20 middle). If the depolarization occurs at a distance but never passes under the recording electrode, characteristically only a positive deflection will occur (Fig. 2.20, bottom). For example, this pattern is seen when stimulating the median nerve and recording a hypothenar muscle, as might be done during routine motor studies looking for an anomalous innervation. The muscle action potential of the median-­innervated thenar muscles occurs at a distance but never travels under the recording electrodes located over the hypothenar muscles. The result is a small positive deflection, volume-­conducted potential. The other type of volume-­ conducted potential is the far-­field potential. Far-­ field potentials are electrical potentials that are distributed widely and instantly. Two recording electrodes, one closer and the other farther from the source, essentially see the source at the same time. Although far-­field potentials are more often of concern in evoked-­potential studies, they occasionally are important in NCSs. The stimulus artifact seen at the

Fig. 2.20  Volume conduction and motor potentials.  With the active recording electrode (G1) over the motor point, depolarization first occurs at that site, with the depolarization subsequently spreading away. The corresponding waveform has an initial negative deflection without any initial positivity (top trace). If the active recording electrode is off the motor point, depolarization begins distally and then travels under and past the active electrode, resulting in an initial positive deflection (middle trace). If the depolarization occurs at a distance and never travels under the recording electrode, only a small positive potential will be seen (bottom trace). Note that, by convention, negative is up and positive is down in all nerve conduction and electromyographic traces.

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Fig. 2.21  Near-­field and far-­field potentials. Median motor study, recording the abductor pollicis brevis muscle, stimulating at the wrist (top trace) and antecubital fossa (bottom trace). At each site, a compound muscle action potential is present, representing a near-­ field recording of the underlying muscle fiber action potentials. The compound muscle action potential latencies occur at different times, reflecting their different arrival times at the recording electrode. At the start of each trace is the stimulus artifact (blue arrow). The stimulus artifact is an example of a far-­field potential being transmitted instantaneously and seen at the same time, despite the difference in distances between the two stimulation sites.

onset of all NCSs is a good example of a far-­field potential (Fig. 2.21). The shock artifact is instantly transmitted and is seen at the same time at distal and proximal recording sites. Those potentials whose latencies do not vary with distance from the stimulation site usually are all far-­field potentials.

22

SECTION I  Overview of Nerve Conduction Studies and Electromyography

Suggested Readings Brown WF. The Physiological and Technical Basis of Electromyography. Boston: Butterworth-­Heinemann; 1984. Dumitru D, Delisa JA. AAEM Minimonograph #10: Volume Conduction. Rochester, MN: American Association of Electrodiagnostic Medicine; 1991. Haymaker W, Woodhall B. Peripheral Nerve Injuries. Philadelphia: WB Saunders; 1953.

Hollinshead WH. Anatomy for Surgeons, Volume 2: The Back and Limbs. New York: Harper & Row; 1969. Mayo Clinic and Mayo Foundation. Clinical Examinations in Neurology. Philadelphia: WB Saunders; 1956. O’Brien MD. Aids to the Examination of the Peripheral Nervous System. London: Baillière Tindall; 1986. Rasminsky M, Sears TA. Internodal conduction in undissected demyelinated nerve fibres. J Physiol. 1972;227:323–350.

SECTION II • Fundamentals of Nerve Conduction Studies

Basic Nerve Conduction Studies

After the history is taken and a directed physical examination is performed, every study begins with nerve conduction studies (NCSs). The needle electromyography (EMG) examination is performed after the NCSs are completed because the findings on the NCSs are used in the planning and interpretation of the needle EMG examination that follows. Peripheral nerves usually can be easily stimulated and brought to action potential with a brief electrical pulse applied to the overlying skin. Techniques have been described for studying most peripheral nerves. In the upper extremity, the median, ulnar, and radial nerves are the most easily studied; in the lower extremity, the peroneal, tibial, and sural nerves are the most easily studied (see Chapters 10 and 11). Of course, the nerves selected for study depend on the patient’s symptoms and signs and the differential diagnosis. Motor, sensory, or mixed nerve studies can be performed by stimulating the nerve and placing the recording electrodes over a distal muscle, a cutaneous sensory nerve, or the entire mixed nerve, respectively. The findings from motor, sensory, and mixed nerve studies often complement one another and yield different types of information based on distinct patterns of abnormalities, depending on the underlying pathology.

MOTOR CONDUCTION STUDIES Motor conduction studies are technically less demanding than sensory and mixed nerve studies; thus, they usually are performed first. Performing the motor studies first also has other major advantages. It is not uncommon for the sensory responses to be very low in amplitude or absent in many neuropathies. Performing the motor studies first allows one to know where the nerve runs, where it should be stimulated, and how much current is needed and also gives some information about whether the nerve is normal or abnormal. On the other hand, if the sensory study is done before the motor study, one might spend a lot of unnecessary time stimulating and trying to record a sensory response that is not present. For example, imagine a patient with a moderately severe median neuropathy at the wrist who is sent for an electrodiagnostic (EDX) evaluation. If the median motor study is performed first, the correct stimulation site can be confirmed, the amount of current needed to stimulate the median nerve will be known, and one will also know that the

3

median nerve is abnormal before doing the median sensory study. Then, when performing the median sensory study, one is confident of where to stimulate the nerve and how much current is needed. In this case, if no sensory response is present, one can have a high degree of certainty that the response is truly absent and move along to the next nerve to be studied. However, if the sensory conduction study is done first and is absent, it will not be as obvious if the absent response is due to a technical problem or is truly absent. One can waste a lot of time unnecessarily trying to figure this out. Do the motor conduction study first; your study will be more efficient, and the patient will tolerate the study much better. Motor responses typically are in the range of several millivolts (mV), as opposed to sensory and mixed nerve responses, which are in the microvolt (μV) range. Thus, motor responses are less affected by electrical noise and other technical factors. For motor conduction studies, the gain usually is set at 2–5 mV per division. Recording electrodes are placed over the muscle of interest. In general, the belly-­tendon montage is used. The active recording electrode (also known as G1) is placed on the center of the muscle belly (over the motor endplate), and the reference electrode (also known as G2) is placed distally, over the tendon to the muscle (Fig. 3.1). The designations G1 and G2 remain in the EMG vernacular, referring to a time when electrodes were attached to grids (hence the G) of an oscilloscope. The stimulator then is placed over the nerve that supplies the muscle, with the cathode placed closest to the recording electrode. It is helpful to remember “black to black,” indicating that the black electrode of the stimulator (the cathode) should be facing the black recording electrode (the active recording electrode). For motor studies, the duration of the electrical pulse usually is set to 200 ms. Most normal nerves require a current in the range of 20–50 mA to achieve supramaximal stimulation. As current is slowly increased from a baseline 0 mA, usually by 5–10 mA increments, more of the underlying nerve fibers are brought to action potential and, subsequently, more muscle fiber action potentials are generated. The recorded potential, known as the compound muscle action potential (CMAP), represents the summation of all underlying individual muscle fiber action potentials. When the current is increased to the point that the CMAP no longer increases in size, one presumes that all nerve fibers

23

24

SECTION II  Fundamentals of Nerve Conduction Studies

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have been excited and that supramaximal stimulation has been achieved. The current is then increased by another 20% to ensure supramaximal stimulation. The CMAP is a biphasic potential with an initial negativity, or upward deflection from the baseline, if the recording electrodes have been properly placed with G1 over the motor endplate. For each stimulation site, the latency, amplitude, duration, and area of the CMAP are measured (Fig. 3.2). A motor conduction velocity can only be calculated after two sites, one distal and one proximal, have been stimulated.

Latency Latency is the time from the stimulus to the initial CMAP deflection from baseline. Latency represents three separate processes: (1) the nerve conduction time from the stimulus site to the neuromuscular junction (NMJ), (2) the time delay across the NMJ, and (3) the depolarization time across the muscle. Latency measurements usually are made in milliseconds (ms) and reflect only the fastest conducting motor fibers. 

Amplitude CMAP amplitude is most commonly measured from baseline to the negative peak and less commonly from the first negative peak to the next positive peak. CMAP amplitude reflects the number of muscle fibers that depolarize. Although low CMAP amplitudes most often result from loss of axons (as in a typical axonal neuropathy), other causes of a low CMAP amplitude include conduction block from demyelination located between the stimulation site and the recorded muscle, as well as some NMJ disorders and myopathies. 

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Fig. 3.2  Compound muscle action potential (CMAP).  The CMAP represents the summation of all the underlying muscle fiber action potentials. With recording electrodes properly placed, the CMAP is a biphasic potential with an initial negative deflection. Latency is the time from the stimulus to the initial negative deflection from baseline. Amplitude is most commonly measured from baseline to negative peak. Duration is measured from the initial deflection from baseline to the first baseline crossing (i.e., negative peak duration). In addition, negative CMAP area (i.e., the area above the baseline) is calculated by most modern computerized electromyographic machines. Latency reflects only the fastest conducting motor fibers. All fibers contribute to amplitude and area. Duration is primarily a measure of synchrony.

Area CMAP area also is conventionally measured as the area above the baseline to the negative peak. Although the area cannot be determined manually, the calculation is readily performed by most modern computerized EMG machines. A negative peak CMAP area is another measure reflecting the number of muscle fibers that depolarize. Differences in CMAP area between the distal and proximal stimulation sites take on special significance in the determination of conduction block from a demyelinating lesion (see the “Conduction Block” section). 

Duration CMAP duration usually is measured from the initial deflection from baseline to the first baseline crossing (i.e., negative peak duration), but it also can be measured from the initial to the terminal deflection back to baseline. The former is preferred as a measure of CMAP duration because when CMAP duration is measured from the initial to terminal deflection back to baseline, the terminal CMAP returns to baseline very slowly and can be difficult to mark precisely. Duration is primarily a measure of synchrony (i.e., the extent to which each of the individual muscle fibers fire at the same time). Duration characteristically increases in conditions that result in slowing of some motor fibers but not others (e.g., in a demyelinating lesion). 

Chapter 3 • Basic Nerve Conduction Studies 25

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Fig. 3.3  Motor conduction velocity (CV) calculation.  Top, Median motor study, recording abductor pollicis brevis, stimulating wrist and elbow. The only difference between distal and proximal stimulations is the latency, with PL being longer than DL. Bottom, DL represents three separate times: the nerve conduction time from the distal stimulation site to the neuromuscular junction (NMJ) (A), the NMJ transmission time (B), and the muscle depolarization time (C). Accordingly, DL cannot be used alone to calculate a motor CV. Two stimulations are necessary. PL includes the nerve conduction time from the distal stimulation site to the NMJ (A), the NMJ transmission time (B), and the muscle depolarization time (C), as well as the nerve conduction time between the proximal and distal stimulation sites (D). If DL (A + B + C) is subtracted from PL (A + B + C + D), only the nerve conduction time between the distal and proximal stimulation sites (D) remains. The distance between those two sites can be measured, and a CV can be calculated (distance/time). CV reflects only the fastest conducting fibers in the nerve being studied. DL, Distal motor latency; PL, proximal motor latency.

Conduction Velocity Motor conduction velocity is a measure of the speed of the fastest conducting motor axons in the nerve being studied, which is calculated by dividing the distance traveled by the nerve conduction time. However, motor conduction velocity cannot be calculated by performing a single stimulation. The distal motor latency is more than simply a conduction time along the motor axon; it includes not only (A) the conduction time along the distal motor axon to the NMJ, but also (B) the NMJ transmission time and (C) the muscle depolarization time. Therefore, to calculate a true motor conduction velocity without including NMJ transmission and muscle depolarization times, two stimulation sites must be used, one distal and one proximal. When the nerve is stimulated proximally, the resulting CMAP area, amplitude, and duration are, in general, similar to those of the distal stimulation waveform. The only major difference between CMAPs produced by proximal and distal stimulations is the latency. The proximal latency is longer than the distal latency, reflecting the longer time and distance needed for the action potential to travel. The proximal motor latency reflects four separate times, as opposed to the three components reflected

in the distal motor latency measurement. In addition to (A) the nerve conduction time between the distal site and the NMJ, (B) the NMJ transmission time, and (C) the muscle depolarization time, the proximal motor latency also includes (D) the nerve conduction time between the proximal and distal stimulation sites (Fig. 3.3). Therefore, if the distal motor latency (containing components A + B + C) is subtracted from the proximal motor latency (containing components A + B + C + D), the first three components will cancel out. This leaves only component D, the nerve conduction time between the proximal and distal stimulation sites, without the distal nerve conduction, NMJ transmission, and muscle depolarization times. The distance between these two sites can be approximated by measuring the surface distance with a tape measure. A conduction velocity then can be calculated along this segment: (distance between the proximal and distal stimulation sites) divided by (proximal latency minus distal latency). Conduction velocities usually are measured in meters per second (m/s). It is essential to note that both latency and conduction velocity reflect only the fastest conducting fibers in the nerve being studied. By definition, conduction along these fibers arrives first and thus it is these fibers that are the

26

SECTION II  Fundamentals of Nerve Conduction Studies

ones measured. The many other normal slower conducting fibers participate in the CMAP area and amplitude but are not reflected in either the latency or conduction velocity measurements. 

SENSORY CONDUCTION STUDIES In contrast to motor conduction studies, in which the CMAP reflects conduction along the motor nerve, NMJ, and muscle fibers, in sensory conduction studies, only nerve fibers are assessed. Because most sensory responses are very small (usually in the range of 1–50 μV), technical factors and electrical noise assume more importance. For sensory conduction studies, the gain usually is set at 10–20 μV per division. A pair of recording electrodes (G1 and G2) are placed in line over the nerve being studied, at an interelectrode distance of 2.5–4 cm, with the active electrode (G1) placed closest to the stimulator. Recording ring electrodes are conventionally used to test the sensory nerves in the fingers (Fig. 3.4). For sensory studies, an electrical pulse of either 100 or 200 ms in duration is used, and most normal sensory nerves require a current in the range of 5–30 mA to achieve supramaximal stimulation. This is less current than what is usually required for motor conduction studies. Thus, sensory fibers usually have a lower threshold to stimulation than do motor fibers. This can easily be demonstrated on yourself; when slowly increasing the stimulus intensity, you will feel the paresthesias (sensory) before you feel or see the muscle starts to twitch (motor). As in motor studies, the current is slowly increased from a baseline of 0 mA, usually in 3–5-­mA increments, until the recorded sensory potential is maximized. This potential, the sensory nerve action potential (SNAP), is a compound potential that represents the summation of all the individual sensory fiber action potentials. SNAPs usually are biphasic or triphasic potentials. For each stimulation site, the onset

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3HDNODWHQF\ 2QVHWODWHQF\ Fig. 3.5  Sensory nerve action potential (SNAP).  The SNAP represents the summation of all the underlying sensory fiber action potentials. The SNAP usually is biphasic or triphasic in configuration. Onset latency is measured from the stimulus to the initial negative deflection for biphasic SNAPs (as in the waveform here) or to the initial positive peak for triphasic SNAPs. Onset latency represents nerve conduction time from the stimulus site to the recording electrodes for the largest cutaneous sensory fibers in the nerve being studied. Peak latency is measured at the midpoint of the first negative peak. Amplitude most commonly is measured from baseline to negative peak. Duration is measured from the initial deflection from baseline to the first baseline crossing (i.e., negative peak duration). Only one stimulation site is required to calculate a sensory conduction velocity, as sensory onset latency represents only nerve conduction time.

latency, peak latency, duration, and amplitude are measured (Fig. 3.5). Unlike motor studies, a sensory conduction velocity can be calculated with one stimulation site alone, by taking the measured distance between the stimulator and active recording electrode and dividing by the onset latency. No NMJ or muscle time needs to be subtracted out by using two stimulation sites.

Onset Latency The onset latency is the time from the stimulus to the initial negative deflection from baseline for biphasic SNAPs or to the initial positive peak for triphasic SNAPs. Sensory onset latency represents nerve conduction time from the stimulus site to the recording electrodes for the largest cutaneous sensory fibers in the nerve being studied. 

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Ground Fig. 3.4  Sensory conduction study setup.  Median sensory study, antidromic technique. Ring electrodes are placed over the index finger, 3–4 cm apart. The active recording electrode (G1) is placed more proximally, closest to the stimulator. Although the entire median nerve is stimulated at the wrist, only the cutaneous sensory fibers are recorded over the finger.

The peak latency is the time from the stimulus to the midpoint of the first negative peak. When sensory NCSs were first developed, peak latencies were classically used instead of onset latencies. In the past, peak latencies offered several advantages, some of which are still as valid today as when they were first developed. The peak latency can be ascertained in a straightforward manner; there is practically no interindividual variation in its determination. In contrast, the onset latency can be obscured by noise or by the stimulus artifact, making it difficult to determine precisely. In addition, for some potentials, especially small ones, it may be difficult to determine the precise point of deflection from the baseline (Fig. 3.6). These problems do not occur in marking

Chapter 3 • Basic Nerve Conduction Studies 27

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Fig. 3.6  Sensory nerve action potential onset and peak latencies.  Onset and peak latency measurements each have their own advantages and disadvantages. Onset latency represents the fastest conducting fibers and can be used to calculate a conduction velocity. However, for many potentials, especially small ones, it is difficult to precisely place the latency marker on the initial deflection from baseline (blue arrows: possible onset latencies). Marking the peak latency is straightforward, with nearly no interexaminer variation. However, the population of fibers represented by peak latency is unknown; it cannot be used to calculate a conduction velocity.

the peak latency. Normal values exist for peak latencies for the most commonly performed sensory studies. However, peak latencies have two distinct disadvantages. Most important, the peak latency cannot be used to calculate a conduction velocity. The population of sensory fibers represented by the peak latency is not known, in contrast to the onset latency, which represents the fastest conducting fibers in the nerve being studied. Second, normal values for peak latencies are dependent on using standard distances. This can be problematic especially in the upper extremities in patients with particularly large or small hands. Both onset and peak latencies can be used in the analysis of sensory NCSs. In the examples given in this text in the later clinical chapters, both values are measured and reported. If the potential has an abrupt, consistent, and easily marked onset latency, the onset latency is the preferred measurement. However, in cases where the onset latency is obscured, or not precise, peak latency is better used. 

Amplitude The SNAP amplitude is most commonly measured from baseline to negative peak, but it can also be measured from the first negative peak to the next positive peak. The SNAP amplitude reflects the sum of all the individual sensory fibers that depolarize. Low SNAP amplitudes indicate a definite disorder of peripheral nerve. 

Duration Like the CMAP duration, SNAP duration is usually measured from the onset of the potential to the first baseline crossing (i.e., negative peak duration), but it also can be measured from the initial to the terminal deflection back to

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Fig. 3.7  Compound muscle action potential (CMAP) and sensory nerve action potential (SNAP) comparison. CMAPs (top) and SNAPs (bottom) are both compound potentials but are quite different in terms of size and duration. CMAP amplitude usually is measured in millivolts, whereas SNAPs are small potentials measured in the microvolt range (note different gains between the traces). CMAP negative peak duration usually is 5–6 ms, whereas SNAP negative peak duration is much shorter, typically 1–2 ms. When both sensory and motor fibers are stimulated (such as when performing antidromic sensory or mixed studies), these differences (especially duration) usually allow an unknown potential to be recognized as either a nerve or muscle potential.

baseline. The former is preferred given that the SNAP duration measured from the initial to terminal deflection back to baseline is difficult to mark precisely because the terminal SNAP returns to baseline very slowly. The SNAP duration typically is much shorter than the CMAP duration (typically 1.5 vs. 5–6 ms, respectively). Thus, duration is often a useful parameter to help identify a potential as a true nerve potential rather than a muscle potential (Fig. 3.7). 

Conduction Velocity Unlike the calculation of a motor conduction velocity, which requires two stimulation sites, sensory conduction velocity can be determined with one stimulation, simply by dividing the distance traveled by the onset latency. Essentially, distal conduction velocity and onset latency are the same measurement; they differ only by a multiplication factor (i.e., the distance). Sensory conduction velocity represents the

28

SECTION II  Fundamentals of Nerve Conduction Studies

speed of the fastest, myelinated cutaneous sensory fibers in the nerve being studied. Sensory conduction velocity along proximal segments of nerve can be determined by performing proximal stimulation and calculating the conduction velocity between proximal and distal sites, in a manner similar to the calculation for motor conduction velocity: (distance between the proximal and distal stimulation sites) divided by (proximal latency minus distal latency). However, proximal sensory studies result in smaller amplitude potentials and often are more difficult to perform, even in normal subjects, because of the normal processes of phase cancellation and temporal dispersion (see later). Note that one can also determine the sensory conduction velocity from the proximal site to the recording electrode by simply dividing the total distance traveled by the proximal onset latency. 

Special Considerations in Sensory Conduction Studies: Antidromic Versus Orthodromic Recording When a nerve is depolarized, conduction occurs equally well in both directions away from the stimulation site. Consequently, sensory conduction studies may be performed using either antidromic (stimulating toward the sensory receptor) or orthodromic (stimulating away from the

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Fig. 3.8  Antidromic and orthodromic sensory studies. Median sensory nerve action potential (SNAPs). Top trace, Antidromic study, stimulating wrist, recording index finger. Bottom trace, Orthodromic study, stimulating index finger, recording wrist. Latencies and conduction velocities are identical for both. The antidromic method has the advantage of a higher-­amplitude SNAP but is followed by a large volume-­conducted motor potential. If the SNAP is absent in an antidromic study, care must be taken not to confuse the volume-­conducted motor potential as the sensory potential. Note the difference in duration between SNAP and compound muscle action potential, which helps discriminate between the SNAP and the volume-­conducted motor potential that follows.

sensory receptor) techniques. For instance, when studying median sensory fibers to the index finger, one can stimulate the median nerve at the wrist and record the potential with ring electrodes over the index finger (antidromic study). Conversely, the same ring electrodes can be used for stimulation, and the potential recorded over the median nerve at the wrist (orthodromic study). Latencies and conduction velocities should be identical with either method (Fig. 3.8), although the amplitude generally is higher in antidromically conducted potentials. In general, the antidromic technique is superior for several reasons, but each method has its advantages and disadvantages. Most important, the amplitude is higher with antidromic than with orthodromic recordings, which makes it easier to identify the potential. The SNAP amplitude is directly proportional to the proximity of the recording electrode to the underlying nerve. For most antidromically conducted potentials, the recording electrodes are closer to the nerve. For example, in the antidromically conducted median sensory response, the recording ring electrodes are placed on the finger, very close to the underlying digital nerves just beneath the skin from which the potential is recorded. When the montage is reversed for orthodromic recording, there is more tissue (e.g., the transverse carpal ligament and other connective tissues) at the wrist separating the nerve from the recording electrodes. This results in attenuation of the recorded sensory response, resulting in a much lower amplitude. The higher SNAP amplitude obtained with antidromic recordings is the major advantage of using this method. The antidromic technique is especially helpful when recording very small potentials, which often occur in pathologic conditions. Furthermore, because the antidromic potential generally is larger than the orthodromic potential, it is less subject to noise or other artifacts. However, the antidromic method has some disadvantages (Fig. 3.9). Because the entire nerve is often stimulated, including the motor fibers, this frequently results in the SNAP being followed by a volume-­ conducted motor potential. It usually is not difficult to differentiate between the two because the SNAP latency typically occurs earlier than the volume-­ conducted motor potential. However, problems occur if the two potentials have a similar latency or, more importantly, if the sensory potential is absent. When the latter occurs, one can mistake the first component of the volume conducted motor potential for the SNAP, where none truly exists. It is in this situation that measuring the duration of the potential can be helpful in distinguishing a sensory from a motor potential. If one is still not sure, performing an orthodromic study will settle the issue, as no volume conducted motor response will occur with an orthodromic study. In this case, the antidromic and orthodromic potentials should have the same onset latency. 

Lesions Proximal to the Dorsal Root ­Ganglion Result in Normal Sensory Nerve Action Potentials Peripheral sensory fibers are all derived from the dorsal root ganglia cells, the primary sensory neurons. These

Chapter 3 • Basic Nerve Conduction Studies 29

20 µV 2 ms Fig. 3.9  Misinterpretation error with antidromic sensory studies.  In an antidromic study, the entire nerve is stimulated, including both sensory and motor fibers, which frequently results in the sensory nerve action potential (SNAP) being followed by a volume-­ conducted motor potential. Top, Normal antidromic ulnar sensory response, stimulating the wrist and recording the fifth digit. Notice the ulnar SNAP, which is followed by the large, volume-­conducted motor response. One can recognize the SNAP by its characteristic shape and especially by its brief negative peak duration of approximately 1.5 ms. Also, notice that the SNAP usually occurs earlier than the volume-­conducted motor response. Bottom, If the sensory response is absent and an antidromic study is performed, one might mistake the first component of the volume-­conducted motor response for the SNAP. The key to not making this mistake is to note the longer duration of the motor potential, which often has a higher amplitude and slowed latency/conduction velocity. In this case, the negative peak duration of this mistaken potential is approximately 2.5 ms. In some cases, one still may not be certain. In those situations, performing the study orthodromically will settle the issue as no volume-­conducted motor potential will occur with an orthodromic study. The onset latencies of the orthodromic and antidromic potentials should be the same. The problem with an orthodromic study is that the amplitude is often much lower than with the antidromic method. (Note: Sensory responses are normally very low, in the microvolt range.)

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Fig. 3.10  Nerve root lesions and nerve conduction studies.  Anatomic differences between sensory and motor nerve fibers result in different patterns of nerve conduction abnormalities in nerve root lesions. The sensory nerve (top) is derived from the dorsal root ganglia (DRG). DRGs are bipolar cells whose central processes form the sensory roots and distal processes continue as the peripheral sensory nerve fibers. The motor nerve (bottom) is derived from the anterior horn cell (AHC), which resides in the ventral gray matter of the spinal cord. Lesions of the nerve roots separate the peripheral motor nerve from its neuron, the AHC, but leave the DRG and its distal processes intact. Thus, nerve root lesions may result in degeneration of the motor fibers distally and, accordingly, abnormalities on motor nerve conduction studies and/or needle electromyogram. However, the distal sensory nerve remains intact in lesions of the nerve roots, as the lesion is proximal to the DRG. Thus, results of sensory conduction studies remain normal.

cells have a unique anatomic arrangement: they are bipolar cells located outside the spinal cord, near the intervertebral foramina. Their central processes form the sensory nerve roots, whereas their peripheral projections ultimately become peripheral sensory nerves. Any lesion of the nerve root, even if severe, leaves the dorsal root ganglion and its peripheral axon intact, although essentially disconnected from its central projection. Accordingly, SNAPs remain normal in lesions proximal to the dorsal root ganglia, including lesions of the nerve roots, spinal cord, and brain

(Fig. 3.10). It is not uncommon, in the EMG lab, for a patient to have sensory symptoms or sensory loss but to have normal SNAPs in that distribution. This combination of clinical and electrical findings should always suggest the possibility of a lesion proximal to the dorsal root ganglia, although rarely, other conditions can produce the same situation. The situation is quite different for motor fibers. The primary motor neurons, the anterior horn cells, are located in the ventral gray matter of the spinal cord. Axons from the motor neurons form the motor roots and, ultimately,

SECTION II  Fundamentals of Nerve Conduction Studies

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MEDIAN VERSUS ULNAR-­ LUMBRICAL-­INTEROSSEI MOTOR STUDIES (FIG. 10.9) Recording Site: Second lumbrical (2L: median innervated) and first palmar interosseous (INT: ulnar innervated); same recording electrodes for both: G1 placed slightly lateral to the midpoint of the third metacarpal G2 placed distally over the proximal interphalangeal joint of digit 2  Stimulation Sites: Median nerve at the wrist: Slightly lateral to the mid-­wrist between the tendons to the flexor carpi radialis and palmaris longus Ulnar nerve at the wrist: Medial wrist, adjacent to the flexor carpi ulnaris tendon  Distal Distance: 8–10 cm (the same distance must be used for both the median and ulnar studies)  Key Points: • Using the same recording electrodes, the second lumbrical is recorded when the median nerve is stimulated at the wrist, whereas the first palmar interosseous is recorded when the ulnar nerve is stimulated at the wrist.

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• I n normal subjects, the difference between the two distal latencies is 1.6 for sensory and >1.2 for motor amplitudes denotes some conduction block.

time is computed over the area of pathology. Only a short length of normal nerve is included that potentially could dilute any slowing present across the carpal tunnel. The technique is performed by stimulating the median nerve in the palm, recording the median nerve at the wrist, and comparing it with the ulnar nerve stimulated in the palm and recorded over the ulnar nerve at the wrist (Fig. 20.8). Each nerve is stimulated supramaximally in the palm at a distance of 8 cm from its respective recording electrodes. The median nerve is stimulated in the palm on a line connecting the median nerve in the middle of the wrist to the web space between the index and middle fingers. The ulnar nerve is stimulated in the palm on a line connecting the ulnar nerve at the medial wrist (lateral to the flexor carpi ulnaris tendon) to the web space between the ring and little fingers. Supramaximal responses are obtained for each

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SECTION VIII   Clinical Disorders 20 µV/D

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nerve, and the difference between the onset or peak latencies is calculated.  Median-­Versus-­Ulnar Digit 4 Sensory Latencies The technique of comparing median-­ versus-­ ulnar digit 4 sensory latencies takes advantage of the fact that, in most individuals, the sensory innervation to the fourth digit (ring finger) is split, with the lateral half innervated by the median nerve and the medial half innervated by the ulnar nerve (Fig. 20.9). Thus, if identical distances are used, the latencies stimulating each nerve can be directly compared. The antidromic technique is performed by stimulating the median and ulnar nerves at the wrist, one at a time, with recording ring electrodes placed over digit 4 (G1 over the metacarpophalangeal joint and G2 over the distal interphalangeal joint). Identical distances must be used for both (range 11–13 cm). Supramaximal responses are obtained, and the difference between the median and ulnar onset or peak latencies is recorded. The study also can be done orthodromically, stimulating with the ring electrodes over digit 4 as just described and recording the median and ulnar nerves at the wrist at identical distances. We do not recommend the

latter method because, with orthodromic stimulation at digit 4, co-­stimulation of the median and ulnar nerves cannot be avoided, and spread of the potential from the adjacent nerve may contaminate the recorded SNAP at the wrist.  Median Second Lumbrical-­Versus-­Ulnar Interossei Distal Motor Latencies The technique of comparing the second lumbrical (2L)-­ versus-­interosseous distal motor latencies takes advantage of two facts: (1) motor fibers are easy to record and more resistant to compression than sensory fibers, and (2) the median 2L muscle lies just above the ulnar INT. In some cases of generalized polyneuropathy with superimposed CTS, the SNAPs and mixed nerve potentials may be absent. In severe cases, the routine median CMAP recording the APB may also be absent, whereas the motor fibers to the second lumbrical and ulnar INT are still recordable. CMAPs from both the median-­innervated 2L and the ulnar-­innervated INT can easily be recorded by placing an active electrode (G1) slightly lateral and distal to the midpoint of the third metacarpal, with the reference electrode over the proximal interphalangeal joint of the second digit,

Chapter 20 • Median Neuropathy at the Wrist 331

and stimulating the median and ulnar nerves at the wrist, respectively (Fig. 20.10). The motor point to the 2L is identified when the active recording electrode has been placed such that stimulation of the median nerve at the wrist elicits a waveform with the fastest rise time and an initial negative deflection. Because the 2L cannot be seen or palpated, moving the active electrode slightly may be necessary to ensure the electrode is optimally placed. In some individuals, if the sensitivity is increased, a small mixed nerve potential will be seen slightly before the onset of the 2L CMAP. This is a normal finding, especially in younger patients. If this small mixed nerve potential is present, the latency should be measured from the onset of the 2L CMAP, not from the onset of the mixed nerve potential. The ulnar nerve is then stimulated supramaximally at the wrist, at the same distance, leaving the recording electrodes in place. A CMAP from the underlying ulnar INT muscles will be easily elicited. The ulnar CMAP is generally larger than the median CMAP. Identical distances (range 8–10 cm) must be used to compare the difference between the distal latencies.

The normal values for the three median-­versus-­ulnar comparison studies are given in Table 20.3. In our laboratory, the palmar mixed nerve peak latency difference is the most sensitive study, followed closely by the digit 4 sensory and 2L-­INT motor studies. However, there is a very high degree of correlation among the results of the three studies. In one comparison study, two of the three studies yielded abnormal results in 97% of all patients with mild CTS. In a patient in whom only one of the median-­ versus-­ulnar comparison studies is abnormal, one should be hesitant to make a definite electrodiagnosis of CTS (see Chapter 9).  Wrist-­to-­Palm Versus Palm-­to-­Digit Sensory Conduction Velocity (Segmental Sensory Conduction Studies Across the Wrist) Another extremely sensitive internal comparison study includes the wrist-­to-­palm versus palm-­to-­digit sensory conduction velocity (segmental sensory conduction studies across the wrist). This test is more technically challenging than the

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Table 20.3  Median-­Ulnar Comparison Studies. Nerve

Palmar mixed

Median Ulnar

Median palm Ulnar palm

Median nerve at wrist Ulnar nerve at wrist

Digit 4 sensory

Median

Median nerve at wrist Ulnar nerve at wrist

Digit 4

11–13a

Digit 4

11–13

Median nerve at wrist Ulnar nerve at wrist

Lateral to the mid-­third metacarpal (over the second lumbrical and interossei) Lateral to the mid-third metacarpal (over the second lumbrical and interossei)

Ulnar Lumbrical-­interossei

Median Ulnar

aMust

Stimulate

Record

Distance (cm)

Study

use the identical distance for median and ulnar nerve stimulation.

8 8

8–10a 8–10

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≥0.5

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others listed previously but is extremely sensitive in detecting CTS. This technique compares the sensory conduction velocity along the median nerve at two segments of identical distance: the wrist-­to-­palm segment and the palm-­to-­digit segment. Digit 3 is the preferred finger to record from due to its longer length. The recording electrodes (G1, G2) are placed at the proximal and the distal interphalangeal joints, respectively. Placing G1 at the proximal interphalangeal instead of the metacarpal-­phalangeal joint allows more distance between it and the stimulator (and less stimulus artifact). The median nerve is then stimulated at the wrist at a fixed distance to G1. The median nerve is next stimulated at the palm, with the recording ring electrodes left in place, at half the wrist-­to-­digit distance (Fig. 20.11). If the EMG machine is set up to automatically compute the wrist-­to-­palm and palm-­to digit conduction velocities, any distance can be used. Otherwise, making the palm-­to-­digit distance half that of the wrist-­to-­digit distance (e.g., 7 cm and 14 cm) greatly simplifies the mathematical equation. In this situation, the wrist-­to-­palm conduction velocity is then computed by multiplying the palm-­to-­digit conduction velocity by the wrist-­ to-­ digit conduction velocity, and then dividing it by the quantity of the palm-­to-­digit conduction velocity times two, minus the wrist-­to-­digit conduction velocity (Fig. 20.12). In normal subjects, the wrist-­to-­palm segment (i.e., the segment across the carpal tunnel) is equal to or faster than the distal segment (palm-­to-­digit) because proximal nerve normally conducts faster than distal segments, secondary to larger nerve diameter and warmer temperatures. In CTS, there is a reversal of this normal pattern; the proximal segment (wrist-­to-­palm) conducts more slowly than the distal palm-­to-­digit segment. In general, any slowing of more than 10 m/s is considered abnormal.  Other Useful Studies Inching Across the Wrist and Palmar Stimulation Another technique useful in demonstrating CTS, first described by Kimura and later by others, involves segmental

Distance A = Distance B B C A

A = CV (wrist-palm) B = CV (palm-digit) C = CV (wrist-digit) BxC A= (2 x B) – C Normals: A ≥ B CTS: B – A ≥ 10 m/s

Fig. 20.12  Calculation of the wrist-­to-­palm velocity in segmental sensory studies.  There is no direct way to stimulate the median cutaneous sensory fibers at the wrist and record them at the palm. The wrist-­to-­palm conduction velocity (CV) can be calculated from knowledge of the wrist-­ to-­digit and palm-­to-­digit CVs, both of which can be directly measured. If the palm-­to-­digit distance is half the wrist-­to-­digit distance, the calculation is simplified. In normal nerves, one expects the proximal segments to conduct at the same velocity or faster than the distal segments, due to larger nerve diameters and warmer temperatures (see Chapter 8). In carpal tunnel syndrome (CTS), there is a reversal of this pattern: the wrist-­to-­palm CV (across the carpal tunnel) is slower than the palm-­to-­ digit CV. Any slowing ≥10 m/s is considered abnormal.

stimulation (“inching”) of the median nerve across the carpal tunnel (Fig. 20.13). One looks for an abrupt change in latency or increase in amplitude above normal control values, recording either a median CMAP at the APB or a median digital SNAP at the index or middle finger. Kimura’s method begins at 4 cm proximal to the distal wrist crease and continues to 6 cm distal to the wrist crease, with segmental stimulation at 1-­cm increments. For each 1-­cm increment, latency usually increases 0.2 to 0.3 ms. Any abrupt change in latency greater than this is highly suggestive of focal demyelination. Although the inching

Chapter 20 • Median Neuropathy at the Wrist 333

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technique has the advantage of showing the exact site of the lesion, its effectiveness often is limited by difficulty stimulating the nerve at the sites just distal to the wrist crease. The technique is particularly difficult to perform recording the median CMAP because stimulation of motor fibers at 1-­cm increments following the course of the recurrent thenar branch of the median nerve can be quite difficult. Furthermore, stimulation in the palm often requires rotation of the anode to prevent excessive stimulus artifact (Fig. 20.14). Rather than measuring a change in latency, comparing the CMAP or SNAP amplitudes stimulating at the wrist and palm can be technically easier and can yield additional information about the underlying pathophysiology (Fig. 20.15). Wrist and palmar stimulation can be performed for either median motor or sensory studies. Only single palm and wrist stimulations are required, whereas inching requires stimulation at multiple 1-­cm increments. Several technical factors must be taken into account. First, as noted earlier for motor studies, the anatomy of the recurrent thenar motor branch is such that for stimulating the motor branch in the palm, the stimulator often must be placed beyond the thenar eminence with the anode rotated distally to prevent excessive stimulus artifact (Fig. 20.14). Second, the examiner must be aware of normal values when comparing amplitudes proximal and distal to the carpal tunnel. There is always some drop in amplitude PV'

Fig. 20.15  Palmar and wrist stimulation comparison. The median nerve is stimulated at the wrist and palm while recording the abductor pollicis brevis muscle. Left, G1, Active recording electrode; G2, reference recording electrode; S1, stimulation at the wrist; S2, stimulation in the palm. Right, A significantly larger amplitude response stimulating in the palm compared to the wrist signifies conduction block (i.e., demyelination) across the wrist.

SECTION VIII   Clinical Disorders

334

Fig. 20.16  Change in compound muscle action potential (CMAP) and sensory nerve action potential (SNAP) amplitude across the carpal tunnel.  To assess possible conduction block across the carpal tunnel, either the median CMAP or SNAP can be recorded with stimulation of the wrist and palm. Note that in normal controls, there is only a slight increase in amplitude between wrist and palm stimulation sites. A large difference in amplitude between wrist and palm sites in patients with carpal tunnel syndrome (CTS) signifies conduction block. For motor studies, a normal palm to wrist amplitude ratio is ≤1.2 and for sensory studies it is ≤1.6. (Adapted with permission from Lesser EA, Venkatesh S, Preston DC, et al. Stimulation distal to the lesion in patients with carpal tunnel syndrome. Muscle Nerve. 1995;18:503.)

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Fig. 20.17  Distal conduction block mimicking axonal loss.  Low distal amplitudes usually are attributed to axonal loss. However, if conduction block is present distal to the typical distal stimulation site, it can mimic the pattern of axonal loss. Such is often the case in carpal tunnel syndrome (CTS) in which the lesion is distal to the usual distal stimulation site. Left, Median motor study, stimulating the wrist and antecubital fossa. Note that this appears to be a typical axonal loss pattern. Right, Median motor study, stimulating the palm and wrist. In this patient with CTS, a markedly higher-­ amplitude CMAP is evoked stimulating the palm, signifying conduction block. The identification of conduction block not only localizes the lesion but also denotes a much better prognosis than axonal loss. The clinical clue to the presence of conduction block in a patient with CTS is a weak thumb abduction and relatively intact muscle bulk (i.e., no atrophy) of the abductor pollicis brevis muscle, with a low median CMAP stimulating at the wrist.

proximally compared with distally due to greater temporal dispersion and phase cancellation with proximal stimulation. The effects of normal temporal dispersion and phase cancellation are always greater for sensory fibers than for motor fibers. In normal median nerves, the ratio of the distal to proximal CMAP amplitude does not exceed 1.2, whereas the ratio of distal to proximal SNAP amplitude does not exceed 1.6. Larger ratios suggest some element of conduction block (Fig. 20.16). This assumption presumes

that both stimulations are supramaximal, that there is no co-­stimulation of adjacent nerves, and that the baseline is not obscured by shock artifact or noise that precludes an accurate amplitude measurement. In CTS, if wrist stimulation yields a low CMAP or SNAP amplitude, there are two possible explanations: (1) there is conduction block secondary to demyelination across the carpal tunnel with the underlying axon intact, or (2) there has been secondary axonal loss (Fig. 20.17). Comparing the amplitudes

Chapter 20 • Median Neuropathy at the Wrist 335

obtained with wrist and palmar stimulation can easily sort out these two possibilities. Take the following example: Case A

Case B

CMAP (stimulate wrist, record APB)

2 mV

2 mV

CMAP (stimulate palm, record APB)

6 mV

2 mV

In both cases, when the median nerve is stimulated at the wrist, the recorded CMAP is low (normal value >4.0 mV). When the palm is stimulated in case A, however, the CMAP amplitude increases by an additional 200%; the distal-­to-­proximal amplitude ratio is 3.0, signifying conduction block. In contrast, there is no change in amplitude in case B, signifying that the low amplitude is secondary to axonal loss.  Median-­Versus-­Radial Digit 1 Sensory Latencies Comparison of the median-­ versus-­ radial digit 1 sensory latencies takes advantage of the fact that, in most individuals, digit 1 (the thumb) is innervated by both the median and radial nerves (Fig. 20.18). The basic concept is the same as in the median-­versus-­ulnar digit 4 sensory study: the median and radial nerves are stimulated at the wrist, using identical distances, with recording ring electrodes over digit 1 (G1 over the metacarpophalangeal joint and G2 over the interphalangeal joint). The radial nerve is stimulated at the wrist along the lateral border of the radial bone. Using the same distance, the median nerve is stimulated at the wrist in the usual location. Supramaximal responses are obtained at each stimulation site, and the onset or peak latencies are compared. Although this technique is popular in some laboratories, stimulating the nerves at identical distances may be difficult because the median nerve travels to the thumb at an angle, which can hinder measurement of its true distance. Any difference between the median and radial latencies greater than or equal to 0.5 ms is considered abnormal. 

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Fig. 20.19  Inverted F waves in carpal tunnel syndrome.  In normal subjects, the minimum F-­wave latency of the median nerve is approximately 1–2 ms shorter than that of the ulnar nerve. In carpal tunnel syndrome, the median F waves often are prolonged compared with the ulnar F waves, providing a useful measure to confirm median neuropathy.

Median-­Versus-­Ulnar Minimum F-­Wave Latencies This technique compares the minimum F-­wave latency stimulating the median and ulnar nerves at the wrist, recording the APB and abductor digiti minimi muscles, respectively. In normal individuals, the minimum F-­wave latency from the median nerve is approximately 1–2 ms shorter than the minimum F-­wave latency from the ulnar nerve. A reversal of this pattern is considered abnormal (Fig. 20.19). This test is nonspecific, however, because the F wave measures conduction along the entire length of nerve, from the recording electrode to the spinal cord. Although this study can confirm a problem with the median nerve, it cannot localize the lesion to the wrist. It is generally used only as confirmatory evidence for a diagnosis of CTS, in conjunction with abnormalities noted using more sensitive techniques. 

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Fig. 20.18  Median-­radial sensory comparison study.  In most individuals, the thumb is innervated by both the superficial radial and median sensory nerves. Using identical distances, the median and radial sensory latencies to the thumb can be compared in patients with suspected carpal tunnel syndrome, looking for preferential slowing of the median sensory fibers. Any difference between the median and radial latencies ≥0.5 ms is considered abnormal. G1, Active recording electrode; G2, reference recording electrode; S1, radial stimulation point; S2, median stimulation point.

Electromyographic Approach The recommended EMG approach to a patient with CTS is outlined in Box 20.3. The EMG strategy is designed with the clinical differential diagnosis in mind (i.e., proximal median neuropathy, brachial plexopathy, C6–C7 radiculopathy). The key muscle to check is the APB. In mild or early cases of CTS, the APB often is normal. In later or more severe cases, EMG may reveal secondary axonal loss resulting in denervation and reinnervation. In general, the hand muscles are best approached with a smaller-­gauge needle. Because examination of the APB often is painful for patients to tolerate, it is best to begin the study with a different C8– T1-­innervated muscle, such as the first dorsal interosseous

336

SECTION VIII   Clinical Disorders

Box 20.3  Recommended Electromyographic Protocol for Carpal Tunnel Syndrome

A

. Abductor pollicis brevis (APB) 1 2. At least two C6–C7-­innervated muscles (e.g., pronator teres, flexor carpi radialis, triceps brachii, extensor digitorum communis) to exclude a cervical radiculopathy If APB is abnormal, the following additional muscles should be sampled: 1. At least one proximal median-­innervated muscle (e.g., flexor carpi radialis, pronator teres, flexor pollicis longus) to exclude a proximal median neuropathy (note: the pronator teres may be spared in pronator syndrome) 2. At least two other non-median, lower trunk/C8–T1-­ innervated muscles (e.g., first dorsal interosseous, extensor indicis proprius) to exclude a lower trunk brachial plexopathy, polyneuropathy, or C8–T1 radiculopathy Note: If the carpal tunnel syndrome is superimposed on another condition (e.g., polyneuropathy, plexopathy, radiculopathy), a more detailed electromyographic examination will be required. The APB study frequently is painful and difficult for some patients to tolerate. It is best not studied first but also best not left for the end of the electromyographic study in case the patient is unable to tolerate the entire examination.

B

(FDI). The APB can be examined next. Although some electromyographers may prefer to study the APB toward the end of the examination, there is the potential problem that the patient may quit the study before this key muscle can be studied, especially if the patient is generally intolerant of the EMG examination. If the APB is abnormal, proximal median-innervated muscles and at least two other non-median C8–T1/lower trunk-­innervated muscles should be sampled. In addition, C6–C7-­innervated muscles should be sampled to exclude a cervical radiculopathy. The PT and FCR are very helpful muscles to sample because they can be used both as proximal median and C6–C7-­innervated muscles. Some electromyographers have difficulty with the notion that the C6–C7-­ innervated muscles are important to sample, because the distal median hand muscles are innervated by the C8–T1 roots. One must remember that the distribution of numbness (not the weakness) in CTS may be very similar to the numbness noted in C6–C7 radiculopathies. Of course, because each case is different, the electromyographer must always be willing to modify each study throughout the testing, based on abnormalities noted as the study progresses. 

Special Situation: EDX Studies After Carpal Tunnel Release It is not uncommon for a patient who has previously undergone carpal tunnel release surgery to be referred for EDX studies. The patient may either have recently undergone surgery with no clinical improvement or may have developed recurrent symptoms a long period of time after successful carpal tunnel decompression. In some cases, the patient will not have had a preoperative EDX study to confirm the diagnosis of CTS, which further complicates the issue. Thus, every electromyographer should be aware of

C

D Fig. 20.20  Persistent “slowing” following demyelination and remyelination.  (A) The process of myelination is completed at approximately age 3. (B) Between childhood and adulthood, the limb grows in length; however, the number of internodes does not change. (C) Demyelination occurs at the site of compression (blue arrows). (D) After the compression is successfully released, remyelination occurs. However, the new internodes are short, the same distance apart that they were when originally laid down as a child. Therefore, more nodes are required to remyelinate the original site of compression. The greater the number of nodes of Ranvier, the more depolarizations and, hence, the longer total time of depolarization. Thus, conduction velocity across the remyelinated area of compression will be slower than normal, because of the increase in number of nodes.

what happens to nerve conduction study abnormalities after successful carpal tunnel release surgery. In general, the distal latencies and amplitudes improve both for median motor and sensory studies. However, this may take many weeks to months, and in some studies, improvement continues up to a year after surgery. However, some slowing may persist indefinitely. In the authors’ experience:    1. Median distal motor latencies improve and usually return to the “normal” range. Never do distal latencies remain in the demyelinating range (i.e., >130% the upper limit of normal) after successful carpal tunnel release. 2. Median sensory latencies improve and usually return to the “normal” range. Never do conduction velocities remain in the demyelinating range (i.e., 4.5 ms (provided CMAP amplitude is not markedly reduced) DML comparing FDI to ADM: >2.0-ms difference DML comparing symptomatic FDI to contralateral FDI: >1.3 ms difference DML comparing ulnar INT to second lumbrical: >0.4 ms difference

The following patterns denote ulnar neuropathy at the wrist with certainty: DML to FDI in the demyelinating range: >130% upper limit of normal (i.e., any DML to the FDI >6.0 ms) Focal slowing across the wrist during inching studies: ≥0.5 ms over a 1-­cm increment, recording FDI Conduction block, comparing palm and wrist stimulations, recording FDI Conduction velocity slowing across the wrist, recording FDI  Special considerations: • If the superficial sensory branch is affected, the SNAP amplitude will be low or absent, with a normal dorsal ulnar cutaneous SNAP. (Caution must be taken in interpreting this pattern, which also can occur in patients with UNE.) • Occasional false-­positive results occur when using the DML to FDI or ADM; comparing DML to FDI versus ADM; and the lumbrical-­interossei study, especially in cases of moderate or severe UNE with axonal loss. Wrist versus palmar stimulation studies, or inching studies across the wrist should be done to demonstrate UNW with certainty. • If the dorsal ulnar cutaneous sensory study is performed and is absent, it is prudent to stimulate the superficial radial sensory nerve along the lateral radius with the recording electrodes in place for the dorsal ulnar cutaneous sensory study to ensure that an anomalous innervation is not present (recall there is a very rare anomalous innervation wherein the superficial radial sensory nerve supplies the entire dorsum of the hand, including the usual territory of the dorsal ulnar cutaneous sensory nerve).

ADM, Abductor digiti minimi; CMAP, compound muscle action potential; DML, distal motor latency; FDI, first dorsal interosseous; INT, interossei; SNAP, sensory nerve action potential; UNE, ulnar neuropathy at the elbow; UNW, ulnar neuropathy at the wrist.

cases of ulnar nerve entrapment in the arm or forearm, which can present with similar symptoms and signs. 

ELECTROPHYSIOLOGIC EVALUATION Nerve Conduction Studies The findings on nerve conduction studies in UNW depend on (1) whether the superficial sensory branch is involved and (2) if the deep motor branch is involved, whether it is affected proximal or distal to the hypothenar muscles. If the lesion is distal, affecting only the deep palmar motor branch after the take-­off to the hypothenar muscles, then the routine ulnar sensory study, recording the fifth digit, and the routine ulnar motor conduction study, recording the ADM, will be normal. In suspected UNW, additional nerve conduction studies must always be performed to detect abnormalities that may not be present on routine ulnar motor and sensory studies (Box 23.2). In addition to routine ulnar motor studies recording ADM and sensory studies recording digit 5, the following studies often are helpful. Ulnar Motor Studies Recording the First Dorsal Interosseous In all cases of suspected UNW, it is imperative to perform ulnar motor studies recording the first dorsal interosseous

(FDI). In lesions of the distal deep palmar motor branch, the latency to the FDI may be prolonged with a decreased compound muscle action potential (CMAP) amplitude. Comparison with the contralateral asymptomatic side often is helpful as well. In cases where the lesion is more proximal, affecting the hypothenar branches, the distal motor latency (DML) to the ADM also may be prolonged, with a decreased CMAP amplitude. However, one of the patterns highly suggestive of UNW is preferential involvement of the distal deep palmar motor branch, whereby the ulnar motor study recording the FDI is affected out of proportion to the ulnar motor study recording the ADM. Comparison of their relative distal motor latencies often can be helpful. 

Normal Values DML to FDI

≤4.5 ms

DML comparing FDI to ADM

≤2.0 ms difference

DML comparing symptomatic FDI to contralateral FDI

≤1.3 ms difference

ADM, Abductor digiti minimi; DML, distal motor latency; FDI, first dorsal interosseous.

SECTION VIII   Clinical Disorders

406

sensory study in the context of an abnormal digit 5 ulnar sensory study certainly suggests a diagnosis of UNW, this is not always the case. This pattern does not necessarily exclude the possibility of UNE (see Chapter 22). In some patients with definite UNE with axonal loss (although usually mild), the dorsal ulnar cutaneous sensory potential is spared. This is thought to be due to preferential fascicular sparing of the dorsal ulnar cutaneous sensory fibers. Therefore care must be taken when interpreting the findings of a patient with a normal dorsal ulnar cutaneous SNAP and an abnormal digit 5 ulnar sensory response, especially if there is no conduction block or focal conduction velocity slowing across the elbow. These findings must be interpreted in light of findings on the ulnar motor studies and the needle electromyographic (EMG) study. Only when the dorsal ulnar cutaneous sensory study is abnormal is one assured that the lesion is above the level of the wrist; the converse is not always true. 

Fig. 23.4  Occupational and activity risk factors for ulnar neuropathy at the wrist.  Occupations that require repetitive use of hand tools can result in pressure on the hypothenar eminence (upper arrow). In addition, certain activities, especially prolonged cycling, can similarly result in ulnar neuropathy at the wrist (bottom arrow).

Dorsal Ulnar Cutaneous Sensory Study In cases of suspected UNW where the routine ulnar sensory conduction to digit 5 is abnormal, it is important to study the dorsal ulnar cutaneous sensory nerve. As the dorsal ulnar cutaneous sensory nerve arises 5–8 cm proximal to the wrist, it is expected to be normal in all cases of UNW. A normal antidromic response is greater than 8 μV, but, as in other uncommonly performed sensory nerve conduction studies, comparison with the contralateral asymptomatic side frequently is helpful. Any potential that is less than 50% of the amplitude of the contralateral asymptomatic side likely is abnormal as well, even if the absolute amplitude is greater than 8 μV.1 Although the dorsal ulnar cutaneous sensory study often is helpful in establishing the level of the lesion, there are significant limitations of which every electromyographer must be aware. Although a normal dorsal ulnar cutaneous 1Very

rarely, there is an anomalous innervation wherein the superficial radial sensory nerve supplies the entire dorsum of the hand, including the usual territory of the dorsal ulnar cutaneous sensory nerve. Thus, in cases where the dorsal ulnar cutaneous sensory response is absent, it is prudent to stimulate the superficial radial sensory nerve along the lateral radius, with the recording electrodes in place for the dorsal ulnar cutaneous sensory study, to ensure that this very rare anomalous innervation is not present (see Chapter 7, Fig. 7.14).

Median Second Lumbrical Versus Ulnar Interossei Distal Motor Latencies The lumbrical-­interossei distal latency comparison often is performed as a sensitive, internal comparison study to demonstrate median nerve slowing across the carpal tunnel (see Chapter 20, Fig. 20.10). However, this study can be used just as effectively to demonstrate UNW (Fig. 23.5), looking for significant slowing of ulnar compared with median fibers across the wrist. Because the interossei are innervated by the distal deep palmar motor branch of the ulnar nerve and the second lumbrical is innervated by the median nerve, this comparison test can be very useful in identifying ulnar slowing at the wrist. A DML difference of greater than 0.4 ms comparing the ulnar interossei with the median second lumbrical, stimulating the nerves at the same distance, suggests focal slowing of the ulnar nerve across the wrist. This study is reliable and easy to perform. However, two limitations must be kept in mind. First, if an ulnar neuropathy has a moderate or severe amount of axonal loss, be it at the wrist or higher, one should expect some mild slowing across the wrist simply on the basis of loss of some of the fastest conducting axons. Second, the lumbrical-­interossei study will fail in cases of UNW if there is a coexistent median neuropathy at the wrist. This is generally not an issue when using this comparison study for median neuropathy at the wrist, as UNW is so rare. However, when looking for a UNW, an incidental median neuropathy at the wrist may not be that uncommon.  Short Segment Incremental Studies Using a technique identical to that used for ulnar nerve lesions at the elbow, short segment incremental studies, or “inching,” can be effectively performed at the wrist, recording the FDI, looking for an abrupt change in either latency or amplitude (Fig. 23.6). One-­centimeter increments are carefully marked off from 2–4 cm above the distal wrist crease to 4–5 cm below. The ulnar nerve is then stimulated supramaximally at each location at successive 1-­cm intervals, from below to above the wrist. Any abrupt increase in latency or drop in amplitude

Chapter 23 • Ulnar Neuropathy at the Wrist 407

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Fig. 23.5  Lumbrical-­interossei comparison study. This study is used most often in the diagnosis of carpal tunnel syndrome but can be equally helpful in the diagnosis of ulnar neuropathy at the wrist. The median nerve is stimulated at the wrist (S1), while the second lumbrical muscle is recorded (right top trace); the ulnar nerve is stimulated at the wrist (S2), using the same distance, while the interossei muscles are recorded (right bottom trace). In normal controls, latencies are similar. In a patient with ulnar neuropathy at the wrist, the interossei latency is prolonged compared with the second lumbrical.

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between successive stimulation sites implies focal demyelination. In normal individuals, the latency between two successive 1-­cm stimulation sites usually is 0.1–0.3 ms and rarely 0.4 ms. Any latency shift ≥0.5 ms suggests focal slowing.  Wrist and Palmar Stimulation Comparing the CMAP amplitudes stimulating at the wrist and palm can be technically easier than inching across the wrist and yields similar information (Fig. 23.7). To perform this study, the ulnar nerve is stimulated 3 cm above the wrist and 4 cm distal to the distal wrist crease in the palm, recording the FDI. Whereas inching requires multiple stimulations at 1-­cm increments, this study only requires single palm and wrist stimulations. UNW can be localized either by finding a conduction block between the wrist and palm stimulation sites or by finding conduction velocity slowing across the wrist. Similar to all routine motor studies, if a nerve is stimulated at two sites, a conduction velocity can be calculated. In UNW, any conduction velocity less than 37 m/s is considered abnormal and is of localizing value. In UNW, the demonstration of conduction block or conduction velocity slowing is most helpful in definitively

Fig. 23.6  Short segment incremental study of the ulnar nerve across the wrist.  Left, Recording the first dorsal interosseous, the ulnar nerve is stimulated in successive 1-­cm increments across the wrist. Right, Note the abrupt increase in amplitude, shift in latency, and change in morphology of the compound muscle action potential between 2 and 3 cm distal to the distal wrist crease (DWC). Inching studies allow for exact localization of the lesion. (From Preston DC, Shapiro BE, Schecht HM. Ganglion cyst at Guyon’s canal: electrophysiology and pathology. J Clin Neuromusc Dis. 2001;3:89–91.)

localizing the lesion. However, additional information is also gained about prognosis, as demyelinating lesions have a far better prognosis than those associated with axonal loss.  Comparison of the Various Electrophysiologic Tests in Ulnar Neuropathy at the Wrist There has been little data comparing the relative usefulness of the various studies outlined earlier, because UNW is relatively uncommon. Most reports of UNW have been single case reports or reports of a small number of patients. One large study of 20 consecutive patients with clinically defined UNW was performed prospectively, comparing the following studies: (1) wrist and palmar stimulation studies, recording FDI, looking for conduction block across the wrist; (2) wrist and palmar stimulation studies, recording FDI, looking for conduction velocity slowing across the wrist; (3) lumbrical-­interossei study, comparing ulnar versus median distal latencies; and (4) routine ulnar motor studies, recording FDI and ADM, comparing their respective DMLs. In five patients, inching studies across the wrist also were performed. Importantly, these studies were also compared

408

SECTION VIII   Clinical Disorders

P9 PV $PSOLWXGH P9 :ULVW Fig. 23.7  Wrist and palm stimulation in ulnar neuropathy at the wrist.  As an alternative to inching studies, a compound muscle action potential can be recorded at the first dorsal interosseous with stimulation at the wrist and palm, looking for conduction block and/or conduction velocity slowing across the ulnar wrist. Note that in this case of ulnar neuropathy at the wrist (UNW), there is a large decrease in amplitude with stimulation at the wrist compared to the palm, signifying conduction block and a slowed conduction velocity. Both findings localize the ulnar neuropathy to the wrist. CV, Conduction velocity; DWC, distal wrist crease.

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in 30 asymptomatic normal control subjects and in 20 consecutive disease control patients with definite UNE. The most sensitive and specific studies for localizing the lesion to the wrist were conduction block across the wrist and a slowed wrist-­to-­palm conduction velocity recording the FDI. Conduction block was found in 70% and a slowed wrist-­to-­ palm conduction velocity in 80% of patients with UNW, using wrist and palmar stimulation (Fig. 23.8). Overall, 95% of the patients with UNW had either conduction block or a slowed conduction velocity. These findings were 100% specific. Neither conduction block nor conduction velocity slowing across the wrist was found in any of the control patients with UNE. Of the five patients in whom inching was performed, all showed focal slowing and conduction block. The lumbrical-­interossei comparison study had a sensitivity of 60% (Fig. 23.9). However, one patient with a severe UNE had an abnormal study (latency difference of 0.6 ms). One reason for the lower than expected sensitivity for this study was the presence of coexistent median neuropathy at the wrist in 25% of patients. A prolonged DML to the FDI or ADM also had a lower sensitivity, in the range of 55%–60% (Fig. 23.9). More importantly, prolonged distal latencies to these muscles were also less specific than the previously described studies. A prolonged DML to the FDI was found in one patient with mild UNE and in 40% of patients with severe UNE. Similarly, a prolonged DML to the ADM was found in 40% of patients with severe UNE. The prolonged DMLs in patients with UNE presumably were the result of axonal loss and dropout of some of the faster conducting fibers. The least sensitive study for UNW was the comparison of DMLs to the FDI versus ADM, being abnormal in only 15% of patients with UNW. However, one patient with a mild UNE also had a relatively prolonged DML to FDI compared with ADM. The important points to take away from this study are as follows:    1. By performing an additional stimulation at the palm, while recording the FDI, conduction block or focal

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slowing across the wrist can be demonstrated in 95% of patients with clinically definite UNW. This finding was 100% specific; it was not seen in any control patient with UNE. 2. Inching studies across the wrist also are very sensitive and specific. However, these studies are more time-­ consuming and technically demanding than simply stimulating at one additional site in the palm. 3. The lumbrical-­interossei study is a sensitive and helpful test, with one important exception. Its usefulness is greatly diminished if there is a coexistent median neuropathy at the wrist. Rarely, a false-­positive result can occur if a patient has a severe UNE. Increasing the cutoff value to 0.7 ms or above may eliminate this problem. 4. Prolongation of the DML to FDI or ADM is much less sensitive than conduction block or slowing across the wrist, recording the FDI. In addition, it is also much less specific, being present in some cases of UNE. 5. Comparing the DML to FDI versus ADM is only infrequently helpful, being fairly insensitive to UNW. 

Electromyographic Approach The needle EMG examination in suspected UNW is straightforward (Box 23.3). The FDI and ADM must be sampled, with the electromyographer looking for involvement of the distal and proximal deep palmar motor branches, respectively. The flexor digitorum profundus (FDP) 5 and flexor carpi ulnaris (FCU) must be sampled to exclude an ulnar neuropathy proximal to the wrist. Finally, median-­and radial-­innervated C8 muscles (e.g., abductor pollicis brevis, flexor pollicis longus, extensor indicis proprius) and the lower cervical paraspinal muscles must be sampled to exclude a cervical root or motor neuron lesion. As in UNE, the lesion in UNW can be purely axonal, indicated by low CMAP amplitudes at ADM and FDI with normal or only mild slowing of distal latency. In these cases, it can be difficult to differentiate a lesion of the deep palmar motor branch from a lesion proximal to the dorsal root ganglion (cervical root or motor neuron). The EMG is helpful

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Fig. 23.8  Conduction block and focal slowing across the wrist.  Top, Change in first dorsal interosseous (FDI) compound muscle action potential (CMAP) amplitude with the ulnar nerve stimulated above and below the wrist is plotted for normals, patients with ulnar neuropathy at the wrist (UNW), and patients with ulnar neuropathy at the elbow (UNE) (mild and severe). Conduction block is calculated as follows: (palmar CMAP amplitude minus wrist CMAP amplitude) / palmar CMAP amplitude. Bottom, Conduction velocity across the ulnar wrist, recording the FDI, is plotted for normals, patients with UNW, and patients with UNE (mild and severe). Normal limits are shown as dotted lines. (From Cowdery SR, Preston DC, Herrmann DN, et al. Electrodiagnosis of ulnar neuropathy at the wrist: conduction block versus traditional tests. Neurology. 2002;59:420–427.)

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Fig. 23.9  Distal motor latency studies in ulnar neuropathy at the wrist (UNW).  Distal motor latencies to the first dorsal interosseous (top left), difference in distal motor latencies between the interosseous and lumbrical (top right), and distal motor latencies to the abductor digiti minimi (bottom left) are plotted for normals, patients with UNW, and patients with ulnar neuropathy at the elbow (UNE) (mild and severe). Normal limits are shown as dotted lines. Note the false-­positive results that occur in some cases of UNE. FDI, First dorsal interosseous. (From Cowdery SR, Preston DC, Herrmann DN, et al. Electrodiagnosis of ulnar neuropathy at the wrist: conduction block versus traditional tests. Neurology. 2002;59:420–427.)

410

SECTION VIII   Clinical Disorders

Box 23.3  Recommended Electromyographic Protocol for Ulnar Neuropathy at the Wrist Routine studies: 1. Distal deep palmar motor ulnar-­innervated muscle (first dorsal interosseous) 2. Proximal deep palmar motor ulnar-­innervated branches to hypothenar muscles (abductor digiti minimi) 3. Forearm ulnar-­innervated muscles (flexor carpi ulnaris and flexor digitorum profundus 5) If any of the ulnar-­innervated muscles are abnormal, test the following additional muscles: 4. At least two non-­ulnar lower trunk/C8-­innervated muscles (e.g., abductor pollicis brevis, flexor pollicis longus, extensor indicis proprius) to exclude a lower trunk brachial plexopathy, polyneuropathy, C8–T1 radiculopathy, or motor neuron disease 5. C8 and T1 paraspinal muscles Special consideration: If the pathology at the wrist is purely axonal and spares sensory fibers, it is difficult to completely exclude a lesion proximal to the dorsal root ganglion (i.e., root or motor neuron).

in this regard. The electromyographer can confirm that the abnormalities are limited to ulnar-­innervated muscles distal to the wrist by also sampling proximal ulnar-­innervated and non-­ulnar C8–T1-­innervated muscles. Again, however, early motor neuron disease may be difficult to exclude. In these cases, the clinical presentation and serial follow-­up remain important. 

ULTRASOUND CORRELATIONS As noted earlier, UNW is very uncommon and has a limited differential diagnosis that includes compression both external and internal to the wrist, the latter from various structural lesions. Accordingly, neuromuscular ultrasound plays an important role in the evaluation of these patients. Similar to other ulnar neuropathies, it is especially helpful in those cases where the electrodiagnostic study is unable to localize the ulnar neuropathy and UNW remains in the differential diagnosis. To visualize the ulnar nerve at the wrist, the probe is placed in short axis over the median nerve at the distal wrist crease at the standard starting median nerve location. Once the median nerve is identified, the probe is slowly moved toward the ulnar side of the wrist looking for a prominent hypoechoic structure, which is the ulnar artery. This can be confirmed by color or power Doppler. Once the ulnar artery is identified, the probe is very slowly moved toward the distal wrist. The pisiform bone will then appear on the ulnar side of the wrist. It is easily identified by its well-­ demarcated bone shadow. The ulnar nerve at this location (the entrance to Guyon’s canal) is found between the ulnar artery and the pisiform bone (Fig. 23.10). Its cross-­ sectional area should then be measured while inspecting for any nearby structural lesions. The floor of Guyon’s canal is the transverse carpal ligament with the roof formed by the superficial palmar carpal ligament (Fig. 23.11). Moving slightly distally into the palm, the nerve divides into its

Fig. 23.10  Ulnar nerve at the wrist.  Top, Short axis, ulnar nerve at the wrist, native image. Bottom, Same image, with the ulnar nerve in yellow, ulnar artery in red, and pisiform bone in green. At the wrist, the ulnar nerve is located between the ulnar artery and the pisiform bone.

superficial and deep branches. The deep branch then moves medially while the superficial branch remains lateral, adjacent to the hook of the hamate. The ulnar artery also divides to follow the two branches of the nerve. External compression, such as from repetitive use of hand tools or in bikers, can result in an enlarged ulnar nerve (Fig. 23.12). However, more importantly, there are several structural abnormalities to specifically look for when assessing the ulnar nerve at the wrist. The most common is a ganglion or synovial cyst (Fig. 23.13). These cysts most frequently arise from the nearby pisiform-­triquetral joint, although they have been reported to arise from other carpal joints and tendon sheaths. They often form a “dumbbell” shape within Guyon’s canal, which compresses the ulnar nerve. As the ulnar nerve runs with the ulnar artery, rare cases of thrombosis or aneurysm of the ulnar artery can occur, which affect the ulnar nerve in the wrist, either from direct compression or ischemia. Similar to the reverse palmaris longus for the median nerve, the ulnar nerve at the wrist can also be affected by anomalous muscles. The most common is an accessory ADM (Fig. 23.14). This muscle may originate from different forearm structures but most often arises from the forearm superficial fascia and the distal tendon of the palmaris longus. It runs anterior to the ulnar nerve and artery in Guyon’s canal to insert on the pisiform bone near the origin of the ADM. In some cases, it continues as a muscle in the palm to insert on the base of the proximal fifth phalanx. Note that the presence of this muscle on ultrasound may be incidental. Only when it is large can it result in compression of the ulnar nerve at the wrist. Although uncommon, arthritis and bony abnormalities can affect the ulnar nerve in the wrist. Arthritis of the pisotriquetral joint can affect the nerve. Bony callus from remote fracture or bone fragments from a recent fracture can affect the ulnar nerve near or at the wrist (Fig. 23.15). This includes fracture of the hook of the hamate. Bone is easily recognized on ultrasound by its hyperechogenicity and posterior acoustic shadowing.

Chapter 23 • Ulnar Neuropathy at the Wrist 411

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Fig. 23.11  Normal cross-sectional anatomy at the wrist.  Axial magnetic resonance images. Top, Level at the entrance to Guyon’s canal. Bottom, Level at the exit from Guyon’s canal. Left, Native images. Right, Same images with the ulnar nerve in yellow with a U, superficial branch of the ulnar nerve in yellow with an S, deep branch of the ulnar nerve in yellow with a D, median nerve in yellow with an M, ulnar artery in red, transverse carpal ligament in purple, superficial palmar carpal ligament in light blue, and the pisiform and hamate bones in green.

Fig. 23.12  Ulnar neuropathy at the wrist from external compression.  Left, Native images. Right, Same images with the ulnar nerve in yellow, ulnar artery in red, and pisiform bone in green. Top, Short axis at the ulnar wrist. Bottom, Long axis. Note the marked enlargement of the ulnar nerve.

412

SECTION VIII   Clinical Disorders







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Fig. 23.13  Ulnar neuropathy at the wrist from compression from a ganglion cyst. Top left, Short axis native image at the ulnar wrist. Top right, Short axis slightly distal to the ulnar wrist, native image. Middle, Same images with the ulnar nerve in yellow, ulnar artery in red, ganglion cyst in purple, pisiform bone edge in green, and posterior acoustic shadowing in light blue. Note that the images at the wrist are normal, but slightly distal is a large anechoic oval mass that is displacing the ulnar nerve and artery. The posterior acoustic enhancement is a common ultrasound feature that helps to identify cystic lesions. Bottom left, Native image, long axis slightly distal to the ulnar wrist. Bottom right, Same image with color flow Doppler. Note the large anechoic oval mass with posterior acoustic enhancement that is displacing the ulnar artery above.

Chapter 23 • Ulnar Neuropathy at the Wrist 413

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Fig. 23.14  Ulnar nerve and an accessory abductor digiti minimi (AADM).  Two different individuals with an AADM muscle. Top, Left and Middle, Short axis at the ulnar wrist, native images. Bottom, Left and Middle, Same images with the ulnar nerve in yellow, ulnar artery in bright red, ulnar vein in blue, pisiform bone in green, and an AADM in dark red. Right, Anatomic dissection of the hand. The pisiform bone is marked by an asterisk. ADM, Abductor digiti minimi muscle; AF, antebrachial fascia; AH and red arrow, accessory head of abductor digiti minimi muscle; PLT, palmaris longus tendon muscle; UA, ulnar artery; UN, ulnar nerve. (Anatomic dissection adapted with permission from Ballesteros LE, Ramirez LM. Possible implications of an accessory abductor digiti minimi muscle: a case report. J Brach Plex Periph Nerve Inj. 2007;2:22. https://doi.org/10.1186/1749-­7221-­2-­22.)

Fig. 23.15  Ulnar neuropathy near the wrist from a bone fragment.  Left, Short axis images just proximal to the ulnar wrist, native images, successive images moving from distal (top) to proximal (bottom). Right, Same images with the ulnar nerve in yellow, ulnar artery in red, and the bone in green. Note that a bone fragment projects up (middle image) and deforms the ulnar nerve. Ulnar neuropathy near the wrist can occur from bone fragments from the distal ulna or carpal bones proper.

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SECTION VIII   Clinical Disorders

digits 4 and 5 were strong. There was no Tinel’s sign at the elbow. Sensation to pin and light touch was normal.

EXAMPLE CASE Case 23.1

Summary

History and Physical Examination

The history and physical examination both are suggestive of ulnar neuropathy. Despite the normal sensory examination, the patient noted paresthesias and numbness in the ulnar-­innervated fourth and fifth digits. In addition, the motor examination showed atrophy and weakness of the right ADM and the interossei. Thus the patient has clear symptoms of ulnar sensory and motor dysfunction. The suggestion of pain at the right elbow leads one to seriously consider the possibility of ulnar neuropathy in the region of the elbow. However, at this point, there are no other

A 36-­year-­old right-­handed man complained of numbness and paresthesias over digits 4 and 5 and right arm pain for 6 months. The sensory disturbance had become worse over the past few weeks. He worked in a library stacking books and denied any history of trauma. He had vague complaints of right elbow pain. On examination, there was mild atrophy of the intrinsic hand muscles. There was mild weakness of the ADM and interossei muscles on the right. The long flexors of

CASE 23.1 Nerve Conduction Studies Amplitude Motor = mV; Sensory = μV

Stimulation Site

Recording Site

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52

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LT

NL

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31

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   Note: All sensory and mixed latencies are peak latencies. All sensory and mixed-­nerve conduction velocities are calculated using onset latencies. The reported F-­wave latency represents the minimum F-­wave latency. ADM, Abductor digiti minimi; APB, abductor pollicis brevis; LT, left; m, motor study; NL, normal; RT, right; s, sensory study.

CASE 23.1 Additional Nerve Conduction Studies

Nerve Stimulated

Stimulation Site

Dorsal ulnar (s)

Lateral wrist

Amplitude Motor = mV; Sensory = μV

Conduction Velocity (m/s)

Latency (ms)

Recording Site

RT

LT

RT

LT

NL

RT

LT

NL

Dorsal medial hand

24

26

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50

51

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Second lumbrical Interosseous

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4.4

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Wrist Below elbow Above elbow Palm

NL

   FDI, First dorsal interosseous; LT, left; m, motor study; NL, normal; RT, right; s, sensory study.

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F-­wave Latency (ms) RT

LT

NL

Chapter 23 • Ulnar Neuropathy at the Wrist 415 CASE 23.1 Electromyography Spontaneous Activity Muscle

Insertional Activity

Fibrillation Potentials

Voluntary Motor Unit Action Potentials

Fasciculation Potentials Activation

Configuration Recruitment

Duration

↓

+1

Amplitude

Polyphasia

↑

+1

0

NL

Right ADM

↑

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0

NL

↓

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Right APB

NL

0

0

NL

NL

NL

NL

NL

Right EIP

NL

0

0

NL

NL

NL

NL

NL

Right FCU

NL

0

0

NL

NL

NL

NL

NL

Right FDP 5

NL

0

0

NL

NL

NL

NL

NL

Right FDI

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   ↑ = Increased; ↓ = slightly reduced; ADM, abductor digiti minimi; APB, abductor pollicis brevis; EIP, extensor indicis proprius; FCU, flexor carpi ulnaris; FDI, first dorsal interosseous; FDP, flexor digitorum profundus; NL, normal.

signs to help localize the lesion. The fact that the long flexors to digits 4 and 5 (ulnar portion of the FDP) are normal suggests that the ulnar neuropathy either is mild and has not affected these more proximal muscles or is more distal. The clinical approach to this case is similar to that used in other cases of ulnar nerve dysfunction. The differential diagnosis includes UNW, UNE, lower trunk/ medial cord lesions of the brachial plexus, or a C8–T1 radiculopathy. The nerve conduction studies include, first, a normal median motor conduction study recording the abductor pollicis brevis muscle. However, the ulnar motor conduction study shows a mildly low CMAP amplitude recording the ADM with a moderately prolonged distal latency but a normal conduction velocity in the forearm and across-­elbow segments. There is no conduction block or significant differential slowing of the ulnar nerve across the elbow (>10–11 m/s) to substantiate the possibility of UNE. Median and ulnar routine sensory studies are then performed. The median study is completely normal, but the ulnar study shows a decreased amplitude on the right with a normal amplitude on the left. Therefore, at this point in the study, one can be fairly certain that the patient has an ulnar neuropathy because both the ulnar motor and sensory studies are abnormal. The normal median motor and sensory studies exclude a more generalized process such as a polyneuropathy to explain the abnormal ulnar motor and sensory findings. Although a lower trunk brachial plexopathy is still a consideration, one would expect to also see a low median CMAP amplitude in this case. At this point in the study, we are confronted with a common problem, that of a nonlocalizable ulnar neuropathy. There is no focal slowing or conduction block to suggest an UNE. Several questions should be addressed.

What Is the Significance of the Prolonged Ulnar DML? The only unusual abnormality is the moderately prolonged distal latency to the ADM muscle (4.1 ms). This value is more than 125% of the upper limit of normal and suggests the possibility of a demyelinating lesion at the wrist. Recall from the history that the patient uses his hands to stack books repetitively, which may be a risk factor for entrapment of the ulnar nerve at the wrist. Further studies of the ulnar nerve at the wrist are indicated. 

What Other Tests Can Be Used to Help Localize the Lesion? Because the routine ulnar conduction studies typically are normal or equivocal in UNW, additional nerve conduction studies are required to localize the lesion to the wrist (see Box 23.2). In UNW, the dorsal ulnar cutaneous sensory response is expected to be normal, whereas the sensory potential to the fifth digit may be abnormal. When the dorsal ulnar cutaneous sensory response is checked and compared with the contralateral side, it is normal and symmetric bilaterally. The presence of a normal dorsal ulnar cutaneous response with an abnormal digit 5 ulnar response is consistent with UNW, although, as already noted, this pattern occasionally can be seen in mild cases of UNE. Next, the lumbrical-­ interossei comparison study is performed using identical distances. On the left (asymptomatic) side, an identical distal latency of 4.4 ms to both the lumbrical and interossei is found. On the involved right side, however, there is a clear asymmetry: the ulnar latency is 1.1 ms longer than the median latency. Any difference of more than 0.4 ms suggests focal slowing across the wrist. Lastly, the ulnar motor study is repeated but recording the FDI. There is no focal slowing or conduction block across the elbow. However, the FDI distal latency on the involved right side is moderately prolonged at 5.2 ms, with a normal value of 4.4 ms on the contralateral side. In addition, the CMAP amplitude is reduced on the right

416

SECTION VIII   Clinical Disorders

compared with the left. Comparing the distal latency to the FDI to that of the ADM, there is a difference of 1.1 ms, which is in the range of normal (≤2.0 ms). When an additional stimulation is given in the palm while recording the FDI, the amplitude markedly increases to 8.0 mV, signifying a conduction block between the palm and wrist. In addition, the calculated velocity across the wrist is in the demyelinating range, being less than 37 m/s. Proceeding to the needle EMG study, particular attention must be paid to the ulnar-­innervated muscles above the level of the wrist, which would be expected to be normal in cases of UNW. The EMG study shows active denervation and reinnervation in the FDI (innervated by the distal deep palmar motor branch of the ulnar nerve). The right ADM yields similar findings, indicating that the branch to the hypothenar muscles is also affected. The right abductor pollicis brevis is normal, as is the right extensor indicis proprius. The normal findings in these two non-­ulnar C8-­ innervated muscles again signify that the problem likely is limited to the ulnar nerve. Finally, both proximal ulnar muscles, the FCU and FDP 5, are sampled and are normal. Therefore, with EMG and nerve conduction studies completed, we are ready to form an electrophysiologic impression. IMPRESSION: There is electrophysiologic evidence of a right ulnar neuropathy at the wrist. From the pattern of the nerve conduction and EMG data, we can conclude that the patient has an ulnar nerve lesion at the wrist affecting the superficial sensory branch and the proximal deep palmar branch. This pattern is one variant of UNW. In this case, the patient’s history, examination, and electrophysiologic results all correlate well. The atrophy and weakness of the intrinsic hand muscles correlate with the reduced ulnar CMAP amplitudes seen on nerve conduction studies and with the denervation and reinnervation with reduced recruitment of MUAPs revealed by the needle EMG findings. The findings that, taken together, tend to localize the lesion at the wrist include not only the EMG abnormalities that are limited to ulnar muscles distal to the wrist but also the intact dorsal ulnar cutaneous sensory response and the prolonged ulnar latency on the lumbrical-­interossei study. However, the study that unequivocally localizes the ulnar neuropathy to the wrist is the palmar stimulation compared to the wrist stimulation, while recording the FDI. The finding of focal demyelination across the wrist (conduction block and/or conduction velocity slowing) is the key finding. One can easily see that if additional studies had not been performed (i.e., the dorsal ulnar cutaneous sensory study, motor conduction study to the FDI including palmar stimulation, and lumbrical-­interossei distal latency comparison study), the erroneous diagnosis of a nonlocalizable ulnar neuropathy might have been made. The initial clue to this diagnosis on the nerve conduction studies was the relatively prolonged distal latency to the ADM muscle in conjunction with only a mildly reduced CMAP amplitude.

In this case, sensory symptoms and abnormalities on nerve conduction studies indicated an ulnar nerve lesion. However, one should remember that in other cases of UNW, in which the lesion affects the deep palmar motor branch in isolation, only the motor fibers are affected; the sensory fibers are spared. In such cases, excluding a lesion proximal to the dorsal root ganglion (either nerve root or anterior horn cell) may be very difficult. If the pathology is axonal loss alone and there is no focal slowing or conduction block of ulnar motor fibers across the wrist, making that differentiation is impossible. In those unusual cases, the EMG report must be considered indeterminate. Although EMG abnormalities may be limited to ulnar-­innervated muscles, the possibility that those muscles are the first to be affected in a lesion of the nerve root or anterior horn cells cannot be completely excluded. Indeed, there are cases of focal motor neuron disease that mimic UNW on initial presentation, preferentially affecting the deep palmar motor branch. In those cases, clinical history and often follow-­up electrophysiologic studies are required to make the differentiation.

Suggested Readings Bakke JL, Wolff HG. Occupational pressure neuritis of the deep palmar branch of the ulnar nerve. Arch Neurol Psychiatry. 1948;60:549. Cowdery SR, Preston DC, Herrmann DN, et al. Electrodiagnosis of ulnar neuropathy at the wrist: conduction block versus traditional tests. Neurology. 2002;59:420–427. Eckman PB, Perlstein G, Altrocchi PH. Ulnar neuropathy in bicycle riders. Arch Neurol. 1975;32:130. Hunt JR. Occupation neuritis of deep palmar branch of ulnar nerve: well defined clinical type of professional palsy of hand. J Nerv Ment Dis. 1908;35:673. Iyer VG. Palmaris brevis sign in ulnar neuropathy. Muscle Nerve. 1998;21:675–677. Kothari MJ, Preston DC, Logigian EL. Lumbrical and interossei recordings localize ulnar neuropathy at the wrist. Muscle Nerve. 1996;19:170–174. McIntosh KA, Preston DC, Logigian EL. Short segment incremental studies to localize ulnar entrapments at the wrist. Neurology. 1998;50:303–306. Moneim MS. Ulnar nerve compression at the wrist: ulnar tunnel syndrome. Hand Clin. 1992;8:337. Olney RK, Hanson M. AAEE case report no. 15: ulnar neuropathy at or distal to the wrist. Muscle Nerve. 1988;11:828. Parra S, Orenga JV, Ghinea AD, Estarelles MJ, Masoliver A, Barreda I, et al. Neurophysiological study of the radial nerve variant in the innervation of the dorsomedial surface of the hand. Muscle Nerve. 2018;58(5):732–735. Raynor EM, Shefner JM, Preston DC, et al. Sensory and mixed nerve conduction studies in the evaluation of ulnar neuropathy at the elbow. Muscle Nerve. 1994;17:785. Shea JD, McClain EJ. Ulnar-­nerve compression syndrome at and below the wrist. J Bone Joint Surg Am. 1969;51:1095. Wu JS, Morris JD, Hogan GR. Ulnar neuropathy at the wrist: case report and review of the literature. Arch Phys Med Rehabil. 1985;66:785.

SECTION VIII • Clinical Disorders PART I • Common Mononeuropathies

Radial Neuropathy

In the electromyography (EMG) laboratory, the radial nerve is studied less frequently than the median and ulnar nerves and their respective well-­known lesions. Nevertheless, entrapment of the radial nerve does occur, often affecting the main radial nerve either in the upper arm or axilla. Isolated lesions of its terminal divisions in the forearm, the posterior interosseous, and superficial radial sensory nerves, also occur. Although radial motor nerve conduction studies are technically demanding, the electrophysiologic evaluation of radial neuropathy usually is able to localize the lesion, assess the underlying pathophysiology, and provide useful information regarding severity and subsequent prognosis. In addition, similar to other entrapment neuropathies, neuromuscular ultrasound is often very useful in adding specific anatomic information regarding the location and etiology of a radial neuropathy.

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ANATOMY The radial nerve receives innervation from all three trunks of the brachial plexus and, correspondingly, a contribution from each of the C5–T1 nerve roots (Figs. 24.1 and 24.2). After each trunk divides into an anterior and posterior division, the posterior divisions from all three trunks unite to form the posterior cord. The posterior cord gives off the axillary, thoracodorsal, and subscapular nerves before becoming the radial nerve. In the high arm, the radial nerve first gives off the posterior cutaneous nerve of the arm, the lower lateral cutaneous nerve of the arm, and the posterior cutaneous nerve of the forearm (Fig. 24.3), followed by muscular branches to the three heads of the triceps brachii (medial, long, and lateral) and the anconeus. In some patients, there is evidence that the long head of the triceps may be supplied either by the axillary nerve or the posterior cord directly. The anconeus is a small muscle in the proximal forearm that effectively is an extension of the medial head of the triceps brachii. After giving off these muscular branches, the radial nerve wraps around the posterior humerus in the spiral groove. The posterior cutaneous nerve of the forearm accompanies the radial nerve through the spiral groove and remains in the posterior compartment of the arm before becoming subcutaneous approximately 6–7 cm directly proximal to the lateral epicondyle. Descending into the region of the elbow, the main radial nerve then pierces the lateral intermuscular septum to run between the brachialis and brachioradialis muscles. Muscular branches are

Fig. 24.1  Anatomy of the radial nerve.  The radial nerve receives innervation from all three trunks of the brachial plexus and, correspondingly, a contribution from each of the C5–T1 nerve roots. (Adapted with permission from Haymaker W, Woodhall B. Peripheral Nerve Injuries. Philadelphia, PA: WB Saunders; 1953.)

then given off to the brachioradialis and the long head of the extensor carpi radialis. The radial nerve then enters the radial tunnel, which is the space formed posteriorly by the distal humerus and radiocapitellar joint, the brachialis muscle medially, the brachioradialis muscle anteriorly, and the extensor carpi radialis brevis muscle laterally. The radial tunnel is approximately 5 cm in length and runs between the area where the radial nerve pierces the lateral intermuscular septum to where the deep motor branch enters the proximal edge of the supinator.a Next, 3–4 cm distal to the lateral epicondyle, the radial nerve bifurcates into two separate nerves: one superficial and the other deep. The superficial branch, known as the superficial radial sensory nerve, descends distally under the brachioradialis in the forearm and eventually moves subcutaneous over the radial bone to supply sensation over the lateral dorsum of the hand as well aSome

consider the radial tunnel to continue to where the posterior interosseous nerve leaves the distal border of the supinator.

417

418

SECTION VIII   Clinical Disorders &

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'RUVDOGLJLWDOQHUYHV Fig. 24.2  Anatomy of the radial nerve.  The radial nerve is derived from the posterior cord of the brachial plexus. In the high arm, the radial nerve first gives off the posterior cutaneous nerve of the arm, the lower lateral cutaneous nerve of the arm, and the posterior cutaneous nerve of the forearm, followed by muscular branches to the triceps brachii and anconeus. The radial nerve then wraps around the humerus, descending into the region of the elbow where muscular branches are given to the brachioradialis and long head of the extensor carpi radialis. The nerve then bifurcates into the superficial radial sensory and deep motor branch of the radial nerve. The deep motor branch supplies the extensor carpi radialis brevis (in most cases) and the supinator muscle before continuing on as the posterior interosseous nerve. The posterior interosseous nerve supplies the remainder of the wrist and finger extensors, as well as the abductor pollicis longus. (Adapted with permission from Haymaker W, Woodhall B. Peripheral Nerve Injuries. Philadelphia, PA: WB Saunders; 1953.)

as part of the thumb and the dorsal proximal phalanges of the index, middle, and ring fingers (Fig. 24.4). Distally, the nerve is quite superficial, running over the tendon to the extensor pollicis longus, where it can easily be palpated (Fig. 24.5). The deep branch, known as the deep radial motor branch, first supplies the extensor carpi radialis brevis and the supinator muscles before it enters the supinator muscle under the Arcade of Frohse (Fig. 24.6). The Arcade of Frohse is the proximal border of the supinator and in some individuals is quite tendinous. After the nerve enters the supinator, it is known as the posterior interosseous nerve, which then supplies the remaining extensors of the wrist, thumb, and fingers (extensor digitorum communis, extensor carpi ulnaris, abductor

Fig. 24.4  Sensory territory of the superficial radial sensory nerve.  The superficial radial sensory nerve supplies sensation over the lateral dorsum of the hand, as well as part of the thumb and dorsal proximal phalanges of the index, middle, and ring fingers.

Fig. 24.5  Superficial radial sensory nerve.  The superficial radial nerve runs distally in the forearm over the radial bone to supply sensation over the lateral dorsum of the hand, as well as part of the thumb and the dorsal proximal phalanges of the index, middle, and ring fingers. It runs over the extensor tendons to the thumb (arrows), where it can easily be palpated.

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Fig. 24.6  Anatomy of the radial nerve at the elbow.  Distal to the elbow, the radial nerve bifurcates into the superficial radial sensory and deep radial motor branch. The deep radial motor branch enters the supinator muscle under the Arcade of Frohse, where it is then known as the posterior interosseous nerve, which supplies the remaining extensors of the wrist, thumb, and fingers. (Adapted with permission from Wilbourn AJ. Electrodiagnosis with entrapment neuropathies. AAEM plenary session I: entrapment neuropathies. Charleston, South Carolina; 1992.)

pollicis longus, extensor indicis proprius [EIP], extensor pollicis longus, and extensor pollicis brevis). Although the posterior interosseous nerve is thought of as a pure motor nerve (supplying no cutaneous sensation), it does contain sensory fibers that supply deep sensation to the interosseous membrane and joints between the radial and ulna bones.

Nomenclature of the Branches of the Radial Nerve Near the Elbow One of the more confusing aspects of radial nerve anatomy is the inconsistency regarding the nomenclature of the branches of the radial nerve near the elbow used in various anatomic texts and clinical reports (Fig. 24.7). The following points should help the electromyographer when dealing with potential lesions of the radial nerve in this area: Radial Nerve Between the Spiral Groove and the Bifurcation Near the Elbow • Distal to the spiral groove but before the elbow, the main radial nerve always supplies two muscles: the brachioradialis and the extensor carpi radialis longus (also known as the long head of the extensor carpi radialis).

$UFDGHRI)URKVH Fig. 24.7  Anatomy and nomenclature of the radial nerve around the elbow.  As the main radial nerve enters the region of the elbow (purple), it supplies the brachioradialis (BR) and extensor carpi radialis longus (ECRL) muscles. It then divides into a superficial radial sensory branch (green) and a deep radial motor branch (yellow). The deep radial motor branch typically innervates the extensor carpi radialis brevis (ECRB) and supinator muscles before entering into the substance of the supinator muscle at the Arcade of Frohse. Past the Arcade of Frohse, the continuation of the deep radial motor branch is known as the posterior interosseous nerve (blue). However, please note that some anatomic texts define the posterior interosseous nerve as originating at the bifurcation of the main radial nerve and thus use the terms deep radial motor branch and posterior interosseous nerve interchangeably. If this definition is used, then both the ECRB and the supinator muscle would both be supplied by the posterior interosseous nerve. (Adapted with permission from Thomas SJ, Yakin DE, Parry BR, et al. The anatomical relationship between the posterior interosseous nerve and the supinator muscle. J Hand Surg Am 25. 2000;(5):936–941.)

• I n some individuals, the main radial nerve will also supply a third muscle, the extensor carpi radialis brevis muscle.b  The Bifurcation Near the Elbow • The main radial nerve always bifurcates into superficial and deep branches just distal to the elbow.  Superficial Branch • The superficial branch continues as a pure cutaneous sensory branch (the superficial radial sensory branch). • However, in a small number of individuals, there is an anatomic variation wherein the superficial branch near its origin will supply one muscle, the extensor carpi radialis brevis.b  Deep Branch • The deep radial motor branch first supplies the extensor carpi radialis brevis muscle in some individuals.b • It then supplies one or more branches to the supinator muscle before entering the supinator muscle proper. • The deep radial motor branch then runs under the Arcade of Frohse (the proximal border of the supinator) and through the supinator muscle. • After leaving the supinator muscle, branches are given off that supply the extensor muscles to the thumb and fingers as well as the abductor pollicis longus and extensor carpi ulnaris. The inconsistency in the nomenclature regarding these nerve branches involves where bThus,

the innervation to the extensor carpi radialis brevis has several normal variations: from the main radial nerve, the superficial radial nerve, and the deep radial motor branch of the radial nerve.

420

SECTION VIII   Clinical Disorders

the posterior interosseous nerve begins and whether the posterior interosseous nerve and the deep radial motor branch are one and the same nerve: • In some textbooks and many clinical reports, the entire deep radial motor branch is known as the posterior interosseous nerve, with the two names used interchangeably. Thus, using this anatomic definition, a complete posterior interosseous neuropathy (PIN) would include the supinator and the extensor carpi radialis brevis muscles, as well as the extensors to the thumb and fingers, and the abductor pollicis longus and extensor carpi ulnaris. • In most anatomic texts, however, only the segment of the deep branch between the bifurcation of the main radial nerve at the elbow to where the nerve enters the supinator muscle at the Arcade of Frohse is known as the deep radial motor branch. The posterior interosseous nerve is then the continuation of the deep radial motor branch after it enters the supinator. In the remainder of this text, we will use this latter anatomic definition. Thus, with this anatomic definition, a complete PIN would spare the supinator and the extensor carpi radialis brevis muscles. As the most common entrapment site of the posterior interosseous nerve is at the Arcade of Frohse, the use of this anatomic convention fits the common clinical syndromes most appropriately as well. 

CLINICAL Radial neuropathies can be divided into those caused by lesions at the spiral groove, lesions in the axilla, and isolated lesions of the posterior interosseous and superficial radial sensory nerves. These lesions usually can be differentiated by clinical findings.

Radial Neuropathy at the Spiral Groove The most common radial neuropathy occurs at the spiral groove. Here, the nerve lies juxtaposed to the humerus and is quite susceptible to compression, especially following prolonged immobilization (Fig. 24.8). One of the times this characteristically occurs is when a person has draped an arm over a chair or bench during a deep sleep or while intoxicated (‘Saturday night palsy’). The subsequent prolonged immobility results in compression and demyelination of the radial nerve. Other cases may occur after strenuous muscular effort, fracture of the humerus, or infarction from vasculitis. Clinically, marked wrist drop and finger drop develop (due to weakness of the EIP, extensor digitorum communis, extensor carpi ulnaris, and long head of the extensor carpi radialis), along with mild weakness of supination (due to weakness of the supinator muscle) and elbow flexion (due to weakness of the brachioradialis). Notably, elbow extension (triceps brachii) is spared. Sensory disturbance is present in the distribution of the superficial radial sensory nerve, consisting of altered

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Fig. 24.8  Radial nerve and the spiral groove.  The most common radial neuropathy occurs at the spiral groove on the posterior side of the humerus. Here, the nerve lies juxtaposed to bone and is susceptible to external compression.

sensation over the lateral dorsum of the hand, part of the thumb, and the dorsal proximal phalanges of the index, middle, and ring fingers. In isolated radial neuropathy at the spiral groove, median-­ and ulnar-­innervated muscles are normal. However, tested in a wrist drop and finger drop posture, finger abduction may appear weak, giving the mistaken impression of ulnar nerve dysfunction. To prevent this error, one should test the patient’s finger abduction (ulnar-­innervated function) with the fingers and wrist passively extended to a neutral wrist position. This often can be accomplished by placing the hand on a flat surface. 

Radial Neuropathy in the Axilla Radial neuropathy may occur in the axilla from prolonged compression. For instance, this is often seen in patients on crutches who use them inappropriately, applying prolonged pressure to the axilla. The clinical deficit is similar to that seen in radial neuropathy at the spiral groove, with the notable exception of additional weakness of arm extension (triceps brachii) and sensory disturbance extending into the posterior forearm and arm (posterior cutaneous nerves of the forearm and arm). Radial neuropathy in the axilla is differentiated from even more proximal posterior cord lesions by normal strength of the deltoid (axillary nerve) and latissimus dorsi (thoracodorsal nerve). 

Posterior Interosseous Neuropathy PIN clinically resembles entrapment of the radial nerve at the spiral groove at first glance. In both conditions, patients present with wrist drop and finger drop with sparing of elbow extension. However, with closer inspection, several important differences easily separate the two. In PIN, there is sparing of radial-­innervated muscles above the takeoff of the posterior interosseous nerve (i.e., brachioradialis, long

Chapter 24 • Radial Neuropathy 421

and short heads of the extensor carpi radialis, triceps). Thus, a patient with PIN still may be able to extend the wrist, but weakly, with a radial deviation. This is due to the relative preservation of the extensor carpi radialis longus and brevis that arise proximal to the posterior interosseous nerve, with a weak extensor carpi ulnaris. In addition, of course, are the sensory findings. In PIN, there is no cutaneous sensory loss. However, there may be pain in the forearm from involvement of the deep sensory fibers of the posterior interosseous nerve that supply the interosseous membrane and joint capsules. Five potential sites of compression of the deep radial motor branch/posterior interosseous nerve have been reported. These include (1) the medial proximal edge of the extensor carpi radialis brevis muscle; (2) the fibrous tissue anterior to the radiocapitellar joint between the brachialis and brachioradialis muscles; (3) the “Leash of Henry” (recurrent radial vessels that fan over the deep motor branch proximal to the supinator; (4) the Arcade of Frohse; and (5) the distal edge of the supinator muscle. PIN most often occurs as an entrapment neuropathy under the tendinous Arcade of Frohse. Rarely, other mass lesions (e.g., ganglion cysts, tumors) result in PIN. Radial Tunnel Syndrome This is one of the more controversial and disputed nerve entrapment syndromes. In radial tunnel syndrome, patients are reported to have isolated pain and tenderness in the extensor forearm, not unlike persistent tennis elbow, thought to result from compression of the posterior interosseous nerve near its origin. However, as opposed to patients with a true PIN (see previous discussion), these patients typically have no objective neurologic signs on examination and accordingly have normal EDX studies. They are said to have increased pain with maneuvers that contract the extensor carpi radialis or the supinator (e.g., resisted extension of the middle finger or resisted supination, respectively). However, there is little compelling evidence that this chronic pain syndrome is caused by any nerve entrapment in most patients. Nevertheless, this syndrome is important to know of, as it is not unusual for a patient to be referred to the EMG laboratory for evaluation of “radial tunnel syndrome.” In such cases, the focus of the EDX is to look for any objective evidence of a PIN, although in the absence of any weakness or other neurologic signs, the EDX study is almost always normal. Nevertheless, follow-­up with an ultrasound study of the deep motor branch of the radial nerve/ posterior interosseous nerve can be useful to exclude any structural abnormalities of this nerve (see later). 

bands, watches, or bracelets may result in compression of the superficial radial nerve. Handcuffs, especially when excessively tight, also characteristically result in a superficial radial neuropathy. Because the superficial radial sensory nerve is purely sensory, no weakness develops. A characteristic patch of altered sensation develops over the lateral dorsum of the hand, part of the thumb, and the dorsal proximal phalanges of the index, middle, and ring fingers. 

DIFFERENTIAL DIAGNOSIS The differential diagnosis of wrist drop, aside from a radial neuropathy at the spiral groove, axilla, and PIN, includes unusual presentations of C7 radiculopathy, brachial plexus lesions, and central causes (Box 24.1). Because most muscles that extend the wrist and fingers are innervated by the C7 nerve root, C7 radiculopathy may rarely present solely with a wrist drop and finger drop, with relative sparing of non-­radial C7-­innervated muscles. However, several key clinical features help differentiate a C7 radiculopathy from a radial neuropathy, PIN, brachial plexopathy, or central lesion (Table 24.1). Radial neuropathy at the spiral groove or axilla should result in weakness of the brachioradialis, a C5– C6-­innervated muscle, which should not be weak in a lesion of the C7 nerve root. On the other hand, radial neuropathy at the spiral groove and PIN should spare the triceps, which would be expected to be weak in a C7 radiculopathy. If a C7 radiculopathy is severe enough to cause muscle weakness, other non-­radial C7-­innervated muscles also should be weak (e.g., pronator teres, flexor carpi radialis), leading to weakness of arm pronation and wrist flexion. However, in rare situations, non-­radial C7-­innervated muscles may be relatively spared, making the clinical differentiation quite difficult. Although lesions of the posterior cord of the brachial plexus result in weakness of radial-­innervated muscles, the deltoid (axillary nerve) and latissimus dorsi (thoracodorsal nerve) should also be weak. Central lesions may result in a wrist drop and finger drop. The typical upper motor neuron posture results in flexion of the wrist and fingers, which in the acute phase or when the lesion is mild may superficially resemble a radial neuropathy. Central lesions are identified by increased muscle tone and deep tendon reflexes (unless acute), slowness of movement, associated findings in the lower face and leg, and altered sensation beyond the radial distribution. 

Superficial Radial Sensory Neuropathy The superficial radial sensory nerve is derived from the main radial nerve in the region of the elbow. In the distal third of the forearm, it runs subcutaneously next to the radius. Its superficial location next to bone makes it extremely susceptible to compression, a syndrome coined “Cheiralgia Paresthetica,” which translates from the Greek as cheir + algos, meaning pain in the hand. Tight-­fitting

Box 24.1  Wrist Drop: Possible Anatomic Localizations Posterior interosseous nerve Radial nerve at the spiral groove Radial nerve in the axilla Posterior cord of the brachial plexus C7 root Central nervous system

422

SECTION VIII   Clinical Disorders

ELECTROPHYSIOLOGIC EVALUATION

In the evaluation of a patient with a wrist drop, the role of nerve conduction studies and EMG is to identify a

potential radial neuropathy, assess its location and severity, and, by defining the underlying pathophysiology, establish a prognosis (Table 24.2).

Table 24.1  Clinical Differentiating Factors in Wrist Drop. Posterior Interosseous Neuropathy

Radial Nerve: Spiral Groove

Radial Nerve: Axilla

Posterior Cord

C7

Wrist drop or finger drop

X

X

X

X

X

Radial deviation on wrist extension

X

Weakness of supination (mild)

X

X

X

Weakness of elbow flexion (mild)

X

X

X

Diminished brachioradialis tendon reflex

X

X

X

Weakness of elbow extension

X

X

X

Diminished triceps tendon reflex

X

X

X

Weakness of shoulder abduction

X

Sensory loss in lateral dorsal hand

X

Sensory loss in posterior arm or forearm

X

X

X (equivocal)

X

X

X (equivocal)

Weakness of wrist flexion

X

X, May be present.

Table 24.2  Electromyographic and Nerve Conduction Abnormalities Localizing the Lesion Site in Wrist Drop. Posterior Interosseous Neuropathy

Radial Nerve: Spiral Groove

Radial Nerve: Axilla

Posterior Cord

C7

  Extensor indicis proprius

X

X

X

X

X

  Extensor digitorum communis

X

X

X

X

X

  Extensor carpi ulnaris

X

EMG Findings

X

X

X

X

  Extensor carpi radialis-­long head

X

X

X

X

 Brachioradialis

X

X

X

 Supinator

X

X

X

 Anconeus

X

X

X

 Triceps

X

X

X

 Deltoid

X

  Latissimus dorsi

X

X

  Flexor carpi radialis, pronator teres

X

  Cervical paraspinal muscles

X

Nerve Conduction Study Findings   Abnormal radial SNAP (if axonal)   Low radial CMAP (if axonal)

X

  Conduction block at spiral groove (if demyelinating)   Conduction block between forearm and elbow (if demyelinating)

X

X

X

X

X

X

X X

X, May be abnormal; CMAP, compound muscle action potential; EMG, electromyography; SNAP, sensory nerve action potential.

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Chapter 24 • Radial Neuropathy 423

Box 24.2  Recommended Nerve Conduction Study Protocol for Radial Neuropathy Routine studies: 1. Radial motor study recording extensor indicis proprius, stimulating the forearm, elbow, below spiral groove, and above spiral groove; bilateral studies 2. Ulnar motor study recording the abductor digiti minimi, stimulating the wrist, below groove, and above groove in the flexed elbow position 3. Median motor study recording the abductor pollicis brevis, stimulating the wrist and antecubital fossa 4. Median and ulnar F responses 5. Superficial radial sensory study recording over the extensor tendons to thumb, stimulating the forearm; bilateral studies 6. Ulnar sensory study recording digit 5, stimulating the wrist 7. Median sensory study recording digit 2 or 3, stimulating the wrist  The following patterns may result: • P  osterior interosseous neuropathy (axonal loss lesion): Normal superficial radial SNAP, low-­amplitude distal radial CMAP. • P  osterior interosseous neuropathy (demyelinating lesion): Normal superficial radial SNAP, normal-­amplitude distal radial CMAP with motor conduction block between the forearm and elbow. • P  osterior interosseous neuropathy (mixed axonal loss and demyelinating lesion): Normal superficial radial SNAP, low-­ amplitude distal radial CMAP with motor conduction block between the forearm and elbow. • R  adial neuropathy at the spiral groove (axonal loss lesion): Reduced superficial radial SNAP, low-­amplitude distal radial CMAP. No conduction block across the spiral groove. • R  adial neuropathy at the spiral groove (demyelinating lesion): Normal superficial radial SNAP, normal amplitude distal radial CMAP with conduction block across the spiral groove. • R  adial neuropathy at the spiral groove (mixed axonal loss and demyelinating lesion): Reduced superficial radial SNAP, low-­amplitude distal radial CMAP with conduction block across the spiral groove. • R  adial neuropathy at the axilla (axonal loss lesion): Reduced superficial radial SNAP, low-­amplitude distal radial CMAP. • R  adial neuropathy at the axilla (demyelinating lesion): Normal superficial radial SNAP, normal-­amplitude distal radial CMAP with normal motor study to above spiral groove. • S uperficial radial sensory neuropathy: Reduced superficial radial SNAP, normal radial motor study. CMAP, Compound muscle action potential; SNAP, sensory nerve action potential.

Nerve Conduction Studies The most important nerve conduction study in assessing a wrist drop is the radial motor study (Box 24.2). A radial compound muscle action potential (CMAP) can be recorded over the EIP muscle, placing the active electrode two fingerbreadths proximal to the ulnar styloid with a reference electrode placed over the ulnar styloid (Fig. 24.9). The radial nerve can be stimulated in the forearm, at the elbow (in the groove between the biceps and brachioradialis muscles), and below and above the spiral groove. The normal CMAP recorded from the EIP typically is 2–5 mV. Comparing the CMAP amplitude to that on the contralateral asymptomatic side is always important. Any axonal loss will result in a decreased distal CMAP amplitude after

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Fig. 24.9  Radial motor study.  The active electrode is placed over the extensor indicis proprius, 2 cm proximal to the ulnar styloid, with the reference electrode over the ulnar styloid. The radial nerve can be stimulated in the forearm, at the elbow, and below and above the spiral groove.

3–5 days, when wallerian degeneration for motor fibers has occurred. In fact, the best way to assess the degree of axonal loss is to compare the CMAP amplitudes between the involved side and the contralateral side. Several significant technical points must be considered when performing radial motor studies. First, placement of the active recording electrode over the EIP almost always results in a CMAP with an initial positive deflection. This occurs because volume-­conducted potentials from other nearby radial-­ innervated muscles (e.g., extensor pollicis brevis and longus) contaminate the CMAP response, resulting in an initial positive deflection. Second, it may be difficult to make accurate surface distance measurements. Because the radial nerve winds around the humerus and takes a somewhat circuitous course through the arm, surface distance measurements often are inaccurate. Measuring distance with obstetric calipers, especially between the elbow and arm, reduces some of this error. However, the combination of difficulty measuring the true nerve length and the initial positive deflection CMAP can lead to considerable potential inaccuracies in measuring true conduction velocities. Radial conduction velocities sometimes are calculated as factitiously fast (>75 m/s). The value of performing radial motor studies usually lies not in the measurement of conduction velocities but in looking for a focal conduction block between the proximal and distal sites and determining the relative CMAP amplitude to assess axonal loss (Fig. 24.10). In cases of radial neuropathy at the spiral groove, CMAPs recorded with stimulation at the forearm, elbow, and below the spiral groove can be completely normal if the lesion is purely demyelinating. However, stimulation above the spiral groove will result in electrophysiologic evidence of a conduction block, i.e., a marked decrease of amplitude and area. The relative drop in distal to proximal CMAP amplitude will give some indication of the proportion of fibers blocked. Rarely, in cases of PIN, there may be conduction block between the forearm and elbow sites. However, most cases of PIN are pure axonal loss lesions (akin to ulnar neuropathy at the elbow), and no conduction block is demonstrable.

424

SECTION VIII   Clinical Disorders

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Fig. 24.10  Radial motor studies for radial neuropathy at the spiral groove.  Left, Symptomatic arm. Right, Contralateral asymptomatic arm. Recording extensor indicis proprius and stimulating the forearm, elbow, below spiral groove, and above spiral groove. Note the marked drop in amplitude and area across the spiral groove on the left (conduction block) and the symmetric distal compound motor action potential amplitudes from side to side. Taken together, these findings imply a predominantly demyelinating lesion at the spiral groove.

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In these cases, the distal radial CMAP amplitude will be decreased in proportion to the amount of axonal loss. In contrast to radial motor studies, the superficial radial sensory nerve is easy to stimulate and record (Figs. 24.11 and 24.12). The active electrode is placed over the tendon of the extensor pollicis longus, with the reference electrode placed 3–4 cm distally. The nerve is easily stimulated 10 cm proximally over the radius. If there has been secondary axonal loss, the response will be diminished in amplitude. Similar to motor studies, it is often useful to compare the response with the contralateral asymptomatic side. If the pathology is one of pure or predominant proximal demyelination, a very interesting phenomenon occurs. Although the patient reports marked numbness in the distribution of the superficial radial sensory nerve, the superficial radial sensory nerve action potential (SNAP) will be normal, even comparing side to side. This unusual finding (a normal sensory response in the distribution of cutaneous numbness) can occur in only one

Fig. 24.12  Radial sensory nerve action potential.  The radial sensory nerve action potential is easy to record and typically has a triphasic morphology. It is expected to be normal in all posterior interosseous neuropathy lesions, as well as in other higher radial neuropathies that are purely demyelinating.

Box 24.3  Causes of Wrist Drop and a Normal Superficial Radial Sensory Nerve Action Potential Posterior interosseous neuropathy Demyelinating radial neuropathy at the spiral groove or axilla C7 radiculopathy Central nervous system lesion Hyperacute axonal loss injury of the main radial nerve (50% difference in amplitudes). This is a key piece of information because

it strongly implies that the lesion is at or distal to the dorsal root ganglion, either in the lumbar plexus or in the femoral nerve. Additional routine nerve conduction studies in the left lower extremity are performed, including tibial and peroneal motor studies and the sural sensory study, to rule out a coexistent polyneuropathy or a possible lumbosacral plexopathy. The fact that those studies are normal makes the diagnosis of plexopathy or polyneuropathy unlikely. The needle EMG examination reveals fibrillation potentials in the quadriceps muscles (specifically the vastus lateralis and vastus medialis) with decreased recruitment of normal configuration motor unit action potentials (MUAPs). Notably, the iliacus muscle is normal. Non-­ femoral lumbar-­ innervated muscles, specifically the thigh adductors (L2–L4) and the tibialis anterior (L4–L5), are normal, as are the L3 and L4 paraspinal muscles. At this point we, are ready to formulate an electrophysiologic diagnosis. IMPRESSION: There is electrophysiologic evidence of a subacute femoral neuropathy, most probably at the inguinal ligament, that is predominantly demyelinating in nature, with some secondary axonal loss. This case raises several important questions. 

How Does One Determine That the Pathology Is Predominantly Demyelinating? The lesion is predominantly demyelinating because the CMAP amplitudes are fairly symmetric from side to side, yet the patient is clearly weak. Because more than 5 days have passed, any wallerian degeneration along motor fibers that is going to occur has already taken place. Therefore, the relatively normal CMAP amplitude distal to the lesion implies that most of the axons of the femoral nerve remain intact. The predominant cause of the weakness must be demyelination of the femoral nerve at the inguinal ligament,

Chapter 26 • Femoral Neuropathy 467

which is proximal to the stimulation site (just inferior to the inguinal ligament). With demyelination, axons are blocked and weakness follows. On the needle EMG, this manifests mostly as moderately decreased recruitment of MUAPs. The MUAP configuration is normal, however, for the following reasons: (1) the lesion is predominantly demyelinating, and (2) not enough time has transpired for reinnervation to occur. Note that there are fibrillation potentials in the vastus lateralis and vastus medialis. Most demyelinating lesions result in some secondary axonal loss. Axonal loss is also indicated by the low saphenous sensory potential. The best way to quantitate axonal loss of motor fibers, however, is not by the degree of fibrillation activity but by the amplitude of the CMAP. In this case, the CMAP amplitude on the symptomatic side is approximately 85% that on the asymptomatic side, indicating roughly 15% loss of axons. This is only an estimate, however; this degree of side-­to-­side asymmetry may well fall within the normal range. 

Is the EMG Helpful in Determining the Etiology and Prognosis of the Femoral Neuropathy? The nerve conduction studies and EMG clearly demonstrate a postganglionic lesion of the femoral nerve, most likely at the inguinal ligament. The preserved hip flexion strength correlates with the normal EMG examination of the iliacus. This finding is important in excluding a lesion

proximal to the inguinal ligament. By suggesting that the lesion is at the inguinal ligament, the EMG is helpful in determining that the most likely etiology of the neuropathy is compression of the femoral nerve that occurred while the patient was in the lithotomy position during surgery. The EMG also is very helpful in assessing the prognosis. Because the CMAP amplitude is relatively intact and the likely pathophysiology is one of demyelination, the prognosis for recovery is quite good. Remyelination in such cases usually occurs over several weeks. Therefore, the duration of the patient’s disability will likely be short. Remyelination undoubtedly will occur over the next several weeks to months, accompanied by the return of full strength

Suggested Readings Al-­Ajmi A, Rousseff RT, Khuraibet AJ. Iatrogenic femoral neuropathy: two cases and literature update. J Clin Neuromusc Dis. 2010;12:66–75. Al Hakim M, Katirji MB. Femoral mononeuropathy induced by the lithotomy position: a report of 5 cases and a review of the literature. Muscle Nerve. 1993;16:891. Dawson DM, Hallet M, Wilbourn AJ. Entrapment Neuropathies. 3rd ed. Philadelphia: Lippincott Raven; 1999. Sharma KR, Cross J, Santiago F, et al. Incidence of acute femoral neuropathy following renal transplantation. Arch Neurol. 2002;59:541–545.

SECTION VIII • Clinical Disorders PART I • Common Mononeuropathies

27

Tarsal Tunnel Syndrome

Patients with pain and numbness in the foot often are referred to the electromyography (EMG) laboratory for evaluation of possible tarsal tunnel syndrome (TTS). TTS results from entrapment of the distal tibial nerve under the flexor retinaculum at the medial ankle. Superficially, it might seem that tibial nerve entrapment under the flexor retinaculum at the ankle would be analogous to median nerve entrapment under the flexor retinaculum at the wrist (i.e., carpal tunnel syndrome [CTS]). However, in contrast to CTS, which is very common, TTS is exceptionally rare. Although electrophysiology can be useful in demonstrating focal slowing at the tarsal tunnel in those rare cases of true TTS, every electromyographer should be aware that significant technical difficulties are often encountered when studying the distal tibial nerve and the muscles it innervates, especially in older patients. As discussed later in this chapter, neuromuscular ultrasound can be very helpful in cases of suspected tibial neuropathy at the tarsal tunnel, especially in cases of trauma or unusual structural lesions.

ANATOMY As the tibial nerve descends distal to the medial malleolus, it runs beneath the flexor retinaculum on the medial side of the ankle, through the tarsal tunnel (Fig. 27.1). The tarsal tunnel is a fibro-­osseous tunnel below the medial malleolus with a bony floor and a roof formed by the flexor retinaculum. In addition to the tibial nerve, the tibial artery, the tibial veins and tendons of the flexor hallucis longus (FHL), flexor digitorum longus, and tibialis posterior pass through the tarsal tunnel. The distal tibial nerve typically divides into three branches. One branch, the medial calcaneal sensory nerve, is purely sensory and provides sensation to the heel of the sole (Fig. 27.2). The other two branches, the medial and lateral plantar nerves, contain both motor and sensory fibers that supply the medial and lateral sole of the foot, respectively. Typically, the medial plantar nerve supplies the first three and a half toes (including the great toe), whereas the lateral plantar nerve supplies the little toe and the lateral fourth toe. The first branch of the lateral plantar nerve is the inferior calcaneal nerve (a.k.a., Baxter’s nerve). Both plantar nerves innervate the intrinsic muscles of the foot. The muscles that are most accessible to study using needle EMG are the abductor hallucis brevis (AHB), flexor hallucis brevis (FHB), and flexor digitorum brevis (FDB) for the medial plantar nerve and the abductor digiti quinti

468

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pedis (ADQP) for the lateral plantar nerve via the inferior calcaneal nerve. 

CLINICAL The most frequent symptom in patients with TTS is perimalleolar pain. Ankle and sole pain often is described as burning and often is worse with weight bearing or at night. Paresthesias and sensory loss involving the sole of the foot may occur due to compression of the plantar or calcaneal nerves (Fig. 27.3). There are few other reliable clinical signs. Intrinsic foot muscle atrophy may occur but is not specific to TTS. For example, atrophy of intrinsic foot muscles may occur in L5–S1 radiculopathy, proximal tibial neuropathy, or polyneuropathy. It is extremely difficult to assess strength of the intrinsic foot musculature, because most of the important toe and ankle functions are subserved by the long extensors and flexors in the lower leg, which are innervated by the proximal peroneal and tibial nerves. Finally, many consider a Tinel’s sign over the tarsal tunnel to be suggestive of TTS. Unfortunately, like Tinel’s

Chapter 27 • Tarsal Tunnel Syndrome 469

signs elsewhere, this is a nonspecific sign and may occur in some normal subjects. Significantly, the ankle tendon reflex, which is mediated by the tibial nerve proximal to the tarsal tunnel, is normal in TTS, as is sensation over the lateral foot (sural nerve) and the dorsum of the foot (superficial peroneal nerve). 

ETIOLOGY The incidence of TTS is widely debated. Some podiatrists believe that TTS is rather common, whereas most neurologists, physiatrists, and electrophysiologists believe that it is quite rare. Lesions of the medial and lateral plantar nerves most often occur as a result of trauma (including sprain and fracture) or occasionally from degenerative bone or 0HGLDOSODQWDU EUDQFK /DWHUDOSODQWDU EUDQFK

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DIFFERENTIAL DIAGNOSIS The differential diagnosis of TTS includes local orthopedic problems of the foot (especially tendonitis and fasciitis), proximal tibial neuropathy, and, especially early on, mild polyneuropathy. S1 radiculopathy or lumbosacral plexopathy may cause sensory loss over the sole, but neither is typically associated with local foot pain. It is not unusual for patients who first present with polyneuropathy to be misdiagnosed with TTS. Most patients studied in our laboratory referred for possible TTS have either a normal electrophysiologic examination (and may have had a local orthopedic problem) or are found to have a mild distal polyneuropathy. 

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Fig. 27.2  Tibial sensory innervation of the foot.  The distal tibial nerve supplies sensation to the sole of the foot via the medial plantar, lateral plantar, and calcaneal sensory nerves. (Adapted from Omer GE, Spinner M. Management of Peripheral Nerve Problems. Philadelphia, PA; WB Saunders; 1980.)

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connective tissue disorders. Rare cases of TTS are caused by varicosities or other unusual mass lesions (e.g., lipomas, ganglions, cysts, exostoses, varices). TTS caused by hypertrophy of the flexor retinaculum from repetitive use (akin to CTS) is unusual. One or more of the three nerve branches (medial calcaneal, medial plantar, and lateral plantar) may be involved. 

Evaluation of suspected TTS is greatly simplified if one side is symptomatic and the other side is normal. This situation allows for side-­to-­side comparison studies (Box 27.1). The important nerve conduction studies to perform include bilateral tibial distal motor latencies to both the AHB and ADQP, for the medial and lateral plantar nerves, respectively, stimulating the tibial nerve proximal to the tarsal tunnel at the medial malleolus (Fig. 27.4). Compound muscle action potential (CMAP) amplitudes and distal latencies are compared from side to side. Theoretically, if there is demyelination across the tarsal tunnel, the distal latencies on the involved side should be markedly

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Fig. 27.3  Sensory loss in tarsal tunnel syndrome.  (A) The first case of tarsal tunnel syndrome was reported by Captain Keck in an army recruit who developed pain in the feet and anesthesia in the distribution of the distal tibial nerve. (B) Black shading indicates areas of anesthesia from the original case report. (From Keck C. The tarsal tunnel syndrome. J Bone Joint Surg. 1962;44:180.)

470

SECTION VIII   Clinical Disorders

Box 27.1  Recommended Nerve Conduction Study Protocol for Tarsal Tunnel Syndrome Routine studies: 1. Distal tibial motor (medial and lateral plantar) studies, stimulating tibial nerve at medial malleolus and recording abductor hallucis brevis (medial plantar) and abductor digiti quinti pedis (lateral plantar). Comparison with contralateral side is required. 2. Routine tibial motor study, recording abductor hallucis brevis, stimulating medial ankle and popliteal fossa 3. Routine peroneal motor study, recording extensor digitorum brevis, and stimulating the ankle, below fibular neck, and lateral popliteal fossa 4. Medial and lateral plantar mixed or sensory studies (plantar mixed and sensory responses usually require averaging several potentials). For mixed studies, stimulate medial sole and record medial ankle (medial plantar mixed); stimulate the lateral sole and record medial ankle (lateral plantar mixed). For sensory studies, stimulate the great toe and record medial ankle (medial plantar sensory); stimulate the little toe and record medial ankle (lateral plantar sensory). Comparison with the contralateral side is required, using identical distances between the stimulating and recording sites. 5. Sural sensory response, stimulating posterior calf, recording the posterior ankle 6. Tibial and peroneal F responses 7. H reflexes, bilateral studies (may be abnormal in S1 radiculopathy or polyneuropathy but not in tarsal tunnel syndrome)

prolonged. In axonal loss lesions, the CMAP amplitudes will be reduced, and the latencies will be normal or only slightly prolonged. Surface sensory and mixed nerve studies are difficult to perform, even in normal healthy subjects, but they increase the sensitivity of making the electrodiagnosis of TTS. Orthodromic surface sensory studies can be performed stimulating the great and little toes (medial and lateral plantar sensory nerves, respectively) and recording over the tibial nerve at the medial ankle proximal to the tarsal tunnel. The potentials are usually extremely small in amplitude, making it necessary to average many potentials. Antidromic surface sensory studies also can be performed, but they have similar technical limitations. Surface recording of the mixed plantar nerves is slightly easier (Fig. 27.5). Both the medial and lateral plantar mixed nerves can be stimulated in the sole, recording over the tibial nerve at the medial ankle, proximal to the tarsal tunnel. Averaging is still required to measure these small potentials, and in older individuals, they may be absent. Often, medial and lateral plantar sensory and mixed nerve potentials are unobtainable even in normal subjects. Consequently, an absent or low-­amplitude potential should not be considered abnormal unless a clear side-­ to-­ side difference is found using identical distances between the stimulating and recording sites. No diagnostic significance should be attributed to bilaterally absent plantar mixed or sensory nerve responses, especially in middle-­aged or older individuals. It is important to emphasize that the plantar

A

B Fig. 27.4  Distal tibial motor studies.  The medial and lateral plantar distal motor latencies can be measured by recording the abductor hallucis brevis (A) and abductor digiti quinti pedis (B), respectively, and by stimulating the tibial nerve behind the medial malleolus.

mixed and sensory nerves are the most distal nerves in the lower extremities. As such, their conduction velocities normally are slower than those of more proximal nerves and are more susceptible to the effects of temperature and cooling. In addition to bilateral plantar motor, sensory, and mixed nerve studies, further nerve conductions should be performed routinely, especially to exclude a polyneuropathy. Routine peroneal and tibial motor studies and their respective F responses should be obtained along with the sural sensory response. If the sural sensory response is abnormal, any abnormalities in the plantar nerves are likely secondary to either a polyneuropathy or, less often, a sciatic or lumbosacral plexus lesion. In some situations, assessment of bilateral H reflexes can yield useful information. H reflexes are normal in TTS but may be abnormal in polyneuropathy, proximal tibial neuropathy, sciatic and lumbosacral plexus lesions, and S1 radiculopathy, all of which clinically may cause sensory abnormalities over the sole of the foot. 

Electromyographic Approach EMG often is quite problematic in the assessment of TTS (Box 27.2). An EMG study of the intrinsic foot muscles is fraught with problems. First is the limited ability of patients to tolerate the examination. The sole is quite sensitive,

Chapter 27 • Tarsal Tunnel Syndrome 471 Fig. 27.5  Medial and lateral plantar mixed nerve responses: value of comparing symptomatic side to asymptomatic contralateral side.  The medial and lateral soles are stimulated while recording over the tibial nerve at the medial ankle. Sensory and mixed nerve potentials are very low in amplitude and must be averaged to be discerned from background noise. Although the right medial plantar mixed nerve potential is two to three times lower in amplitude than the left, the absolute difference is only 2–3 μV. However, the right medial and lateral plantar mixed nerve potentials are significantly prolonged in comparison with the left, demonstrating that the right side is abnormal.

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Box 27.2  Recommended Electromyographic Protocol for Tarsal Tunnel Syndrome Routine muscles: 1. Abductor hallucis brevis and abductor digiti quinti pedis (must be compared with the contralateral side) 2. At least two distal tibial-­innervated muscles proximal to the tarsal tunnel (e.g., medial gastrocnemius, soleus, tibialis posterior, flexor digitorum longus) 3. At least one distal peroneal-­innervated muscle in the lower leg (tibialis anterior, extensor hallucis longus)  Special considerations: • If any muscle proximal to the tarsal tunnel is abnormal, additional muscles must be sampled to determine whether the lesion represents a more proximal tibial or sciatic neuropathy, lumbosacral plexopathy, radiculopathy, or polyneuropathy. • From a practical point of view, it is nearly impossible to diagnose tarsal tunnel syndrome in the presence of a polyneuropathy. • Examination of intrinsic foot muscles often is painful for patients and these muscles are difficult to activate. Increased insertional activity and occasionally fibrillation potentials associated with large, long-­duration motor unit action potentials are frequently found in normal subjects without symptoms. Interpreting the electromyographic findings in an intrinsic foot muscle as abnormal requires that (1) the abnormalities be fairly marked or (2) the contralateral asymptomatic muscle is distinctly different on EMG from the symptomatic side.

and placement of the EMG needle into the intrinsic foot muscles is painful for most patients. Second, activating these muscles is difficult; therefore, it frequently is difficult to assess a sufficient number of motor unit action potentials (MUAPs). Third, it may be theoretically hazardous to puncture the skin of the foot in a patient who is insensate and/ or has vascular insufficiency in the lower extremities. This is most common in patients with diabetes who need meticulous foot care to prevent any injury to the sole of the foot, which

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can lead to a serious infection of the foot and potential loss of limb (see Chapter 43). Finally, the interpretation of what is normal may be difficult. Intrinsic foot muscles commonly show increased insertional activity and occasionally fibrillation potentials associated with large, long-­duration MUAPs, as one would expect in a neurogenic lesion. Such findings are not unusual in normal subjects without symptoms, however, and are thought to be due to everyday wear and tear on the feet. Therefore, interpretation of these abnormalities is problematic. Interpreting the EMG findings in an intrinsic foot muscle as abnormal requires that (1) the abnormalities be fairly marked or (2) the contralateral asymptomatic muscle is distinctly different on EMG from the symptomatic side. In addition to the plantar-­innervated intrinsic foot muscles (AHB, FHB, and ADQP), tibial-­and peroneal-­innervated muscles in the lower leg should be sampled to exclude a more proximal lesion or polyneuropathy. If abnormalities are found in these muscles, a more extensive evaluation should be performed to sort out whether the changes are due to a proximal tibial neuropathy, sciatic neuropathy, lumbosacral plexopathy, radiculopathy, or polyneuropathy. 

ULTRASOUND CORRELATIONS Neuromuscular ultrasound can be very useful in cases of suspected tibial neuropathy at the tarsal tunnel for several reasons. First, as noted earlier, the EDX diagnosis of TTS is very challenging due to the fact that (1) responses from the medial and lateral plantar sensory and mixed nerve studies are difficult to obtain or may be absent in older individuals and (2) needle EMG “abnormalities” in intrinsic foot muscles are often seen in asymptomatic patients. In addition, true TTS is quite rare, but when it does occur, it usually results from trauma or unusual structural lesions. In these clinical situations, ultrasound is especially helpful. Lastly, ultrasound may aid in the diagnosis of other orthopedic causes of foot pain, especially plantar fasciitis, which can sometimes be mistaken for TTS.

472

SECTION VIII   Clinical Disorders







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Fig. 27.6  Tibial nerve at the tarsal tunnel.  Top, Native images. Bottom, Same images with the nerves in yellow, posterior tibial artery in bright red; posterior tibial veins in blue, outline of the medial malleolus in green, tendons in purple, and FHL muscle in dark red. Left, Proximal tarsal tunnel. Right, Distal tarsal tunnel. Note the larger TP tendon compared with the FDL; the neurovascular bundle consisting of the posterior tibial artery, two veins and the tibial nerve; and the ill-­defined FHL muscle, which is deep. Distally in the tarsal tunnel, the nerve divides into the larger medial plantar and smaller lateral plantar nerves. FDL, Flexor digitorum longus; FHL, flexor hallucis longus; LP, lateral plantar; MP, medial plantar; TN, tibial nerve; TP, tibialis posterior.

To visualize the tibial nerve at the ankle, the patient is asked to lie supine on the bed with their legs slightly externally rotated. This position allows for easy comparison from side to side. The probe is placed with one end over the medial malleolus and the other distally over the calcaneus. The large tendon of the tibialis posterior lies adjacent to the medial malleolus superiorly, with the smaller tendon of the flexor digitorum longus below. Both normally show prominent anisotropy. Adjacent to these two tendons is the neurovascular bundle, which typically consists of the posterior tibial artery, two veins, and the tibial nerve (Fig. 27.6). Color or power Doppler allows easy differentiation of the artery from the veins (Fig. 27.7). Lastly, below the neurovascular bundle are the muscle and tendon of the FHL. As the FHL is quite deep at this location, and it is more muscular than tendon, it may be more difficult to clearly see. Passive or active motion of the great toe will help identify its location. The tibial nerve is usually quite hyperechoic and easily visualized at the tarsal tunnel. As the nerve is followed distally toward the sole, it can commonly be seen dividing into the medial and lateral plantar nerves. In some individuals, the bifurcation

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Fig. 27.7  Blood vessels in the tarsal tunnel.  Top, Native image. Bottom, Same image with color Doppler applied. Note the common pattern of the posterior tibial artery flanked by two veins adjacent to the tibial nerve. FDL, Flexor digitorum longus muscle; TN, tibial nerve; TP, tibialis posterior muscle.

Chapter 27 • Tarsal Tunnel Syndrome 473

Fig. 27.8  Ganglion cyst in the tarsal tunnel.  Top, Native images. Bottom, Same images with the tibial nerve in yellow, ganglion cyst in green, and posterior acoustic enhancement designated by the red arrows. Left, Short axis. Right, Long axis. Note the large anechoic ganglion cyst located just above the tibial nerve, presumably exerting pressure on the distal tibial distal nerve. Ultrasound is very helpful in assessing for structural causes of tibial nerve entrapment at the tarsal tunnel.

occurs in the tarsal tunnel; in others, it can occur above the entrance to the tarsal tunnel. It is important to visualize the nerve in both short and long axis. Following the nerve in long axis is often easier than short axis. When inspecting the tibial nerve, one assesses the cross-­sectional area, echogenicity, and fascicular structure, similar to other entrapment neuropathies. However, it is especially important to look for nearby structural abnormalities, including ganglion cysts, bone spurs, and dilated veins (varices) (Figs. 27.8 and 27.9). Lastly, if a patient has foot pain, especially with a “burning” feeling in

the sole, the plantar fascia should be assessed. The probe is put in long axis with one end over the medial calcaneus and the other end in the mid-­sole. The plantar fascia can be easily seen running over and inserting on the medial calcaneus (Fig. 27.10). The thickness of the fascia is measured and the echogenicity assessed. The central fascia of the sole can then be followed both in long and short axis throughout the sole to the level of the metatarsal heads. Plantar fascia thickness >4.6 mm, especially when associated with hypoechogenicity, is indicative of plantar fasciitis (Fig. 27.11).

474

SECTION VIII   Clinical Disorders

Fig. 27.9  Varix at the tarsal tunnel.  Top, Native images. Bottom, Same images with the tibial nerve in yellow and varix in blue. Left, Short axis view of the tibial nerve on the asymptomatic side. Middle, Short axis view of the tibial nerve on the symptomatic side. Right, Long axis view of the tibial nerve on the symptomatic side. On the symptomatic side, note the marked enlargement of the tibial nerve. In long axis, there is a large venous structure immediately adjacent to the enlarged tibial nerve. This is best demonstrated with long axis imaging. On short axis (middle image), the varix is not obvious. Looking at the vein in long axis, note the area on the far left—this is the normal size of the vein. The remainder of the vein is enlarged. A single enlarged vein is known as a varix, which rarely can result in compression of the nearby tibial nerve. Lastly, note the bulbous outpouching of the vein. Although this outpouching is enlarged, these outpouchings are normal areas where the valves are located within the vein.

Fig. 27.10  Plantar fascia.  Top, Native image (long axis; left is toward the heel). Bottom, Same images with the plantar fascia in purple and the medial calcaneus in green. The optimal location to assess for plantar fasciitis is where it inserts onto the medial calcaneus (white double-arrow). In this case, the plantar fascia is normal and measures 2.8 mm in depth (normal 50% difference from side to side, comparing right to left). In addition, the latencies are somewhat prolonged on the right side compared with the left. The degree of prolongation is not in the unequivocally demyelinating range and may be consistent with axonal loss and dropout of the fastest-­conducting fibers. When the nerve conduction studies are completed, there is strong evidence for a lesion affecting the distal tibial nerve and involving the medial and lateral plantar nerves. Polyneuropathy seems less likely, given the intact and robust sural and superficial peroneal sensory

Chapter 27 • Tarsal Tunnel Syndrome 477

responses and the asymmetry of the plantar mixed nerve studies from side to side. However, the reduced amplitude of the medial and lateral plantar mixed nerve responses and the borderline prolonged latencies are well within the range that would indicate axonal loss. Thus, there still is the possibility of a proximal tibial neuropathy in the calf. However, the fact that the sural sensory response is normal, which is derived proximally from the tibial and peroneal nerves in the popliteal fossa, argues against a proximal lesion of the tibial nerve. The needle EMG examination should be useful in helping to localize the lesion; particular attention should be paid to tibial muscles in the calf above the level of the tarsal tunnel. Moving on to the needle EMG findings, fibrillation potentials are present in the right AHB muscle. There is poor activation of MUAPs, which is not unusual even in normal subjects. The few MUAPs seen appear to be of slightly increased duration and amplitude. These findings usually are associated with neuropathic lesions. However, one must always be cautious in assessing the intrinsic foot muscles. Normal subjects without any complaints may have mild active denervation or reinnervation (or both) in the intrinsic foot muscles. Indeed, when the contralateral AHB muscle is checked, there are also sparse fibrillation potentials with borderline large and long MUAPs. Therefore, although we might have initially interpreted the right AHB as abnormal, after examining the contralateral side, we determine that the findings on the right side are of dubious significance. A similar lack of asymmetry is seen in the ADQP muscles; both sides are slightly abnormal. Next, two tibial-­innervated muscles that arise above the tarsal tunnel are sampled (the medial gastrocnemius and the tibialis posterior), and both are entirely normal. Finally, the tibialis anterior muscle is sampled. This is a peroneal-­innervated muscle, and it is completely normal. At this time, we are ready to formulate our electrophysiologic impression. IMPRESSION: The electrophysiologic findings are consistent with a distal tibial neuropathy affecting the medial and lateral plantar nerves. An important question should be addressed at this point.

How Does One Localize the Lesion to the Plantar Nerves? The electrophysiologic abnormalities are limited to the distal tibial nerve, that is, the medial and lateral plantar nerves. Both plantar mixed nerve responses are low compared

with the contralateral side, with mild prolongation of peak latency. This type of abnormality can be seen in TTS, but it can also be seen in proximal tibial neuropathy, sciatic neuropathy, or lumbosacral plexopathy. The clinical findings of intact sensation over the lateral and dorsal foot also argue strongly against a polyneuropathy, sciatic neuropathy, or lumbosacral plexopathy. These findings are later substantiated on the nerve conduction studies, which show normal sural and superficial peroneal sensory responses. In addition, the fact that the EMG study does not demonstrate any abnormality of peroneal-­or tibial-­innervated muscles proximal to the tarsal tunnel argues against a lesion of the proximal tibial nerve, sciatic nerve, or lumbosacral plexus. Note that the asymmetric abnormalities in the mixed nerve responses seen in this case would not be expected in a sacral radiculopathy, because sensory potentials (which make up the majority of mixed nerve potentials) are spared in lesions proximal to the dorsal root ganglion. Therefore, although the electrophysiology fails to definitively localize the lesion, the weight of the evidence favors a lesion of the distal tibial nerve at the ankle (medial and lateral plantar nerves), especially considering the site of the trauma and the site of the persistent pain.

Suggested Readings Almeida DF, Scremin L, Zuniga SF, et al. Focal conduction block in a case of tarsal tunnel syndrome. Muscle Nerve. 2010;42:452–455. Cimino WR. Tarsal tunnel syndrome: review of the literature. Foot Ankle. 1990;11:47. Dawson DM, Hallett M, Millender LH. Entrapment Neuropathies. 2nd ed. Boston: Little, Brown; 1990. Felsenthal G, Butler DH, Shear MS. Across tarsal tunnel motor nerve conduction technique. Arch Phys Med Rehabil. 1992;73:64–69. Keck C. The tarsal tunnel syndrome. J Bone Joint Surg. 1962;44:180. Oh SJ, Arnold TW, Park KH, et al. Electrophysiological improvement in tarsal tunnel syndrome following decompression surgery. Muscle Nerve. 1991;14:407. Oh SJ, Meyer RD. Entrapment neuropathies of the tibial (posterior tibial) nerve. Neurol Clin. 1999;17:593–615. Oh SJ, Sarala PK, Kuba T, et al. Tarsal tunnel syndrome: electrophysiological study. Ann Neurol. 1979;5:327. Patel AT, Gaines K, Malamut R, et al. Usefulness of electrodiagnostic techniques in the evaluation of suspected tarsal tunnel syndrome: an evidence-­based review. Muscle Nerve. 2005;32:236–240. Samarawickrama D, Therimadasamy AK, Chan YC, Vijayan J, Wilder-­Smith EP. Nerve ultrasound in electrophysiologically verified tarsal tunnel syndrome. Muscle Nerve. 2016;53(6):906–912.

SECTION VIII • Clinical Disorders PART I • Common Mononeuropathies

28

Facial and Trigeminal Neuropathy

Although nerve conduction and electromyography (EMG) studies are used most often to evaluate peripheral nerve and muscle disorders, they can also be used to evaluate lesions of the cranial nerves. Outside of the brainstem, the cranial nerves, other than cranial nerves I (olfactory) and II (optic), are essentially the same as peripheral nerves, carrying motor, sensory, and autonomic fibers. Mononeuropathies affecting cranial nerves VII (facial) and V (trigeminal) are the most common cranial nerve lesions evaluated in the EMG laboratory. The facial nerve can be directly stimulated and recorded using standard nerve conduction techniques. The blink reflex can be used to evaluate both the facial and trigeminal nerves. Facial and masticatory muscles, supplied by cranial nerves VII and V, respectively, can easily be examined with an EMG needle. As in other neuromuscular disorders, the electrophysiologic evaluation of facial and trigeminal neuropathies is used to confirm localization of the lesion, assess the underlying pathophysiology and severity of the lesion, and offer a prognosis. In fact, assessment of severity and prognosis are often the key issues addressed by the electromyographer in the most common cranial neuropathy of all, idiopathic facial palsy (i.e., Bell’s palsy).

ANATOMY Facial Nerve The facial nerve, cranial nerve VII, is a complex nerve that carries several different fiber bundles, including the following:    • Motor fibers to all muscles of facial expression, as well as to the posterior belly of the digastric, stapedius, and stylohyoid muscles • Parasympathetic motor fibers supplying the mucosa of the soft palate and the salivary and lacrimal glands • Taste fibers to the anterior two-­thirds of the tongue • Parasympathetic sensory fibers for visceral sensation from the salivary glands and the nasal and pharyngeal mucosa • Somatic sensory fibers supplying a small part of the external auditory meatus and skin of the ear • Proprioceptive sensory afferents from facial muscles    478

The facial nerve is formed by the conjoining of the facial motor root and the adjacent nervus intermedius. The facial motor root supplies the muscles of facial expression and arises from the facial motor nucleus located in the ventral lateral tegmentum of the lower pons. The nervus intermedius carries taste, sensory, and parasympathetic fibers and arises from the solitary nucleus/tract (medulla), trigeminal sensory nuclei (medulla-­pons), and superior salivatory nucleus (pons), respectively. The facial nerve, including the motor root and nervus intermedius, emerges from the brainstem at the cerebellopontine angle and enters the internal auditory meatus, next passing through the geniculate ganglion before traversing the facial canal. Within the bony facial canal, several branches arise from and leave the main facial nerve (Fig. 28.1). First, parasympathetic fibers are given off to the greater and lesser petrosal nerves, bound for the pterygopalatine and otic ganglia. A small motor branch arises next, to innervate the stapedius muscle in the inner ear. The chorda tympani then arises to carry taste fibers to the anterior two-­thirds of the tongue and parasympathetic fibers to the submandibular and sublingual salivary glands. The facial nerve exits the skull at the stylomastoid foramen before coursing through the parotid gland. After the stylomastoid foramen, the nerve supplies the stylohyoid and the posterior belly of the digastric muscles, then gives off a cutaneous posterior auricular branch before dividing into its five major peripheral branches: temporal (a.k.a., frontal), zygomatic, buccal, mandibular, and cervical branches, which innervate the muscles of facial expression (Fig. 28.2). 

Trigeminal Nerve The trigeminal nerve, cranial nerve V, carries sensory fibers to the face and motor fibers to the muscles of mastication. It arises from several different nuclei in the brainstem, including one motor nucleus (mid-­upper pons) and three separate sensory nuclei. The sensory nuclei include the main sensory nucleus (mid-­upper pons), which mediates light touch; the nucleus of the spinal tract of V (pons to upper cervical cord), which mediates pain and temperature; and the mesencephalic nucleus of V (lower midbrain), which mediates proprioception from facial muscles. Exiting from the lateral mid-­pons, the nerve is called trigeminal because it branches into three major peripheral nerves

Chapter 28 • Facial and Trigeminal Neuropathy 479

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Fig. 28.1  Course of the facial motor root and nervus intermedius branches of the facial nerve in the facial canal.  The facial nerve is formed by the merging of the facial motor root and the adjacent nervus intermedius. The motor root supplies the muscles of facial expression. The nervus intermedius carries taste, sensory, and parasympathetic fibers. Within the bony facial canal, several branches arise from and leave the main facial nerve. Parasympathetic fibers are given off to the greater and lesser petrosal nerves, bound for the pterygopalatine and otic ganglia. A small motor branch arises next to innervate the stapedius muscle in the inner ear. The chorda tympani then arises to carry taste fibers to the anterior two-­thirds of the tongue and parasympathetic fibers to the submandibular and sublingual salivary glands. The blue arrow indicates where fibers from the lingual nerve, a branch of V3, join the chorda tympani fibers.

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Fig. 28.2  Major peripheral branches of the facial nerve.  After exiting the stylomastoid foramen, the facial nerve bifurcates into five major peripheral branches: temporal, zygomatic, buccal, mandibular, and cervical to supply the muscles of facial expression. (With permission from Oh SJ. Clinical Electromyography: Nerve Conduction Studies. 2nd ed. Baltimore, MD: Williams & Wilkins; 1993.)

SECTION VIII   Clinical Disorders

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Fig. 28.3  Trigeminal ganglion and origin of the three major peripheral nerve branches.  Exiting from the lateral mid-­pons, the trigeminal nerve divides into three major peripheral nerves—ophthalmic (V1), maxillary (V2), and mandibular (V3)—which arise from the trigeminal ganglion, located just outside the brainstem on the petrous bone in the middle cranial fossa. (Adapted with permission from Montgomery EB, Wall M, Henderson VW. Principles of Neurologic Diagnosis. Boston, MA: Little, Brown; 1986.)

that arise from the trigeminal ganglion (also known as the semilunar or gasserian ganglion), located just outside the brainstem on the petrous bone in the middle cranial fossa (Fig. 28.3). The cavity formed by the folds of dura that contain the trigeminal ganglion, surrounded by cerebrospinal fluid, is known as Meckel’s Cave. Whereas the trigeminal ganglion contains cell bodies of the sensory fibers from both the main sensory nucleus and the nucleus of the spinal tract of V, the cell bodies of proprioceptive sensory fibers from muscle spindles of trigeminal motor fibers are contained within the mesencephalic nucleus of V in the midbrain. The three major peripheral nerve divisions of the trigeminal nerve are the ophthalmic (V 1), maxillary (V2), and mandibular (V3) nerves. Each nerve exits the skull through a distinct opening: (1) the ophthalmic nerve through the superior orbital fissure, (2) the maxillary nerve through the foramen rotundum, and (3) the mandibular nerve through the foramen ovale. Each of the three major nerve branches contains sensory fibers, whereas motor fibers are carried solely in the mandibular nerve branches that supply innervation to the muscles of mastication (masseter, temporalis, medial, and lateral pterygoid muscles) and to the anterior belly of the digastric muscle, the mylohyoid, tensor veli palatini, and tensor tympani muscles. Branches of the trigeminal nerve supply light touch, pain, and temperature sensation to the skin of the face, the anterior half of the scalp, most of the oral and nasal mucosa, the anterior two-

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Fig. 28.4  Trigeminal sensory distribution.  The three branches of the trigeminal nerve—ophthalmic nerve (V1), maxillary nerve (V2), and mandibular nerve (V3)—supply sensation to the face and anterior scalp. (Adapted with permission from Haymaker W, Woodhall B. Peripheral Nerve Injuries. Philadelphia, PA: WB Saunders; 1953.)

t­ hirds of the tongue, and the dura mater of the anterior and middle cranial fossae (Fig. 28.4). 

CLINICAL Facial Neuropathy The most common cranial mononeuropathy is facial nerve palsy, which usually presents as idiopathic Bell’s palsy. Some cases are postinfectious, although a growing amount of evidence suggests that Bell’s palsy is a viral-­induced cranial neuritis caused by herpes simplex virus-­1 in many cases. In addition, the risk of Bell’s palsy is increased in patients with hypertension or diabetes and in pregnant women (the latter especially late in the pregnancy or in the early postpartum period). Unilateral facial nerve dysfunction can also be seen in association with several disorders, most commonly in the setting of diabetes. In addition, facial palsy occurs with herpes zoster involving the geniculate ganglion (Ramsay Hunt syndrome), lymphoma, leprosy, cerebellopontine angle tumors such as acoustic neuroma, multiple sclerosis, stroke, and a host of other disorders (Box 28.1). Bilateral facial weakness is less common; it may be seen in Guillain-­B arré syndrome, Lyme disease, sarcoid, Melkersson-­ Rosenthal syndrome, tuberculous meningitis, and leptomeningeal lymphomatosis/carcinomatosis. Bifacial weakness also is noted in some neuromuscular junction disorders and in various muscular dystrophies.

Chapter 28 • Facial and Trigeminal Neuropathy 481 Box 28.1  Differential Diagnosis of Facial Weakness Idiopathic Bell’s palsy Associated with systemic disorders Guillain-­Barré syndromea Lyme diseasea Diabetes Herpes zoster (Ramsay Hunt syndrome) Vasculitis Infiltrative lesions Lymphoma Leptomeningeal lymphomatosis/carcinomatosisa Tuberculous meningitisa Leprosy Sarcoida Melkersson-­Rosenthal syndromea Multiple sclerosis Associated with tumors Cerebellopontine angle tumor Nasopharyngeal carcinoma Associated with neuromuscular junction disorders Myasthenia gravisa Lambert-­Eaton myasthenic syndromea Muscular dystrophies Facioscapulohumeral dystrophya Oculopharyngeal dystrophya Myotonic dystrophya Stroke aOften

bilateral involvement.

The clinical presentation of facial nerve palsy depends on the location, pathophysiology, and severity of the lesion. A central lesion (proximal to the facial nerve nuclei) causes contralateral weakness primarily of the lower facial musculature, with relative sparing of the orbicularis oculi and frontalis muscles, which are bilaterally innervated. Furthermore, with central lesions, there may be facial movement during laughing or crying because the pathways that mediate responses to emotional stimuli are different from those that mediate voluntary facial movement. Peripheral lesions (at or distal to the facial nerve nuclei) cause ipsilateral facial paralysis that affects both the upper and lower facial musculature, resulting in an inability to wrinkle the forehead, close the eye, or smile. In addition, there may be dysfunction or absent taste sensation over the anterior two-thirds of the tongue, depending on which branches are involved as the nerve courses through the facial canal. In patients with idiopathic Bell’s palsy, complete facial paralysis involving the upper and lower face generally occurs within 24 hours and inevitably is accompanied by pain behind the ipsilateral ear. The etiology is thought to be inflammation of the facial nerve, which causes swelling and compression of the nerve in the facial canal. In most patients, the prognosis is excellent, with full recovery of function over several weeks to months. However, in more severe cases, usually those associated with significant axonal loss, some permanent facial weakness remains, or aberrant reinnervation may occur as the nerve regenerates. Aberrant reinnervation can take one of two forms: (1) an axon that previously innervated a particular

muscle grows down a different fascicle and innervates a different muscle than the original one, or (2) a single axon branches into two or more axons that go to two or more different muscles. Either type of aberrant reinnervation can result in synkinesis of facial movements. For example, closing the eye (orbicularis oculi) may be accompanied by movement of the lips (orbicularis oris). Clinically, these reinnervation abnormalities may vary from being very subtle to very severe. In the most extreme case, synkinesis may lead to massive contractions on one side of the face. As most people blink spontaneously every few seconds, synkinesis involving the orbicularis oculi and other facial muscles can clinically appear very similar to hemifacial spasm (see later), although the etiology is quite different. Aberrant reinnervation may also occur between the motor axons of the facial nerve and the parasympathetic axons (i.e., nerve fibers derived from the facial motor root and nerve fibers derived from the nervus intermedius). Thus, parasympathetic axons may innervate motor endplates, and, conversely, motor axons may innervate the parasympathetic endplates. This may result in lacrimation, salivation, and/or hemifacial sweating when the facial muscles are activated. One can imagine the embarrassing situation wherein tears rather than saliva are produced while eating. 

Hemifacial Spasm Hemifacial spasm is a chronic and often progressive disorder usually associated with chronic compression of or injury to the facial nerve. The disorder is characterized by involuntary contractions that affect one or multiple muscles on one side of the face. The spasms typically occur initially around the eye and later spread to involve other ipsilateral facial muscles. The contractions are often irregular and persist during sleep. Although several unusual causes of chronic irritation are reported in the literature, the most common etiology is an aberrant blood vessel lying in contact with the facial nerve near its exit zone from the brainstem. The spasms are thought to be generated by damage to some axons of the facial nerve with ephaptic transmission to other nearby axons. Surgical decompression of the blood vessel away from the facial nerve often results in complete recovery. As noted earlier, massive reinnervation and subsequent synkinesis of the facial muscles may occur following an idiopathic facial palsy, leading to a pattern nearly identical clinically to hemifacial spasm. However, the underlying pathophysiology of hemifacial spasm (damage to the facial nerve with ephaptic transmission) differs from that of postparalytic facial syndrome (massive synkinesis that occurs with spontaneous blinking, due to aberrant reinnervation of muscles following idiopathic facial palsy). 

Trigeminal Neuropathy Trigeminal neuropathy is less common than facial palsy. It generally occurs as a purely sensory neuropathy in

482

SECTION VIII   Clinical Disorders

association with connective tissue disorders, most notably Sjögren syndrome or systemic lupus erythematosus. In addition, trigeminal neuropathy can be seen in association with toxic neuropathies, sometimes in isolation. Rarely, patients with local or metastatic cancer present with isolated involvement of the mentalis branch of V3 (so-­called “numb chin syndrome”). Isolated motor involvement of the trigeminal nerve is seen occasionally, usually in association with mass lesions or after surgery. Patients with purely sensory dysfunction of cranial nerve V present with numbness over the ipsilateral face. The distribution of numbness depends on the extent of nerve involvement and on which branches of the trigeminal nerve are involved. Involvement of the motor branch causes difficulty chewing and deviation of the jaw to the contralateral side when opening the mouth. 

Trigeminal Neuralgia Trigeminal neuralgia, also known as tic douloureux, is a condition characterized by episodes of severe pain in the distribution of one or more branches of the trigeminal nerve. It occurs most frequently in the maxillary division. Inconsequential stimuli, such as light touch over the cheek, eating, or brushing the teeth, can trigger excruciating pain. There is no associated sensory or motor dysfunction in the fifth nerve distribution, and standard nerve conduction and EMG evaluations are normal. Blink reflex studies usually are normal, although rarely, the R1 component may be abnormal on the affected side (found in 24–48 hours) and longer-­and higher-­dose steroids appear to be more likely to develop this complication. The total dose of intravenous methylprednisolone usually is more than 1000 mg. In recent years, there is growing evidence that CIM also occurs following the systemic inflammatory response syndrome (SIRS) that often accompanies sepsis, multiorgan failure, burns, trauma, and/or major procedures in the ICU. SIRS is felt to be present in the majority of patients hospitalized in the ICU for more than a week. In addition, many of the patients who develop CIM in the ICU also develop CIP as well, further complicating the clinical assessment, as well as the electrophysiologic evaluation (see Chapter 40). 

Late-­Onset Acid Maltase Deficiency (Pompe Disease) Pompe disease results from reduced or absent levels of the lysosomal enzyme alpha-­ glucosidase (GAA). In the

684

SECTION VIII   Clinical Disorders

infantile form, it is a systemic illness that leads to death within the first year of life. However, in adults who have reduced but not absent levels of GAA, it results in a proximal myopathy. This disorder is now extremely important to diagnose as it is treatable with enzyme replacement therapy. However, as the treatment principally prevents progression, starting treatment sooner, before significant disability has occurred, is critical. Late-­onset acid maltase deficiency typically presents in young adults as a proximal myopathy with variable elevations of the CK level. Often, it is misdiagnosed as a limb-­ girdle muscular dystrophy. Clinically, it has a propensity to affect the most proximal muscles, especially the abdominal and respiratory muscles, as well as the paraspinal muscles. Weakness of the abdominal muscles results in the inability to sit up from a lying position. Respiratory muscle weakness results in dyspnea on exertion, and later frank hypercapnic respiratory failure. Paraspinal muscle weakness may result in scoliosis and lumbar hyperlordosis. Scapular winging may be seen. The limb muscles may be surprisingly spared, including the biceps and quadriceps. Rarely, ptosis, dysarthria, and dysphagia may occur, which can result in a mistaken diagnosis of an NMJ disorder. On EDX testing, routine motor and sensory nerve conduction studies are normal. Repetitive nerve conduction studies are normal. The needle EMG often shows active denervation and myotonic discharges. However, these may be limited to the very proximal muscles, especially the paraspinal muscles, tensor fascia latae and diaphragm. Thus, the paraspinal muscles and tensor fascia latae are the key muscles to sample. In those muscles, MUAPs are typically small, short, and polyphasic. Definitive diagnosis is made with a simple blood test. This is a diagnosis not to miss, because of early treatment ramifications. The diagnosis should be considered in any patient with a myopathy involving abdominal and respiratory muscles. EMG can be extremely helpful in suggesting the diagnosis if myotonic discharges are found in the very proximal muscles. 

Fig. 38.7  Normal muscle on ultrasound.  Short axis of the tibialis anterior. Normal muscle fibers are hypoechoic, whereas the surrounding connective tissue in the perimysium and epimysium is hyperechoic, creating the “starry night” appearance on short axis imaging. The bone shadow of the tibia is on the left.

ULTRASOUND CORRELATIONS Neuromuscular ultrasound of myopathies was discussed in detail in Chapter 19. Although the indications for ultrasound in myopathy are more limited than mononeuropathies and polyneuropathies, ultrasound can add key information in selected cases. Normal muscle fibers are hypoechoic, whereas the surrounding connective tissue in the perimysium and epimysium is hyperechoic, creating the “starry night” appearance on short axis imaging (Fig. 38.7). On long axis, fascicles are typically arranged in parallel. In muscles where the fascicles attach to a central tendon, a “pennate” or feather-­like pattern will result (Fig. 38.8). The appearance of normal muscle on ultrasound varies depending on the patient’s age and sex and the particular muscle being studied. This is analogous to normal MUAPs on needle EMG varying in size depending on the muscle and the patient’s age.

Fig. 38.8  Normal muscle on ultrasound.  Long axis of the tibialis anterior. Fascicles are typically arranged in parallel in long axis. In muscles where the fascicles attach to a central tendon, a “pennate” or feather-­like pattern is seen. Top, Native image. Bottom, Same image with the central tendon in blue, fascia surrounding the muscle in green, and two individual muscle fascicles in pink.

In pathologic conditions, muscle most commonly results in one of three patterns on ultrasound (Fig. 38.9):    • Diffuse homogeneously increased echogenicity with attenuation of the ultrasound beam

Chapter 38 • Myopathy 685

Fig. 38.9  Ultrasound images of myogenic and neurogenic pathology.  Transverse views. Left, Duchenne muscular dystrophy. Middle, Immune myositis. Right, Denervation atrophy in amyotrophic lateral sclerosis. In the muscular dystrophy and myositis patients, the muscle has homogenously increased echogenicity. However, the bone shadow is well maintained in myositis patients (red arrow). Note the moth-­eaten appearance in denervation atrophy. (From Zaidman CM, vanAlfen N. Ultrasound in the assessment of myopathic disorders. J Clin Neurophysiol. 2016;33:103–111.)

• D  iffuse homogeneously increased echogenicity without attenuation of the ultrasound beam • Patchy hyperechogenic pattern with a “moth-­eaten appearance”    The first two patterns generally occur in primary muscle disorders, whereas the last pattern is seen in neuropathic conditions. In all three, the echogenicity increases as the size and number of muscle fibers decrease, and the amount of fat and connective tissue increases. In the muscular dystrophies and other very chronic myopathies, the first pattern is usually seen on ultrasound (diffuse homogeneously increased echogenicity with attenuation of the ultrasound beam). The muscle in this pattern is often said to have a “ground glass” appearance. As the myopathy becomes more severe, the ultrasound beam is attenuated as it passes through the abnormal muscle. This prevents echoes from returning from structures deep to the muscle. The second pattern seen in myopathies is similar to the first with the exception that there is a lack of significant attenuation of the ultrasound beam. The muscle has the same “ground glass” appearance as in the first pattern, but echoes from below the muscle remain well seen. Most often, this is best appreciated by intact echoes from adjacent bone. Immune myopathies (myositis) tend to show this pattern on muscle ultrasound. This pattern occurs because early in the disease, edema and inflammation are present, but the increased connective tissue or fat seen in dystrophies or the advanced stages of chronic myositis are not present in early stages of the disease. When this pattern is present, it strongly suggests an inflammatory myopathy over a muscular dystrophy. The last pattern, the “moth-­eaten” appearance, results in a patchy hyperechogenic picture, which can be present with any neuropathic disorder that results in denervation. From the previous discussion, it is clear that the determination of muscle echogenicity is critical in the assessment of

muscle on ultrasound. In scoring the severity of ultrasound abnormalities of muscle echogenicity, the Heckmatt scale is commonly used (Table 19.2). This scale was initially created to assess the severity of ultrasound changes in patients with muscular dystrophies. This is a subjective scale that looks at the echogenicity of muscle compared with a nearby bone shadow (Fig. 38.10). Muscle echogenicity is scored from 1 to 4, where 1 is normal, 2 is increased echogenicity but the bone shadow is well seen, 3 is increased echogenicity with the bone shadow partially obscured, and 4 is markedly increased echogenicity with the bone shadow completely obliterated. Thus, the extent to which adjacent bone shadow is seen is used as a measure of how much the ultrasound beam is attenuated as it travels through the diseased muscle. The Heckmatt scale can be used to assess echogenicity both in myopathic and neuropathic conditions, assess severity of muscle abnormalities in muscular dystrophies, and help differentiate myositis from muscular dystrophies. Both muscular dystrophies and myositis result in marked increased echogenicity of muscle. However, in myositis, an adjacent bone shadow is fairly well maintained, whereas in the dystrophies, it is usually markedly obscured. Once abnormal muscle has been identified on ultrasound, the next step is to look at the pattern of muscles that are affected and those that are spared. It is increasingly recognized that in some myopathies and dystrophies, certain muscles are affected or affected out of proportion to others. This selective muscle involvement can be demonstrated clinically in some disorders. In others, imaging is needed to show the specific pattern of muscle involvement. This has been extensively studied with magnetic resonance imaging (MRI), especially in the inherited myopathies. For example, MRI has shown that the most commonly affected muscle in the lower extremity in facioscapulohumeral muscular dystrophy is the semimembranosus muscle. In contrast, the use of neuromuscular ultrasound in demonstrating the pattern of muscle involvement in different myopathies is in its early stages.

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SECTION VIII   Clinical Disorders

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However, ultrasound has been reported as a useful adjunct in suggesting possible diagnoses based on the pattern of muscle involvement in certain myopathies. This is not simply a proximal vs distal pattern of involvement, but a difference between muscles at the same level and sometimes between muscles in the same functional group. For example, Fig. 38.11 shows sparing of the distal leg anterior compartment muscles with severe involvement of posterior calf muscles in a patient with an inherited distal myopathy. Although there are several types of inherited distal myopathies, some have a predilection for the posterior calf, as noted in Fig. 38.11, whereas others preferentially affect the anterior lower leg muscles. Another common example of selective muscle involvement occurs in IBM, wherein the long finger flexors are affected out of proportion to nearby muscles. On ultrasound, a characteristic pattern may be seen: myopathic changes are present in the FDP with relative sparing of the flexor digitorum sublimis or the adjacent flexor carpi ulnaris (Fig. 38.12). Similarly, in IBM, although the quadriceps are typically very weak and atrophic, the rectus femoris is relatively spared compared with the vastus medialis, lateralis, and intermedialis. This pattern of relative sparing of the rectus femoris can also be demonstrated on ultrasound (Fig. 38.13).

Lastly, the pattern of muscle involvement in late-­onset acid maltase deficiency has been well studied by Zaidman and colleagues. They concluded that three patterns should suggest the possibility of this diagnosis:    1. Involvement of the biceps brachii and brachialis with sparing of the triceps 2. Involvement of the biceps brachii and brachialis with sparing of the outer layer of the biceps brachii 3. Involvement of the vastus intermedialis with relative sparing of the rectus femoris    It is important to emphasize that the pattern of muscle involvement is only one piece of data that is helpful in the evaluation of various myopathies. However, no pattern is completely specific. Take two examples: First, in cases of ulnar neuropathy at the elbow, one can often see more involvement of the FDP to digits 4 and 5 than the flexor carpi ulnaris, a pattern also seen in IBM. However, in IBM, remember that one will also see involvement of several other muscles in the upper and lower extremities, suggesting a more widespread process. Second, the pattern of an abnormal vastus intermedialis with sparing of the rectus femoris is seen both in IBM as well as in late-­onset acid maltase deficiency. However, the clinical presentation in

Chapter 38 • Myopathy 687

Fig. 38.11  Selective pattern of muscle abnormalities.  Ultrasound can be helpful not only in identifying a myopathy but also in assessing the pattern of muscle involvement. In this case of an inherited distal myopathy affecting the posterior calf muscles, the tibialis anterior is normal (left), whereas the soleus (middle) and medial gastrocnemius (right) are markedly abnormal.

)&8

)'3

8/1$

Fig. 38.12  Selective muscle involvement in inclusion body myositis.  Left, Short axis view over the proximal medial forearm, native image. Right, Same image with the flexor carpi ulnaris (FCU) in red and the flexor digitorum profundus (FDP) in purple. One common example of selective muscle involvement is seen in inclusion body myositis, wherein the long finger flexors are affected out of proportion to nearby muscles. On ultrasound, a characteristic pattern may be seen: myopathic changes are present in the FDP with relative sparing of the flexor digitorum sublimis or the adjacent FCU. Note the difference in echogencity between the two muscles in this patient with IBM.

these two myopathies is very different. Thus ultrasound follows the same caveat as EDX studies: any abnormality must be considered in conjunction with the history and physical examination. When screening muscle, ultrasound can also be used to aid selection of which muscle to biopsy. Ideally, one needs to choose a muscle that is abnormal but not end-­stage. Biopsy of a muscle that looks completely normal on ultrasound may result in a normal muscle biopsy on pathology. Biopsy of an end-­stage muscle may result in a non-­diagnostic biopsy wherein most of the biopsy is composed of fat and connective tissue and only a few muscle fibers remain, which are not sufficient for a diagnosis. Ultrasound can also be used to measure muscle size and/or thickness. Muscles can be normal, atrophic, hypertrophic, or pseudo-­hypertrophic. When measuring muscle size, it is important that the muscle be in a relaxed state; muscle contraction results in muscle thickening. It is also important to measure the muscle while ensuring that there is little probe pressure on the muscle. Muscles are easily compressed, which can alter their size and thickness. Atrophy can be seen in disuse, neuropathic, or myopathic

5)

9,0

Fig. 38.13  Selective muscle involvement in inclusion body myositis (IBM).  Short axis view over anterior thigh. Note the marked difference in echogenicity in this patient with IBM, with relative sparing of the rectus femoris. Although this pattern is not completely specific to IBM, its presence in the appropriate clinical context is highly supportive of the diagnosis. RF, Rectus femoris; VIM, vastus intermedialis.

SECTION VIII   Clinical Disorders

688

conditions. In some dystrophies and metabolic myopathies, and rarely in some inflammatory myopathies, muscle size is increased, which is not due to increased size of muscle fibers. In these conditions, the muscle enlargement is due to pseudo-­hypertrophy, and the muscle is large because it has been infiltrated with fat, connective tissue, amyloid, or granulomatous tissue.

getting out of low chairs are symptoms characteristic of proximal lower extremity weakness. On examination, proximal weakness in both upper and lower extremities, as well as mild weakness in the neck flexors, was found. Weakness of neck flexion is a key finding that indicates abnormalities above the cervical area. In some patients, it may be difficult to differentiate whether upper extremity proximal weakness is due to myopathy or radiculopathy affecting the C5 and C6 roots. In such cases, examination of the neck flexors can be very helpful because they frequently are abnormal in myopathy. The differential diagnosis of proximal weakness includes myopathy, polyradiculopathy, motor neuron disorders, NMJ transmission disorders, and unusual primarily motor demyelinating neuropathies. The absence of any sensory symptoms along with the intact reflexes argues against the possibility of a polyradiculopathy or demyelinating motor neuropathy. The absence of fatigability or weakness of the extraocular muscles makes the diagnosis of MG unlikely, although MG, along with LEMS, must still be considered. The history of long-­term prednisone use may be important, because steroids are a common cause of myopathy. Reviewing the nerve conduction findings, the right median, ulnar, tibial, and peroneal motor studies and F-­response studies are normal. All of the CMAP amplitudes, conduction velocities, and latencies are normal. Likewise, the median, ulnar, and sural sensory responses are intact. These normal motor, sensory, and F-­ response studies effectively exclude a demyelinating polyneuropathy. In addition, the normal

EXAMPLE CASES Case 38.1 History and Physical Examination A 42-­year-­old woman was referred for progressive weakness of several months’ duration. She had a long history of asthma treated with low-­dose oral prednisone. Her initial symptoms were difficulty going up and down stairs and getting out of chairs. In addition, she developed mild difficulty with swallowing. The process was symmetric and progressive with little pain. Neurologic examination showed mild proximal weakness in both upper and lower extremities. There was mild weakness of neck flexion with preserved neck extension. Muscle bulk and tone were normal. No facial or bulbar weakness was noted. Deep tendon reflexes and sensation were normal. 

Summary The history in this case suggests proximal muscle weakness. Difficulty going up and down stairs and difficulty

CASE 38.1 Nerve Conduction Studies. Amplitude Motor = mV; Sensory = μV

Latency (ms)

Nerve Stimulated

Stimulation Site

Recording Site

RT

Median (m)

Wrist Antecubital fossa

APB APB

9.4 8.9

≥4

4.2 8.5

≤4.4

Ulnar (m)

Wrist Below elbow Above elbow

ADM ADM ADM

8.2 8.2 8.2

≥6

2.9 6.5 8.2

≤3.3

Median (s)

Wrist

Index finger

34

≥20

3.4

Ulnar (s)

Wrist

Little finger

25

≥17

Tibial (m)

Ankle Popliteal fossa

AHB AHB

7.4 7.0

Peroneal (m)

Ankle Below fibula Lateral popliteal fossa

EDB EDB EDB

Sural (s)

Calf

Posterior ankle

  

LT

NL

RT

LT

NL

Conduction Velocity (m/s)

F-­wave Latency (ms)

RT

RT

LT

NL

64

≥49

60 60

≥49 ≥49

≤3.5

55

≥50

2.9

≤3.1

64

≥50

≥4

4.7 12.3

≤5.8

44

≥41

4.2 4.0 4.0

≥2

4.8 8.4 11.2

≤6.5

45 44

≥44 ≥44

24

≥6

4.2

≤4.4

47

≥40

LT

NL

28

≤31

29

≤32

52

≤56

51

≤56

Note: All sensory latencies are peak latencies. All sensory conduction velocities are calculated using onset latencies. The reported F-­wave latency represents the minimum F-­wave latency. ADM, Abductor digiti minimi; AHB, abductor hallucis brevis; APB, abductor pollicis brevis; EDB, extensor digitorum brevis; LT, left; m, motor study; NL, normal; RT, right; s, sensory study.

Chapter 38 • Myopathy 689 CASE 38.1 Electromyography. Spontaneous Activity

Voluntary Motor Unit Action Potentials Configuration

Insertional Activity

Fibrillation Potentials

Fasciculation Potentials

Activation

Recruitment

Duration

Amplitude

Polyphasia

Right first dorsal interosseous

NL

0

0

NL

NL

NL

NL

NL

Right abductor pollicis brevis

NL

0

0

NL

NL

NL

NL

NL

Right extensor indicis proprius

NL

0

0

NL

NL

NL

NL

NL

Right biceps brachii

↑

+2

0

NL

Early

−2

−2

+2

Right pronator teres

↑

+1

0

NL

Early

−2

−2

+2

Right iliacus

↑

+1

0

NL

Early

−2

−2

+2

Right vastus lateralis

↑

+1

0

NL

Early

−1

−1

+1

Right tibialis anterior

↑

+1

0

NL

Early

−1

−1

+1

Right L5 paraspinal

↑

+2

0

NL

Early

−2

−2

+2

Right T6 paraspinal

↑

+2

0

NL

Early

−2

−2

+2

Muscle

  

↑, Increased; NL, normal.

CMAP amplitudes at rest make the diagnosis of LEMS unlikely. The EMG findings are very abnormal, with diffuse fibrillation potentials, especially in the proximal muscles. In addition, many of the MUAPs in the proximal muscles are of brief duration, low amplitude, and polyphasic with an early recruitment pattern. This MUAP profile of brief-­ duration, low-­amplitude polyphasic MUAPs with early recruitment is characteristic of myopathic MUAPs. The prominent fibrillation potentials yield additional important diagnostic information, suggesting an inflammatory or necrotic muscle disease. Note that fibrillation potentials are not seen in steroid myopathy or in most cases of MG or LEMS. When the nerve conduction studies and EMG examination are complete, the electrophysiologic impression can be formulated. IMPRESSION: There is electrophysiologic evidence consistent with a proximal myopathy with active denervating features. This case raises several important questions.

Does the EMG–Nerve Conduction–Clinical Correlation Make Sense? There are several important correlations to note among the electrophysiologic study, the clinical history, and the

neurologic examination. Looking first at the correlation between the motor nerve conduction studies and the needle EMG, the motor nerve conduction studies are quite normal, whereas the needle EMG findings are very abnormal. This paradox occurs because motor nerve conduction studies routinely record distal muscles, which are normal in most myopathies, whereas the needle EMG also can sample proximal muscles, which are abnormal in most myopathies. If CMAPs had been recorded from proximal muscles, where denervation is seen on the needle EMG, these would likely be abnormal with low amplitudes. It is not unusual for the routine motor conduction studies to be normal in typical proximal myopathies. The next point to consider is the presence of the prominent fibrillation potentials, in light of the patient’s history of steroid use. Although the patient takes steroids, her myopathy cannot be attributed to steroid use because of the active denervation. This EMG pattern is much more suggestive of an inflammatory myopathy such as PM. The presence of brief-­duration, low-­amplitude, polyphasic MUAPs with early recruitment also eliminates the neuropathic disorders from the differential diagnosis, including amyotrophic lateral sclerosis, adult-­onset spinal muscular atrophy, motor neuropathies, and polyradiculopathy. Early recruitment is characteristic of myopathic disorders. Because there is dropout or dysfunction of individual muscle fibers, each motor unit can generate less force. Therefore, more motor units than usual are needed

SECTION VIII   Clinical Disorders

690

to create a small amount of force. The EMG correlate of this underlying pathophysiology is the finding that the EMG screen fills very easily with many brief-­duration, low-­ amplitude polyphasic MUAPs with a very small amount of force. To judge recruitment requires knowledge of how much force is being generated. Only the electromyographer can clearly assess early recruitment. 

Neurologic examination revealed normal cranial nerves and full strength in the neck flexors and extensors. He had 4/5 strength in the deltoids bilaterally and full strength in the biceps and triceps. More distally, the wrist extensors were 4/5, finger flexors were 3/5, and median and ulnar hand intrinsics were 4/5 bilaterally. Muscle bulk was near normal in the upper extremities, except for mild wasting of the proximal volar forearms. In his lower extremities, hip flexion was mildly weak bilaterally. There was prominent weakness of left knee extension (2/5) and bilateral foot dorsiflexion (3/5). Prominent wasting was noted in the left thigh and distally in both anterior calves. Deep tendon reflexes were 1+ in the upper extremities and at the right knee but were otherwise absent at the ankles and the left knee. Plantar responses were flexor bilaterally. Sensory examination, including vibration sense, light touch, position sense, and temperature sensation, was normal in the distal upper and lower extremities. Coordination was normal. He walked with a marked steppage gait. 

Which Muscle Should Be Biopsied? Muscle biopsy was performed on the contralateral vastus lateralis muscle. The contralateral side was chosen to avoid the possibility that minor inflammation caused by the EMG needle would be misinterpreted. Pathologic examination subsequently showed muscle fiber necrosis, with prominent mononuclear inflammatory infiltrates consistent with the diagnosis of PM. The patient was treated with high-­dose prednisone and responded well. 

Case 38.2 History and Physical Examination

Summary

A 75-­year-­old man developed progressive difficulty walking over a 2-­year period. Initially, he noted that his gait was slightly unsteady. Later, he developed difficulty walking up stairs. His symptoms slowly worsened to the point that he would trip frequently when he walked quickly or walked on uneven ground. He noted no pain, numbness, or paresthesias in his legs and no bowel or bladder difficulties. He complained of no arm weakness, visual difficulties, or speech or swallowing problems.

The history and examination in this case suggest slowly progressive asymmetric weakness, predominantly affecting the lower extremities. There are no sensory complaints or sensory findings suggesting a radiculopathy or polyneuropathy. Examination shows asymmetric weakness and wasting, involving both proximal and distal muscles, but with a predilection for the left knee extensors and bilateral finger flexors. The diminished reflexes at the ankles and the left knee suggest a possible neuropathic process, although

CASE 38.2 Nerve Conduction Studies.

Stimulation Site

Recording Site

Median (m)

Wrist Antecubital fossa

Ulnar (m)

Nerve Stimulated

  

Amplitude Motor = mV; Sensory = μV RT

Latency (ms)

LT

NL

RT

LT

NL

APB APB

9.9 9.8

≥4

4.0 7.9

≤4.4

Wrist Below elbow Above elbow

ADM ADM ADM

9.5 8.9 8.8

≥6

3.3 6.9 8.9

≤3.3

Median (s)

Wrist

Index finger

25

≥20

3.4

Ulnar (s)

Wrist

Little finger

17

≥17

Tibial (m)

Ankle Popliteal fossa

AHB AHB

2.6 2.3

Peroneal (m)

Ankle Below fibula Lateral popliteal fossa

EDB EDB EDB

Sural (s)

Calf

Posterior ankle

Conduction Velocity (m/s) RT

LT

NL

51

≥49

55 50

≥49 ≥49

≤3.5

54

≥50

2.9

≤3.1

50

≥50

≥4

5.3 14.1

≤5.8

40

≥41

1.1 0.9 0.9

≥2

5.1 14.1 16.6

≤6.5

38 40

≥44 ≥44

16

≥6

3.7

≤4.4

45

≥40

F-wave Latency (ms) RT

LT

NL

27

≤31

29

≤32

60

≤56

56

≤56

Note: All sensory latencies are peak latencies. All sensory conduction velocities are calculated using onset latencies. The reported F-­wave latency represents the minimum F-­wave latency. ADM, Abductor digiti minimi; AHB, abductor hallucis brevis; APB, abductor pollicis brevis; EDB, extensor digitorum brevis; LT, left; m, motor study; NL, normal; RT, right; s, sensory study.

Chapter 38 • Myopathy 691 CASE 38.2 Electromyography. Spontaneous Activity

Voluntary Motor Unit Action Potentials Configuration

Insertional Activity

Fibrillation Potentials

Fasciculation Potentials

Activation

Recruitment

Left tibialis anterior

CRD

+1

0

NL

Early

Left medial gastrocnemius

CRD

+2

0

NL

Left vastus lateralis

CRD

+2

0

Left iliacus

CRD

+2

Left L5 paraspinal

CRD

Left first dorsal interosseous

Muscle

Amplitude

Polyphasia

−1

NL

+2

Early

−1

NL

+1

NL

↓

−1/+1

NL

+1

0

NL

Early

−1

NL

+1

+1

0

NL

NL

−1

NL

+1

CRD

+2

0

NL

Early

−1

NL

+1

Left pronator teres

CRD

+1

0

NL

Early

−1

NL

NL

Left triceps

↑

0

0

NL

Early

−1

NL

+1

Left biceps brachii

↑

+1

0

NL

Early

−1

NL

+1

Left medial deltoid

CRD

+1

0

NL

Early

−1

NL

+1

  

Duration

↑, Increased; ↓, slightly reduced; CRD, complex repetitive discharge; NL, normal.

reduced reflexes may be seen with severe weakness from any cause. Given the history and neurologic examination, the differential diagnosis includes motor neuron disease, a demyelinating motor neuropathy, or an unusual myopathy that is asymmetric and affects proximal and distal muscles. The prominent asymmetry and muscle wasting are not consistent with a disorder of the NMJ. Moving on to the electrophysiology, the left median and ulnar motor and sensory nerve conduction studies and F responses are normal. In the left lower extremity, however, the peroneal and tibial CMAP amplitudes are decreased, with normal distal motor latencies and slightly slowed conduction velocities. The tibial F response latency is also slightly prolonged. The left sural sensory response is intact. The low motor responses with normal sensory responses in the lower extremity again suggest a predominant motor problem. The absence of markedly prolonged distal motor latencies or conduction velocity slowing, with no evidence of conduction block or temporal dispersion, effectively excludes a demyelinating motor polyneuropathy. After reviewing the nerve conduction studies, the possibility of motor neuron disease or an unusual disorder of muscle must still be considered. The EMG shows prominent spontaneous activity, with frequent complex repetitive discharges and fibrillation potentials in most muscles tested. Most of the MUAPs, however, are short duration and polyphasic with early recruitment, consistent with a myopathy. The only exception is the left vastus lateralis, which has both long-­and

short-­duration polyphasic MUAPs with slightly reduced recruitment. After the nerve conduction and EMG studies, the electrophysiologic impression can be formulated. IMPRESSION: There is electrophysiologic evidence consistent with a chronic, asymmetric myopathy with denervating features. Several important questions can be addressed.

What Is the Significance of the Complex Repetitive Discharges? The presence of the complex repetitive discharges implies that the process is chronic. In addition, the finding of both long-­and short-­duration MUAPs in the vastus lateralis suggests a chronic process, and, in the setting of small, short-­duration MUAPs with early recruitment in other muscles, a chronic myopathy. Although myopathy is characteristically associated with small, short MUAPs, large, prolonged MUAPs also can be seen in chronic myopathies associated with denervating features (inflammatory and necrotic myopathies) in which reinnervation occurs as well. This patient eventually had a biopsy of the right medial deltoid, a muscle that was clinically involved but had not been studied with the EMG needle. Pathologic examination showed marked variation in fiber size, marked mononuclear inflammatory infiltrates, numerous rimmed vacuoles, and intracytoplasmic inclusions. The pathologic diagnosis was IBM.

692

SECTION VIII   Clinical Disorders

IBM usually presents in older men as a very slowly progressive muscle disorder often affecting both upper and lower extremity muscles. Many patients develop distal as well as proximal weakness. In some patients, weakness may be limited to the distal muscles. IBM often involves certain muscles preferentially, including the quadriceps, iliopsoas, tibialis anterior, biceps, triceps, and the forearm and long finger flexors. Focal atrophy of one of these muscles suggests the possibility of IBM. Occasional patients develop isolated dysphagia from IBM. Electrophysiology often shows normal motor and sensory nerve conduction studies, although approximately one third of patients have mild slowing of motor and sensory conduction velocities. If distal muscles have been affected by the myopathy, the CMAP amplitudes also may be low. Fibrillation potentials are quite common, as are complex repetitive discharges, especially in long-­ standing cases. MUAPs may be brief or of long duration. A combination of large and small MUAPs may be present within the same muscle. In muscles that are severely affected by the myopathy, recruitment may actually be reduced. This occurs if every muscle fiber within a motor unit is lost, effectively leading to loss of the motor unit. In end-­stage muscle secondary to myopathy, it is not unusual to see fibrillation potentials with large, prolonged MUAPs and a decreased recruitment pattern. These findings often incorrectly suggest a neuropathic illness, such as motor neuron disease. However, any EMG examination showing large, prolonged polyphasic MUAPs with a relatively normal or just slightly reduced recruitment pattern should suggest the possibility of a chronic myopathy. The only EMG clue that the disorder is myopathic in these cases is that the magnitude of the MUAP abnormalities appears too great for the mild degree of decreased recruitment. Indeed, there are occasional patients with chronic IBM in whom it is very difficult to differentiate IBM both clinically and electromyographically from the progressive muscular atrophy form of motor neuron disease.

Suggested Readings Brown WF. The Physiological and Technical Basis of Electromyography. Boston: Butterworth; 1984. Brown WF, Bolton CF, eds. Clinical Electromyography. 2nd ed. Boston: Butterworth; 1993. Buchthal F, Pinelli P. Muscle action potentials in polymyositis. Neurology. 1953;3:424. Bunch TW. Polymyositis: a case history approach to the differential diagnosis and treatment. Mayo Clin Proc. 1990;65:480. Dalakas MC. Polymyositis, dermatomyositis, and inclusion-­ body myositis. N Engl J Med. 1991;325:1487.

Dubrovsky A, Corderi J, Karasarides T, Taratuto AL. Pompe disease, the must-­not-­miss diagnosis: a report of 3 patients. Muscle Nerve. 2013;47(4):594–600. Hokkoku K, Sonoo M, Higashihara M, Stålberg E, Shimizu T. Electromyographs of the flexor digitorum profundus muscle are useful for the diagnosis of inclusion body myositis. Muscle Nerve. 2012;46(2):181–186. Joy JL, Oh SJ, Baysal AI. Electrophysiological spectrum of inclusion body myositis. Muscle Nerve. 1990;13:949. Kassardjian CD, Engel AG, Sorenson EJ. Electromyographic findings in 37 patients with adult-­onset acid maltase deficiency. Muscle Nerve. 2015;51(5):759–761. Kramer CL, Boon AJ, Harper CM, Goodman BP. Compound muscle action potential duration in critical illness neuromyopathy. Muscle Nerve. 2018;57(3):395–400. Kolb NA, Trevino CR, Waheed W, et al. Neuromuscular complications of immune checkpoint inhibitor therapy. Muscle Nerve. 2018. Kumar Y, Wadhwa V, Phillips L, Pezeshk P, Chhabra A. MR imaging of skeletal muscle signal alterations: systematic approach to evaluation. Eur J Radiol. 2016;85(5):922–935. Lacomis D, Guiliani MJ, Van Cott A, et al. Acute myopathy of intensive care: clinical, electromyographic, and pathological aspects. Ann Neurol. 1996;40:645. Leung DG. Magnetic resonance imaging patterns of muscle involvement in genetic muscle diseases: a systematic review. J Neurol. 2017;264(7):1320–1333. Lindberg C, Persson LI, Bjorkander J, et al. Inclusion body myositis: clinical, morphological, physiological and laboratory findings in 18 cases. Acta Neurol Scan. 1994;89:123. Mohassel P, Mammen AL. Statin-­associated autoimmune myopathy and anti-­HMGCR autoantibodies. Muscle Nerve. 2013;48(4):477–483. Mongiovi PC, Elsheikh B, Lawson VH, Kissel JT, Arnold WD. Neuromuscular junction disorders mimicking myopathy. Muscle Nerve. 2014;50(5):854–856. Nojszewska M, Gawel M, Szmidt-­Salkowska E, et al. Abnormal spontaneous activity in primary myopathic disorders. Muscle Nerve. 2017;56(3):427–432. Noto Y, Shiga K, Tsuji Y, et al. Contrasting echogenicity in flexor digitorum profundus-­flexor carpi ulnaris: a diagnostic ultrasound pattern in sporadic inclusion body myositis. Muscle Nerve. 2014;49(5):745–748. Ringel SP, Kenny CE, Neville HE, et al. Spectrum of inclusion body myositis. Arch Neurol. 1987;44:1154. Robinson LR. AAEM case report, No. 22: polymyositis. Muscle Nerve. 1991;14:310. Sayers ME, Chou SM, Calabrese LH. Inclusion body myositis: analysis of 32 cases. J Rheumatol. 1992;19:1385. Zaidman CM, Malkus EC, Siener C, Florence J, Pestronk A, Al-­Lozi M. Qualitative and quantitative skeletal muscle ultrasound in late-­onset acid maltase deficiency. Muscle Nerve. 2011;44(3):418–423. Zaidman CM, vanAlfen N. Ultrasound in the assessment of myopathic disorders. J Clin Neurophysiol. 2016;33:103–111.

SECTION VIII • Clinical Disorders PART V • Disorders of Neuromuscular Junction and Muscle

Myotonic Muscle Disorders and Periodic Paralysis Syndromes The myotonic muscle disorders compose a group of disorders characterized by muscle stiffness, pain, and sometimes weakness, which may be intermittent or constant. The primary periodic paralyses are rare inherited disorders associated with attacks of muscle paralysis. Depending on the specific disorder, attacks may last minutes, hours, or days, and some are associated with fixed weakness. The myotonic disorders and periodic paralyses are grouped together as some of them overlap with each other, and all are “channelopathies” associated with mutations of muscle sodium, calcium, potassium, or chloride channels. Evaluation of these disorders in the electromyography (EMG) laboratory is particularly gratifying, as the EMG accompaniment of myotonia is easily recognized by the experienced electromyographer. Clinically, myotonia is characterized by delayed muscle contraction after activation. Myotonia can also be demonstrated after percussion of the muscle. On EMG, myotonic discharges produce a distinctive revving engine sound. This results from the spontaneous firing of muscle fibers that wax and wane in frequency and amplitude, producing this unmistakable sound (Fig. 39.1). The myotonic potential may take the form of either a positive wave or a brief spike potential, thus identifying the source generator as a muscle fiber. Myotonia can be induced by mechanical stimulation, such as percussion of the muscle or movement of the EMG needle or may follow voluntary muscle contraction. Clinically, myotonia is noted most frequently in the myotonic muscle disorders and in some of the periodic paralysis syndromes (Box 39.1). Patients describe an inability to relax their muscles after

—9 PV

Fig. 39.1  Myotonic discharge.  A myotonic discharge is the spontaneous discharge of a muscle fiber that waxes and wanes in both amplitude and frequency. An individual myotonic potential may have either a positive wave or a brief spike morphology (identifying the source generator as a muscle fiber). Myotonic discharges are characteristically seen in myotonic dystrophy, myotonia congenita, paramyotonia congenital, and in some patients with hyperkalemic periodic paralysis. They also may occur in some myopathies, (e.g., acid maltase deficiency, polymyositis, myotubular myopathy, myofibrillar myopathy, and hyperkalemic periodic paralysis).

39

contraction, such as during hand grip. In addition, myotonia may be experienced by the patient as muscle stiffness. Traditionally, the myotonic muscle disorders have been classified into those with dystrophic changes on muscle biopsy, such as the myotonic dystrophies, resulting in weakness, and those without dystrophic changes, such as myotonia congenita and paramyotonia congenita, where weakness is generally not a feature. Myotonia also occurs in several of the periodic paralysis syndromes, both inherited and acquired, as well as on the EMG examination in some metabolic, inflammatory, congenital, and toxic myopathies, although clinical myotonia is generally not apparent. Myotonia can be unmasked or precipitated by various drugs. Very rarely, myotonic discharges are noted on EMG examination in disorders of nerve associated with severe denervation. Although a single, brief run of myotonia may be seen in denervating disorders, it is never the predominant waveform. Neuromyotonia, a rare phenomenon associated with peripheral nerve as opposed to muscle disorders, may result in a delay in muscle relaxation. However, this can be distinguished from myotonia in the EMG laboratory by the spontaneous firing of motor unit action potentials (MUAPs) as opposed to muscle fiber action potentials. Genetic linkage and mutational analyses have identified the molecular basis for several of the myotonic muscle disorders and the periodic paralysis syndromes, resulting in the classification of these disorders based on a specific ion channel or protein kinase defect. However, this still leaves a substantial number of patients in whom the diagnosis rests on clinical and electrophysiologic findings alone. Table 39.1 reviews the classification of these disorders based on clinical, electrophysiologic, and available molecular findings. The electrophysiologic evaluation is directed toward answering several key questions to arrive at the correct diagnosis, including whether myotonia is present or not. To answer these questions, a variety of tests can be performed in the EMG laboratory to distinguish among the dystrophic and nondystrophic myotonic muscle disorders, the periodic paralysis syndromes, and other disorders of muscle with accompanying EMG myotonia. In addition to routine nerve conduction studies and needle EMG, muscle cooling, exercise testing, and repetitive nerve stimulation (RNS) often are very helpful in differentiating among these disorders (Box 39.2).

693

694

SECTION VIII   Clinical Disorders

Box 39.1  Classification of Myotonic and Periodic Paralysis Disorders I. Inherited myotonic muscle/periodic paralysis disorders A. Dystrophic myotonic muscle disorders 1. Myotonic dystrophy, types 1 and 2 B. Nondystrophic myotonic muscle disorders/periodic paralysis syndromes 1. Chloride channel disorders a. Autosomal dominant myotonia congenita (Thomsen) b. Autosomal recessive myotonia congenita (Becker) 2. Sodium channel disorders a. Paramyotonia congenita (Eulenburg) b. Hyperkalemic periodic paralysis (±myotonia) c. Sodium channel myotonia congenita d. Hypokalemic periodic paralysis type 2 (rare form) C. Andersen-­Tawil syndrome (no myotonia) D. Hypokalemic periodic paralysis, type 1 (calcium channel, no myotonia) E. Schwartz-­Jampel syndrome II. Acquired periodic paralysis disorders A. Secondary hyperkalemic periodic paralysis (may be associated with myotonia) may be seen in association with the following: 1. Renal failure 2. Adrenal failure 3. Hypoaldosteronism 4. Metabolic acidosis

MUSCLE COOLING In some of the myotonic disorders, muscle cooling can be used to enhance myotonic discharges or bring out other characteristic abnormalities (see sections on Myotonia Congenita and Paramyotonia Congenita). Muscle cooling is best accomplished by wrapping the limb in a plastic bag and submerging it in ice water for 10–20 minutes. After the skin temperature is brought down to 20°C, needle EMG of the extremity is performed, with the electromyographer looking for abnormalities. Note that the patient should be watched closely, and the limb should always be removed from the ice water immediately if weakness develops. 

EXERCISE TESTING Exercise testing can play an important role in the periodic paralysis and myotonic syndromes. Both short and prolonged exercise tests can be performed. In both, a routine distal compound muscle action potential (CMAP) is evoked with supramaximal stimulation (e.g., stimulating the ulnar nerve at the wrist, recording the abductor digiti minimi [ADM]). The nerve then is stimulated at 1-­minute intervals for several minutes to ensure a stable baseline, before exercise is begun.

Short Exercise Test For the short exercise test, the patient is asked to rest for 5 minutes while a CMAP is recorded every minute, to ensure that the baseline is stable. The baseline may decrease just

B. Secondary hypokalemic periodic paralysis (not associated with myotonia) may be seen in association with: 1. Hyperthyroidism, especially in Asian adult males 2. Primary hyperaldosteronism 3. Diuretics 4. Inadequate potassium intake 5. Chronic licorice ingestion 6. Excessive potassium loss through sweat 7. Gastrointestinal or renal potassium wasting 8. Steroid use III. Muscle disorders associated with electromyographic myotonia A. Metabolic: acid maltase deficiency B. Inflammatory: polymyositis C. Congenital: myotubular myopathy, myofibrillar myopathy D. Associated with systemic disorders: malignant hyperpyrexia E. Drug-­induced hypothyroidism IV. Drugs that unmask or precipitate myotonia either clinically or on electromyographic examination A. Clofibrate B. Propranolol C. Fenoterol D. Terbutaline E. Colchicine F. Penicillamine G. Cyclosporin H. Hydroxymethylglutaryl coenzyme A (HMG-­CoA) reductase inhibitors (lipid-­lowering agents)

with rest in some patients, especially patients with a periodic paralysis disorder. After ensuring a stable baseline, the patient is then asked to perform maximal voluntary contraction for 5–10 seconds. Immediately afterward, a CMAP is recorded. The CMAP is recorded every 10 seconds until the CMAP recovers to baseline (typically 1–2 minutes) (Fig. 39.2). If a decrement occurs after brief exercise and then recovers, the same procedure is repeated several times to see if the decrement continues to occur or habituates, which can help differentiate among some of the myotonic syndromes (discussed later). 

Prolonged Exercise Test For the prolonged exercise test, the recording procedure is the same. The patient is asked to rest for 5 minutes while a CMAP is recorded every minute to ensure the baseline is stable. The baseline may decrease just with rest in some patients, especially patients with a periodic paralysis disorder. After ensuring a stable baseline, the patient is asked to voluntarily contract his or her muscle maximally for 5 minutes, resting every 15 seconds for a few seconds. After the 5 minutes of exercise are complete, the patient relaxes completely. A CMAP is recorded immediately and then every 1–2 minutes for the next 40 minutes. In the periodic paralysis syndromes, both inherited and acquired, the CMAP amplitude may be unchanged or slightly larger immediately after prolonged exercise and then decline substantially over the next 20–40 minutes (Fig. 39.3).

Table 39.1  Clinical Features of Myotonic and Periodic Paralysis Disorders. Myotonic Dystrophy, Type 2

Myotonia Congenita: Dominant

Myotonia Congenita: Recessive

Sodium Channel Myotonia

Hyperkalemic Periodic Paralysis

Hypokalemic Periodic Paralysis

Andersen-­ Tawil Syndrome

Age at onset

Teens to early adult

Teens to mid-­ adult

Infancy

Early childhood

Childhood to early teens

Infancy

Infancy to early childhood

Early teens

Childhood or early teens

Inheritance

Autosomal dominant

Autosomal dominant

Autosomal dominant

Autosomal recessive

Autosomal dominant

Autosomal dominant

Autosomal dominant

Autosomal dominant

Autosomal dominant

Gene defect

Protein kinase, chromosome 19q (DMPK gene)

Cellular nucleic Chloride acid–binding channel, protein, chromosome chromosome 7q (CLCN 3q (CNBP gene) gene)

Chloride channel, chromosome 7q (CLCN gene)

Sodium channel, chromosome 17q (SCN4A gene)

Sodium channel, chromosome 17q (SCN4A gene)

Sodium channel, chromosome 17q (SCN4A gene)

Calcium channel, Potassium chromosome channel, 1q (type 1) chromo(CACNA1S some 17q gene) (KCNJ2 Sodium channel gene) chromosome 17q (type 2) (SCN4A gene)

Myotonia

Yes

Yes

Yes

Yes

Yes

Yes

Yes

No

No

Distribution of myotonia

Distal more Proximal and than proximal distal

Generalized

Generalized

Proximal more than distal

Face, hands, thighs

Generalized, if present

None

None

Periodic weakness

No

No

No

Yes, in some patients

No

Yes

Yes

Yes

Yes, in some patients

Duration of weakness

N/A

N/A

N/A

N/A

N/A

Minutes to days

Minutes to days

Hours to days

Variable

Progressive weakness

Yes

Yes

No

Rarely

No

No

Variable

Yes

Yes

Extramuscular involvement

Yes

Yes

No

No

No

No

No

No

Yes

Provocative factors

None

None

Cold

Cold

Potassium, delay after exercise

Cold, exercise, fasting

Cold, rest after Cold, rest after exercise, exercise, emoemotional tional stress, stress, fasting, carbohydrates, potassium alcohol loading

Rest after exercise, alcohol

Alleviating factors

None

None

Exercise

Exercise

Unknown

Warming

Carbohydrates, mild exercise

Mild exercise

Paramyotonia Congenita

Potassium, mild exercise

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 695

Myotonic Dystrophy, Type 1

696

SECTION VIII   Clinical Disorders

Box 39.2  Protocol for Evaluation of Myotonic and Periodic Paralysis Disorders 1. Routine motor and sensory nerve conduction studies should be done first. Generally, one or two motor and sensory conduction studies and corresponding F responses in an upper and lower extremity should be performed. Distal CMAPs may be low in the dystrophic myopathies. Proceed to needle EMG. 2. Needle EMG study is carried out after standard conduction studies are completed. The study should include proximal and distal muscles of one upper and lower extremity, as well as facial and paraspinal muscles. Careful note should be made of abnormal spontaneous activity, including myotonic discharges, complex repetitive discharges, fibrillation potentials and positive waves, and MUAP potential configuration and recruitment pattern. 3. Muscle cooling is carried out if there is a clinical suspicion of paramyotonia congenita. A. Wrap the limb in a plastic bag, submerge in ice water for about 10–20 minutes to bring skin temperature to 20°C. Remove the patient’s hand from water. The hand should always be removed from the ice water immediately if weakness develops. B. Needle EMG of a distal forearm or hand muscle is performed, noting the presence of abnormal spontaneous activity (e.g., fibrillation potentials, myotonic bursts) and MUAPs with voluntary contraction. C. Allow muscle to rewarm to precooling temperature and continue to record EMG activity (may take >1 hour). 4. Short exercise test is performed if steps 1, 2, and 3 do not yield a definitive diagnosis. A. Immobilize hand. Record supramaximal CMAP at abductor digiti minimi stimulating ulnar nerve at the wrist. B. Record the CMAP once per minute for 5 minutes with the muscle at rest to ensure no decrease in the baseline CMAP.

C. After ensuring a stable baseline, have the patient contract his or her muscle maximally for 5–10 seconds. D. Record the CMAP immediately. If a decrement in amplitude is seen, continue to record the CMAP every 10 seconds until it recovers to baseline (typically 1–2 minutes). E. In cases where a decrement is seen after exercise, repeat the same procedure several times to see if a decrement in the CMAP continues to occur or habituates. 5. Prolonged exercise test is performed if steps 1, 2, 3, and 4 do not yield a definitive diagnosis. A. Immobilize hand. Record supramaximal CMAP at the abductor digiti minimi, stimulating ulnar nerve at the wrist. B. Record the CMAP once per minute for 5 minutes with the muscle at rest to ensure a stable baseline. C. After ensuring a stable baseline, have the patient voluntarily contract his or her muscle maximally for 5 minutes, resting every 15 seconds for 2–3 seconds. D. After the 5 minutes of exercise are complete, have the patient relax completely. E. Record the CMAP immediately, then every 1–2 minutes for 20–40 minutes afterward or until there is no further decline observed in the CMAP (this can go on for >1 hour). Decrement is calculated as follows: (Highest CMAP amplitude after exercise − Smallest CMAP amplitude after exercise) / (Highest CMAP amplitude after exercise × 100). Any amplitude decrement >40% or area decrement > 50% is definitely abnormal. F. Note that immediately after exercise, the CMAP may be larger, before the slow decline in amplitude takes place. This finding is more common when the pre-­exercise rest produces a drop in CMAP, as seen in the periodic paralyses. 6. Repetitive nerve stimulation at 10 Hz.

CMAP, Compound muscle action potential; EMG, electromyography; MUAP, motor unit action potential.

When performing the prolonged exercise test, the decrement can be calculated by comparing the nadir of the CMAP with the baseline value or comparing the nadir with the post-­ exercise peak, which often occurs early in the test. When these two methods have been studied, the peak to nadir method is preferred. This percentage is defined as the [peak – nadir]/ peak × 100. An abnormality is defined as a decrement of >40% of amplitude or >50% of area. Amplitude or area can be used; there is no advantage to one over another. In patients in whom the pretest probability of having one of the periodic paralyses is 50% or less, an abnormal test raises the posttest probability that the patient truly has the disorder to over 95%. In the rare situation where the pretest probability is very high (>90%), then more liberal cutoffs of decrements, such as a decrement of >25% of amplitude or >35% of area, can be used. 

REPETITIVE NERVE STIMULATION Many of the same findings on exercise testing can also be found with RNS. Decrements are not uncommon with RNS in the myotonic syndromes. Although decrements may be seen with slow repetitive stimulation (3 Hz), they are more common with faster frequencies, typically 10 Hz. Abnormalities are not seen in all patients, although when present, they may suggest a specific syndrome.

When all the available electrophysiologic techniques are used, the correct diagnosis usually can be determined by answering several key questions (Table 39.2):    1. Are routine nerve conduction studies normal? 2. On concentric needle EMG: A. Are myotonic discharges present on needle EMG, and, if present, are they widespread or focal? If focal, what is the distribution, proximal or distal? B. Are the MUAPs and recruitment pattern on EMG examination normal or abnormal? If the MUAPs and recruitment pattern are abnormal, are they myopathic or neurogenic? 3. Is there an effect of muscle cooling on the needle examination? 4. What does short exercise testing show? 5. What does prolonged exercise testing show? 6. What does RNS show? 

DYSTROPHIC MYOTONIC MUSCLE DISORDERS Myotonic Dystrophy The myotonic dystrophies are among the most common of the myotonic muscle disorders. They are an autosomal dominant

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 697 

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Fig. 39.2  Short exercise test in the myotonic syndromes.  After a brief maximal voluntary contraction, the compound muscle action potential (CMAP) immediately decrements in the myotonic syndromes. If subsequent CMAPs are evoked every 10 seconds, the decrement recovers to baseline in 1–2 minutes in myotonic dystrophy and myotonia congenita (top). Numbers on the left refer to the time in seconds measured after the exercise. In paramyotonia congenita, the recovery may be quite delayed, in the range of 10–60 minutes. (From Streib EW. AAEE minimonograph, no. 27: differential diagnosis of myotonic syndromes. Muscle Nerve. 1987;10:606. With permission.)

inherited, multisystem disorder characterized by progressive facial and limb muscle weakness, myotonia, and involvement of several organ systems outside of skeletal muscle. Also known as Steinert disease, myotonic dystrophy type 1 (DM1) is the most common; it is due to a defect in the protein kinase myotonin (dystrophia myotonica-­protein kinase [DMPK]) gene on chromosome 19q. The gene defect itself is an unstable expansion of a CTG trinucleotide repeat in the untranslated region of the myotonin gene. Age of onset and severity of symptoms are variable and proportional to the size of the abnormal CTG trinucleotide repeats, which expands over subsequent generations. This phenomenon of “anticipation” results in an earlier onset and more severe course in subsequent generations. Myotonic dystrophy type 2 (DM2), also known as proximal myotonic myopathy (PROMM syndrome) and proximal myotonic dystrophy, is due to a defect in the CNBP (cellular nucleic acid–binding protein) gene (formerly known as ZNF9, or zinc finger protein 9) on chromosome 3q. The gene defect itself is an unstable expansion of a CCTG repeat in intron 1 of the CNBP gene. Myotonic Dystrophy Type 1 Clinical Patients with DM1 generally present in their late teens with mild distal weakness and delayed muscle relaxation, such as difficulty releasing their hand grip. This disorder is distinguished from other muscle disorders by the distal rather than proximal predominance of weakness, as well as the myotonia. The myotonia is less marked than in the myotonia congenitas. In classic myotonic dystrophy, patients experience stiffness that improves with repeated contractions. Thus, patients often report that repeated opening and closing of the hand results in a faster relaxation time with each grip. As the weakness progresses over years, the myotonic symptoms generally recede.

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There is a distinctive clinical appearance characterized by bifacial weakness, temporal wasting, and frontal balding, resulting in a narrow, elongated face and horizontal smile, with ptosis, and distal muscle wasting and weakness (Fig. 39.4). Patients with a smaller CTG trinucleotide repeat may not have the typical facial appearance. Weakness of neck flexion is also an early sign, and patients may notice difficulty lifting their head off the pillow or a tendency for the head to fall backwards during acceleration. DM1 is distinguished from many of the other myotonic disorders by the progressive distal weakness as well as involvement of several organ systems outside of skeletal muscle resulting in cataracts, cardiac conduction and pulmonary defects, endocrine dysfunction, testicular atrophy, hypersomnia, gynecologic problems, and, in some patients, mild to moderate cognitive impairment. As in the other myotonic and periodic paralysis syndromes, patients with myotonic dystrophy should be warned against potential anesthetic complications of succinylcholine and anticholinesterase agents. The clinical examination in a patient suspected of having myotonic dystrophy is directed at recognition of the typical facies; demonstration of bifacial, neck flexor, and distal wasting and weakness; and demonstration of grip and percussion myotonia. Percussion myotonia can generally be

Table 39.2  Electrophysiologic Testing in Myotonic and Periodic Paralysis Disorders.

Test

Myotonic Dystrophy, Type 1

Myotonic Dystrophy, Type 2

Myotonia Congenita: Dominant

Myotonia Congenita: Recessive

Sodium Channel Myotonia

Paramyotonia Congenita

Hyperkalemic Periodic Paralysis

Hypokalemic Periodic Paralysis

Andersen–Tawil Syndrome

Nerve conduction studies

Normal or decreased distal CMAPs

Normal

Normal

Normal

Normal

Normal

Normal between attacks; decreased CMAP amplitude during attack of weakness

Normal between attacks; decreased CMAP amplitude during attack of weakness

Normal

EMG myotonia

++D >P

++D >P (upper extremity) D = P (lower extremity)

+++P and D

+++P and D

++P and D

++P and D

++P and D, especially during attack

No myotonia

No myotonia

EMG MUAPs

Myopathic D

Myopathic P

Normal

Usually NL, ±myopathic

Normal

Normal

Myopathic late in course

Myopathic late in course

Normal

Muscle No effect cooling (20°C) on electromyography

Unknown

May lead to increased duration of myotonic bursts; easier to elicit

No effect

Unknown

Transient dense fibrillation potentials that disappear below 28°C; myotonic bursts disappear below 20°C electrical silence, long-­lasting muscle contracture at 20°C

No effect

No effect

No effect

Short exercise

Drop in CMAP amplitude; quick recovery over 2 minutes; drop is smaller or does not persist on subsequent trials

Not well documented

Variable drop in CMAP amplitude; quick recovery over 2 minutes

Large drop in CMAP amplitude; delay in recovery may become progressive over time

Unknown

Normal or small increment in a warm muscle; marked drop in CMAP amplitude and very slow recovery over 1 hour in cooled muscle

No effect or transient increase in CMAP amplitude during an attack of weakness

No effect or tranNo effect sient increase in CMAP amplitude during an attack of weakness

Prolonged exercise

Small decrement immediately after exercise, with recovery over 3 minutes

Unknown

Unknown

Small decrement immediately after exercise, with recovery over 3 minutes

Unknown

Moderate decrement immediately after exercise, maximal at 3 minutes, with slow recovery over 1 hour in cooled muscle

Most with initial increase in CMAP amplitude (∼35%); progressive drop in CMAP amplitude (∼50%) over 20–40 minutes with slow recovery over 1 hour

Most with initial increase in CMAP amplitude (∼35%); progressive drop in CMAP amplitude (∼50%) over 20–40 minutes with slow recovery over 1 hour

Most with initial increase in CMAP amplitude (∼35%); progressive drop in CMAP amplitude (∼50%) over 20–40 minutes with slow recovery over 1 hour

10 Hz RNS

Decrement

Not well documented

Decrement

Large decrement

Not documented

Normal

Normal

Normal

Normal

CMAP, Compound muscle action potential; CRD, complex repetitive discharge; D, distal; EMG, electromyogram; MUAP, motor unit action potential; NL, normal; P, proximal; RNS, repetitive nerve stimulation.

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 699

Fig. 39.4  Typical facies in myotonic dystrophy.  Note frontal balding, ptosis, temporal wasting, elongated face, horizontal smile. (Reprinted with permission from Brooke MH. A Clinician’s View of Neuromuscular Disease. Baltimore, MD: Williams & Wilkins; 1986.)

elicited most easily over the thenar muscles and long finger extensors. Eyelid myotonia is not seen. Deep tendon reflexes often are reduced or absent in the lower extremities as the disease progresses. Slit lamp examination reveals posterior capsular cataracts, which early on have a characteristic multicolored pattern. Approximately 10% of cases are congenital, characterized by severe weakness and hypotonia at birth and intellectual disability. Children with the congenital form are floppy at birth, have a typical tented upper lip with poor sucking and swallowing, and often have contractures. Surprisingly, clinical myotonia is not present the first year of life. The congenital form nearly always is maternally inherited. In many cases, the mother may be so minimally affected that her diagnosis is not made until the infant is born with severe hypotonia and a myopathic facies. Creatine kinase (CK) levels may be mildly to moderately elevated. Muscle biopsy typically reveals a mild increase in connective tissue, increased variation in fiber size, predominant atrophy of type I muscle fibers, an increase in central nuclei, ring fibers, and occasional small angulated fibers. The clinical severity of DM1 is directly related to the number of CTG repeats. In normals, the number varies between 5 and 37, whereas in patients with DM1, the number of CTG repeats may range into the thousands. In individuals with a very small increase in the number of repeats (50–100), fewer than half of these people are symptomatic, and most have cataracts only. Symptoms and signs of DM1 are more typically present in individuals with over 100 repeats.  Electrophysiologic Evaluation The electrophysiologic evaluation of DM1 (Table 39.2) consists of routine nerve conduction studies, EMG, muscle cooling, and exercise testing.   

1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. A mild neuropathy has been described, perhaps secondary to the accompanying endocrine changes. Low CMAP amplitudes may be noted secondary to the distal myopathy in patients with severe disease. 2. Concentric needle EMG of at least one upper and one lower extremity should be performed, in addition to sampling facial and paraspinal muscles. Most but not all patients with DM1 will demonstrate myotonic discharges on EMG. In very mild cases (e.g., in patients with a small increase in the number of repeats), myotonic discharges may be difficult to find. Otherwise, myotonic discharges are generally most prominent in the distal hand, forearm extensor, foot dorsiflexor (tibialis anterior), and facial muscles but usually are not found in proximal muscles. The distribution of myotonic discharges follows the same pattern as the weakness. Myotonic discharges in DM1 consist of the classic waxing and waning muscle fiber action potentials (Fig. 39.5A). MUAP analysis may be difficult because of the myotonic discharges provoked by needle insertion or muscle contraction. However, careful examination reveals myopathic (low amplitude, short duration, polyphasic) MUAPs with early recruitment, which are generally noted in the forearm extensor and tibialis anterior muscles, consistent with the distal predominant weakness on clinical examination. Late in the course of DM1, MUAPs may become large and long. 3. Muscle cooling to 20°C has no appreciable effect on the EMG examination. 4. The short exercise test produces a drop in the CMAP amplitude immediately after exercise. If the CMAP then is recorded every 10 seconds up to 2 minutes, it recovers to baseline. If short exercise is repeated, the decremental response habituates after one or two cycles, with no further decrement in the CMAP occurring immediately after exercise. 5. RNS at 10 Hz produces a decrement similar to the short exercise test.    When electrophysiologic testing is completed, one has established the presence of myotonia with myopathic MUAPs on the needle examination, with a distal and facial muscle predominance. There is no effect of muscle cooling. The short exercise test demonstrates a decrement that recovers over 1–2 minutes and habituates with further cycles. This pattern of abnormalities strongly suggests the diagnosis of DM1. Note that when a patient presents with typical signs and symptoms of myotonic muscular dystrophy, muscle cooling, exercise testing, and RNS are not necessarily done on a routine basis but may be helpful in some clinical situations, when the diagnosis is still in question after standard nerve conduction studies and EMG needle examination are completed. 

700

SECTION VIII   Clinical Disorders —9 PV

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% Fig. 39.5  Myotonic discharges.  (A) Two-­second myotonic discharge in a patient with myotonic dystrophy type 1 showing typical waxing and waning frequency and amplitude; maximal frequency about 60 Hz, minimal frequency about 8 Hz. (B) Four-­second myotonic discharge (two successive oscilloscope sweeps) in a patient with myotonic dystrophy type 2 in which frequency and amplitude gradually decline with no waxing component; maximal frequency toward onset about 23 Hz, minimal frequency toward termination about 19 Hz. (With permission from Logigian EL, Ciafaloni E, Quinn LC, et al. Severity, type, and distribution of myotonic discharges are different in type 1 and type 2 myotonic dystrophy. Muscle Nerve. 2007;35:479–485.)

Myotonic Dystrophy Type 2 Clinical DM2 has many features in common with DM1. Like DM1, it is an autosomal dominant inherited muscle disorder recognized by a constellation of signs, including bifacial weakness, ptosis, progressive weakness, myotonia, and involvement of several organ systems outside of skeletal muscle. Patients typically present after the age of 40 with progressive weakness. Unlike myotonic dystrophy, however, the weakness involves predominantly proximal, as opposed to distal, muscles. The pattern of weakness typically involves the hip flexors and extensors, neck flexors, elbow extensors, and finger and thumb flexors. Anticipation is generally not seen between generations of affected family members. Like DM1, the multisystem involvement may include posterior capsular cataracts, frontal balding, testicular atrophy, and cardiac conduction defects. However, central nervous system involvement does not occur or is much less common. Patients are recognized by their presentation of proximal greater than distal weakness, with mild bifacial weakness and ptosis in the setting of grip and percussion myotonia. Many patients have a peculiar intermittent pain syndrome in the thighs, arms, or back. CK may be mildly to moderately elevated, and the muscle biopsy reveals a nonspecific myopathic pattern, including increased variation in fiber size, small angulated fibers, pyknotic nuclear clumps, predominant atrophy of type II muscle fibers, and increased central nuclei. Rare cases of isolated elevated CK (“hyper-­CKemia”) without other clinical or electrical abnormalities have been reported in DM2.  Electrophysiologic Evaluation See Table 39.2.    1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. 2. Concentric needle EMG of at least one upper and one lower extremity and paraspinal muscles should

be performed. In contrast to DM1, the myotonic discharges seen in DM2 tend to be predominantly waning potentials (Fig. 39.5B). These potentials are less specific than the classic waxing and waning discharges typically associated with myotonia. The distribution of the myotonic discharges in the upper extremities in DM2 is surprisingly more predominant in the distal than in the proximal muscles, similar to DM1. In the lower extremities, however, the pattern is different. Although myotonic discharges are present in distal muscles (e.g., the tibialis anterior), the number of myotonic discharges is approximately the same in distal and proximal muscles (e.g., tensor fascia lata). Thus the presence of myotonic discharges in the proximal lower extremity muscles is much more common in DM2 than DM1. Similar to DM1, the absence of myotonic discharges does not exclude the diagnosis of DM2. Complex repetitive discharges are noted occasionally. MUAP analysis reveals myopathic (low amplitude, short duration, polyphasic) MUAPs with early recruitment, which are generally noted in the proximal lower extremity muscles.   Once the nerve conduction studies and EMG are completed, the presence of myotonia with myopathic MUAPs has been established on needle examination, present primarily in proximal muscles of the lower extremity, and distal muscles of both the upper and lower extremities. Few disorders associated with myotonia have a proximal predominance with myopathic MUAPs. Rarely, prominent myotonic discharges, complex repetitive discharges, and myopathic MUAPs are noted in the very proximal muscles of patients with adult-­ onset acid maltase deficiency. In this disorder, however, the myotonic discharges are generally restricted to the paraspinal muscles. Myotonic discharges also may be seen in some patients with polymyositis, in whom abnormal spontaneous activity and MUAP changes are more prominent proximally. However, myotonic discharges are only infrequently seen in polymyositis. In the myotonia

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 701

congenitas, myotonic discharges are noted mostly in proximal muscles as well, but with rare exception (i.e., some cases of recessive generalized myotonia congenita), there are no myopathic MUAP changes. 3. The effects of muscle cooling and the short and prolonged exercise tests have not been well described for this disorder. Short exercise testing in one patient personally examined by the authors revealed no drop in the CMAP amplitude recording from a distal hand muscle. This negative finding may reflect the proximal predominance of weakness. 

NONDYSTROPHIC MYOTONIC MUSCLE DISORDERS AND PERIODIC PARALYSIS SYNDROMES Myotonia Congenita Myotonia congenita is distinguished from the dystrophic muscle disorders by the lack of weakness in most patients and by the absence of extramuscular abnormalities. Two forms of myotonia congenita have classically been recognized. An autosomal dominant form, Thomsen disease, was first described in 1876 by Julius Thomsen, who was himself affected. Thomsen noted the great variability among his own affected family members; it was barely apparent in his mother and uncle, but very severe in his younger brother and sister. Muscular hypertrophy is common. An autosomal recessive form of generalized myotonia congenita was first described by Becker. The recessive form is characterized by later onset, marked myotonia, and muscular hypertrophy. Late in the course, there may be minor weakness and atrophy of the forearm and neck muscles, although it is still considered a nondystrophic syndrome. Some patients with recessive myotonia congenita also experience transient attacks of weakness that are relieved with exercise. Both the recessive and dominant forms of myotonia congenita arise from a skeletal muscle chloride channel-­1 (CLCN) gene defect on chromosome 7q. Other myotonia congenita phenotypes have also seen described, but with mutations in the muscle sodium α-­ subunit (SCN4A) gene on chromosome 17. These atypical myotonia congenitas include potassium-­ aggravated myotonia (PAM), myotonia permanens, myotonia fluctuans, and acetazolamide responsive myotonia. This is the same sodium channel gene with mutations that result in hyperkalemic periodic paralysis, paramyotonia congenita, and rare cases of hypokalemic periodic paralysis. These atypical myotonia congenitas are discussed later with the periodic paralyses and paramyotonia congenita disorders to which they are more closely related. Clinical Onset of the dominant form is generally in infancy or early childhood; onset of the recessive form is usually later in childhood. Patients generally present with painless myotonia resulting in muscle stiffness that is nonprogressive. Muscle hypertrophy is common, secondary

to the almost constant state of muscle contraction. The stiffness worsens after rest or with cold and diminishes with exercise. The myotonia may also be exacerbated by hunger, secondary to emotional upset, and during pregnancy. Patients typically describe a warm-­up period, during which they can work through the muscle stiffness. For example, it is not uncommon for a patient to describe difficulty rising from a chair after sitting for a few minutes or difficulty climbing up the first few steps of a stairway, which then improves. In the autosomal dominant form, muscle hypertrophy is often noted in the proximal arms, thighs, and calves. Grip and percussion myotonia are easily elicited. CK levels may be slightly elevated in the dominant form and moderately elevated in the recessive form. Muscle biopsy may show a lack of type IIB fibers in both forms of inheritance.  Electrophysiologic Examination See Table 39.2.    1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. 2. Concentric needle EMG of at least one upper and one lower extremity and paraspinal muscles generally shows widespread myotonic discharges, which are easily elicited with minimal needle movement or muscle contraction in proximal and distal muscles. In the dominant form, the MUAPs and recruitment pattern are normal. In the recessive form, there may be mildly myopathic MUAPs with early recruitment. Muscle cooling to 20°C in the dominant form may produce myotonic bursts of longer duration that may be more easily elicited than at room temperature. 3. The short exercise test in the dominant form produces a variable drop in CMAP amplitude immediately after exercise, which recovers over 1–2 minutes with repeated recording of the CMAP every 10 seconds. In the recessive form, the initial drop in amplitude often is profound with a delay in recovery that may become progressive over time (Fig. 39.2). Muscle cooling has no appreciable effect on the exercise test. This is unlike paramyotonia congenita (see section on Paramyotonia Congenita), in which a decremental response recovers very slowly over many minutes if the muscle is cooled. 4. RNS at 10 Hz may result in large decrements (often greater than 40%) in two-­thirds of patients with recessive myotonia congenita, in contrast to only onethird that demonstrate a decrement using the short exercise test. Thus RNS may be a useful adjunct in the evaluation of patients with recessive myotonia congenita.    The electrodiagnosis of myotonia congenita is based on the presence of widespread myotonic discharges with normal MUAPs and recruitment pattern on needle examination.

702

SECTION VIII   Clinical Disorders

The responses to muscle cooling, the short exercise test, and RNS can then be used to differentiate it from paramyotonia congenita. 

Paramyotonia Congenita, Hyperkalemic Periodic Paralysis, and Sodium Channel Myotonia Congenita Paramyotonia congenita, hyperkalemic periodic paralysis, and sodium channel myotonia are associated with distinct mutations of the voltage-­gated sodium channel α-­subunit (SCN4A) gene on chromosome 17q. Each of these conditions is inherited in an autosomal dominant fashion. Clinical Patients with paramyotonia congenita and hyperkalemic periodic paralysis experience attacks of weakness; patients with sodium channel myotonia congenita do not experience weakness. Paramyotonia Congenita Paramyotonia congenita was first described by Eulenburg in 1886. Patients present in infancy with muscle stiffness that primarily affects the bulbofacial, neck, and hand muscles. In paramyotonia, muscle stiffness is brought on by repeated muscle contraction or exercise, as opposed to myotonia, in which a warm-­up period of repeated muscle contraction alleviates the muscle stiffness. Thus, the designation is paradoxical, or paramyotonia. Muscle stiffness also is triggered by exposure to cold. In most patients, cold induces attacks of stiffness followed by true weakness, especially during prolonged exercise in cold temperatures. It may take hours to regain strength despite warming. The first signs often occur when the infant is noted to have prolonged eye closure after crying or sleeping near a fan or after having his or her face washed with cool water. Patients often are very muscular.  Hyperkalemic Periodic Paralysis Patients with hyperkalemic periodic paralysis present in early childhood with attacks of periodic weakness that are provoked by rest after exercise, fasting, emotional stress, cold, and potassium loading. Weakness commonly occurs in the morning after awakening from sleep. Some patients can forestall an impending attack with mild exercise. Attacks of weakness usually are brief, lasting from minutes to hours, and generally are accompanied by hyporeflexia. Rare patients experience prolonged attacks of weakness. Weakness usually is generalized but spares the facial and respiratory muscles. The potassium level usually is elevated during attacks, although in some patients, it is normal. Symptoms are relieved by ingesting carbohydrates or inhaling a β-­adrenergic agent. Myotonia, if present, can be variable. In some patients, the myotonia is detected only on EMG testing, whereas in others, myotonia is elicited on physical examination. The frequency of attacks generally lessens in middle age, and some patients develop fixed progressive proximal weakness in adulthood. 

Sodium Channel Myotonia Congenita Patients with sodium channel myotonia congenita, also known as potassium-­aggravated myotonia (PAM), present with episodes of generalized stiffness secondary to myotonia. The disorder is quite potassium sensitive, with worsening of symptoms by potassium ingestion but in most patients no worsening with cold. These patients do not experience true episodic weakness. The myotonia may be painful and has a peculiar feature in that it is exercise induced, with a delay in the onset of the myotonia for several minutes after exercise. Several variants with various names, depending on the severity and quality of the fluctuating stiffness and its response to treatment, have been described. All are inherited in an autosomal dominant fashion. These variants include myotonia fluctuans, myotonia permanens, and acetazolamide-­ responsive myotonia. Myotonia permanens is the most severe, often associated with continuous myotonic discharges on EMG. In some reported cases, retarded growth and dysmorphic facial features have been noted.  Electrophysiologic Examination See Table 39.2. Paramyotonia Congenita 1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. 2. Concentric needle EMG of at least one upper and one lower extremity and paraspinal muscles generally shows easily elicited myotonic discharges in proximal and distal muscles, although not as easily elicited as in the myotonia congenitas. The myotonia may be more prominent in distal muscles. The MUAPs are normal in amplitude and duration with a normal pattern of recruitment. Once the presence of myotonia has been established on needle examination, with normal MUAPs and recruitment pattern, muscle cooling and exercise testing may be helpful. 3. Muscle cooling to 20°C may have a profound effect on the needle EMG, which is pathognomonic for this disorder. Transient dense fibrillation potentials appear with cooling and eventually disappear below 28°C. As the muscle cools down further, all myotonic discharges completely disappear below 20°C, giving way to paralysis of the muscle. At this point, the muscle is inexcitable to electrical or mechanical stimulation as the muscle goes into a long-­lasting, electrically silent contracture. This state may last over an hour after the muscle is warmed to room temperature. Note that the patient must be watched carefully, and the hand should always be removed from the ice water immediately if weakness develops. 4. RNS at 10 Hz results in no decrement. 5. The short exercise test results in no decrement and in some cases a slight increment when the muscle is warm at room temperature. However, with the muscle cooled,

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 703 %DVHOLQH

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. The short exercise test produces no decrement. 4 5. The prolonged exercise test often produces an immediate increase in the CMAP amplitude, especially if the initial amplitude is low. This is followed, however, by a progressive drop in the CMAP amplitude by about 50% over 20–40 minutes, with most of the decline occurring in the first 20 minutes (Fig. 39.3). It should be noted that a similar decline in the CMAP may be noted by simply immobilizing the muscle without exercise. If there is a decline in the CMAP with rest, then exercise may produce a brief increment in the CMAP. 

   

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7LPHPLQ Fig. 39.6  Typical response on the short exercise test in paramyotonia congenita.  After a brief maximal voluntary contraction, the compound muscle action potential immediately decrements in the myotonic syndromes. In paramyotonia congenita, the recovery may be quite delayed, in the range of 10–60 minutes, especially if the muscle is cooled, compared with myotonic dystrophy or myotonia congenita, in which the repair occurs over 1–2 minutes. (From Streib EW. AAEE minimonograph, no. 27: differential diagnosis of myotonic syndromes. Muscle Nerve. 1987;10:603. With permission.)

the short exercise may produce a large drop in CMAP amplitude that shows a marked delay in recovery to the baseline CMAP amplitude with repeated recording of the CMAP up to 1 hour (Fig. 39.6). This is unlike myotonic dystrophy or the chloride channel myotonia congenitas, in which the drop in CMAP amplitude recovers to baseline over 1–2 minutes; though in recessive myotonia congenita, the delay in recovery may become progressive over time.  Hyperkalemic Periodic Paralysis 1. As a rule, routine motor and sensory nerve conduction studies are normal if performed between attacks of weakness. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity suffice. During an attack of weakness, the CMAP amplitudes may decline proportionally to the degree of weakness. 2. Concentric needle EMG of at least one upper and one lower extremity and paraspinal muscles between attacks may be normal in amplitude and duration with a normal pattern of recruitment, but in some patients, myopathic MUAPs may be found. In patients with hyperkalemic periodic paralysis with myotonia, myotonic discharges may either increase or appear for the first time during an attack of weakness in patients whose baseline EMG does not show myotonic discharges. Myotonic discharges are seen early in the attack but then disappear as weakness progresses. During an attack of weakness, there is a reduction in the size and number of MUAPs recruited in weak muscles. 3. Muscle cooling has no appreciable effect on the needle EMG findings. Once the presence of myotonia has been established on needle examination, with normal or myopathic MUAPs, the next step is exercise testing.

Sodium Channel Myotonia Congenita 1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. 2. Concentric needle EMG examination of at least one upper and one lower extremity and paraspinal muscles generally shows myotonic discharges, which are elicited in proximal and distal muscles. The MUAPs are normal in amplitude and duration with normal recruitment. 3. The effects of muscle cooling, short and prolonged exercise testing, and repetitive stimulation are not well documented. 

Hypokalemic Periodic Paralysis Hypokalemic periodic paralysis is not a myotonic disorder. However, the clinical features of periodic attacks of flaccid weakness and the development of fixed proximal weakness later in life resemble the sodium channel disorders discussed earlier. This is an autosomal dominant inherited disorder associated with a defect in the α subunit of a voltage-­sensitive muscle calcium channel (CACNA1S) gene on chromosome 1q (hypokalemic periodic paralysis type 1) in approximately 60% of families. Mutations have also been identified in the α subunit of the sodium channel gene (SCN4A) on chromosome 17q in 20% of families, and the term hypokalemic periodic paralysis type 2 is used to designate this group of patients. Both types result from missense mutations in the voltage-­sensor domains of their respective channel. This similarity suggests a common functional defect produced by these voltage-­sensor mutations and may explain why different mutations on two different channels result in hypokalemic periodic paralysis. At least 20% of cases remain genetically undetermined. Clinical Patients with hypokalemic periodic paralysis present in their teenage years (some earlier) with attacks of periodic weakness. Attacks are provoked by cold, carbohydrate ingestion, alcohol, emotional stress, and rest after exercise. Some patients can forestall an impending attack with mild exercise. Attacks of weakness may be quite prolonged, generally occurring on awakening from sleep and rarely involving respiratory muscles. Weakness often is accompanied by hyporeflexia. The

704

SECTION VIII   Clinical Disorders

potassium level usually is low during attacks, although in some cases it is normal. Myotonia is not present either clinically or with EMG testing, except in extremely rare patients with a sodium channel mutation. Attacks are more frequent in males than females, especially in those families with calcium channel mutations. It is not uncommon for females with calcium channel mutations to be so minimally affected or completely unaffected by periodic weakness that they are unaware that they have the disorder. All patients, however, invariably develop progressive proximal weakness during adulthood, whether or not they have had attacks of periodic paralysis. Muscle biopsy shows a vacuolar myopathy. Approximately 50% of patients with calcium channel mutations respond to acetazolamide (Diamox), which can be ineffective or even harmful in some patients with sodium channel mutations.  Electrophysiologic Examination See Table 39.2.    1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. During an attack of weakness, the CMAP amplitudes generally decline proportionally to the degree of weakness. 2. Concentric needle EMG findings of at least one upper and one lower extremity and paraspinal muscles should show no myotonic discharges. The MUAPs and recruitment pattern are generally normal in the early stages of the disorder. As in hyperkalemic periodic paralysis, however, there is a reduction in the size and number of MUAPs recruited in weak muscles during a paralytic attack. As patients develop fixed proximal weakness, myopathic MUAPs with early recruitment are noted in proximal muscles. We studied one elderly female patient in the later stages of the disorder with fixed proximal weakness who had large, prolonged MUAPs with reduced recruitment in proximal more than distal muscles. Thus, in very chronic myopathies, the EMG changes may resemble those of chronic neurogenic disorders. 3. Muscle cooling has no appreciable effect on the needle EMG findings. 4. The short exercise test produces no decrement. 5. The prolonged exercise test often produces an immediate increase in the CMAP amplitude, especially if the initial amplitude is low. This is followed, however, by a progressive drop in the CMAP amplitude by about 50% over 20–40 minutes, with most of the decline occurring in the first 20 minutes. It should be noted that a similar decline in the CMAP may be noted just by immobilizing the muscle without exercise. If there is a decline in the CMAP with rest, exercise may produce a brief increment in the CMAP. 

Andersen-­Tawil Syndrome Andersen-­Tawil syndrome (ATS) is characterized by a clinical triad of periodic paralysis, cardiac abnormalities, and

characteristic facial and skeletal features. This is an autosomal dominant inherited disorder associated in approximately 60% of families with mutations in the Kir2.1 subunit of the inward rectifying potassium channel (KCNJ2) gene on chromosome 17q, resulting in dysfunctional inward rectifier potassium channels. Genetic heterogeneity is likely, as no mutations in Kir2.1 have been found in 40% of families with ATS. These families may have mutations in other genes that regulate Kir2.1, or entirely different mutations. Clinical Patients present in childhood or adolescence, with some or all features of the clinical triad of periodic paralysis, cardiac abnormalities (ventricular arrhythmias, prolonged QT interval, prominent U waves), and distinctive physical features. Characteristic physical features include short stature, high arched palate, low-­set ears, broad nose, micrognathia, hypertelorism, scoliosis, clinodactyly of the fifth finger, short index finger, and syndactyly of the toes (Fig. 39.7). Some patients may have minor neurocognitive deficits, among them difficulties with complex problem-­solving, attention and concentration, and solving abstract problems. Neurologic examination between paralytic attacks may reveal generalized limb and

Fig. 39.7  Characteristic facial features in Andersen-­Tawil syndrome.  Note low-­set ears, broad nose, and hypertelorism. (Reprinted with permission from Sansone V, Griggs RC, Meola G, et al. Andersen’s syndrome: a distinct periodic paralysis. Ann Neurol. 1997;42: 305–312.)

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 705

neck flexor weakness. There is no associated grip or percussion myotonia. Paralytic attacks may occur spontaneously or may be triggered by rest after exercise or alcohol. Some patients report intermittent muscle pain without attacks of weakness. In patients with the KCNJ2 mutation, paralysis will be accompanied by hyperkalemia in approximately 15% of patients, normokalemia in approximately 20% of patients, and hypokalemia in approximately 65% of patients. As with other types of periodic paralysis, some patients can work through the muscle pain by continuing with mild exercise. Prolonged QT interval is the most consistent cardiac manifestation, present in about 80% of patients, and may be the only finding in some individuals from a family with typical ATS syndrome. In some patients, the long QT interval may be asymptomatic. However, patients may present in childhood with cardiac arrest, with no history of periodic paralysis, although they may experience periodic paralysis in later years. Some patients with periodic paralysis and characteristic facial features do not have a prolonged QT interval at rest, although other electrocardiographic findings may be seen, such as a prominent U wave in the chest leads.  Electrophysiologic Examination See Table 39.2.    1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. During an attack of weakness, the CMAP amplitudes generally decline proportionally to the degree of weakness. 2. Concentric needle EMG findings of at least one upper and one lower extremity and paraspinal muscles should show no myotonic discharges. The MUAPs and recruitment pattern are generally normal. As with the other periodic paralyses, there may be a reduction in the size and number of MUAPs recruited in weak muscles during a paralytic attack. 3. Muscle cooling has no appreciable effect on the needle EMG findings. 4. The short exercise test produces no decrement. 5. The prolonged exercise test often produces an immediate increase in the CMAP amplitude, especially if the initial amplitude is low. This is followed, however, by a progressive drop in the CMAP amplitude by about 50% over 20–40 minutes, with most of the decline occurring in the first 20 minutes. It should be noted that a similar decline in the CMAP may be noted just by immobilizing the muscle without exercise. If there is a decline in the CMAP with rest, exercise may produce a brief increment in the CMAP. 

Schwartz-­Jampel Syndrome (Chondrodystrophic Myotonia) Schwartz-­Jampel syndrome (SJS) is a rare, genetic myotonic-­ like disorder characterized by distinctive physical features, skeletal deformities, and muscle stiffness. The syndrome usually is inherited as an autosomal recessive condition, but in occasional

families, the inheritance pattern suggests an autosomal dominant disorder. SJS was previously divided into types 1 and 2, but SJS type 2 is now considered a more severe, distinct disorder known as Stuve-­Wiedemann syndrome caused by mutations in the leukemia inhibitory factor receptor (LIFR) gene on chromosome 5p. SJS is caused by mutations in the heparin sulfate proteoglycan of basement membrane (HSPG2) gene on chromosome 1p that encodes perlecan. Perlecan is a heparan sulfate proteoglycan present in all basement membranes and is involved in cell adhesion and growth factor signaling. Clinical SJS is subdivided into types 1A and 1B, which are distinguished by severity and age of onset. Type 1A, or the classic form of SJS, is the most commonly recognized type. These individuals develop milder symptoms later in childhood, while those with type 1B have more severe symptoms that manifest immediately after birth. The clinical manifestations may vary among affected members of the same family. Signs and symptoms may include muscle stiffness and weakness, contractures, short stature, short neck, “fixed” facial features including micrognathia, low set ears, pursed lips, prominent eyebrows, and eye abnormalities including upward slanting eyes, blepharophimosis, exotropia, and microcornea (Fig. 39.8). There is often predominantly distal weakness and atrophy, which may be accompanied by prominent proximal upper and lower extremity muscle hypertrophy. In contrast to the pseudohypertrophy seen in dystrophinopathies, proximal limb muscles in SJS are genuinely enlarged. In the literature, there has been controversy whether SJS is a myotonic or neuromyotonic disorder. In mouse models of the disease, the widespread spontaneous discharges can be abolished by curare, which strongly implies that the abnormal discharges are of peripheral nerve origin. In addition, some have shown that the discharges persist immediately after nerve transection but completely disappear when wallerian degeneration has been completed, which also suggests a distal axonal localization of the spontaneous discharges. However, in patients, the current consensus is that SJS is a true myotonic disorder, with patients displaying widespread myotonic discharges on EMG. In some patients, the myotonic discharges do not wax and wane in amplitude and frequency, as seen in most myotonic disorders. Perhaps these discrepancies in EMG findings are due to SJS being a genetically heterogeneous disease.  Electrophysiologic Examination 1. Routine motor and sensory nerve conduction studies are normal as a rule. Generally, one motor and sensory nerve conduction study and F responses in an upper and lower extremity will suffice. 2. Concentric needle EMG findings of at least one upper and one lower extremity and paraspinal muscles generally show continuous discharges. As noted above, these are myotonic discharges, but may not wax and wane as much in amplitude and frequency as in other myotonic disorders. In some cases, complex repetitive discharges are seen. 3. The effects of muscle cooling, short exercise, and prolonged exercise testing are unknown.   

706

SECTION VIII   Clinical Disorders

EXAMPLE CASES Case 39.1 History and Physical Examination

Fig. 39.8  Typical appearance of Schwartz-­Jampel syndrome. Note skeletal and facial anomalies including short neck, small mouth, micrognathia, pursed lips, upward slanting eyes, blepharophimosis, low-­set ears, and prominent eyebrows. Proximal upper and lower extremity muscle hypertrophy and distal predominant generalized weakness and atrophy also are noted. (Reprinted with permission from Spaans F, Theunissen P, Reekers AD, et al. Schwartz-­Jampel syndrome: I. Clinical, electromyographic, and histologic studies. Muscle Nerve. 1990;13:516–527.)

The clinical presentation of SJS is so characteristic that the differential diagnosis is quite limited. The diagnosis is usually established by the combination of characteristic physical features, dwarfism, and stiffness accompanied by muscle enlargement. 

OTHER CONDITIONS ASSOCIATED WITH MYOTONIA AND PERIODIC PARALYSIS

Occasionally, myotonia and periodic paralysis are noted in the clinical and EMG examinations of various other disease states (Box 39.1), including acquired periodic paralyses; various metabolic, inflammatory, and congenital myopathies; and some disorders associated with systemic diseases. Furthermore, certain drugs can either unmask or precipitate myotonia.

A 29-­year-­old man was referred for mild distal weakness and difficulty releasing his hand grip. He first noted difficulty with releasing his grip approximately 10 years ago, especially while shaking hands, driving his car, or using a hammer. Symptoms were not worse in the cold. Family history was notable for the following: his mother had early cataracts, several miscarriages, and very mild distal weakness that began in her late 40s; a maternal aunt had mild diabetes; and a younger sister had similar complaints of occasional muscle stiffness. On examination, the patient’s mental status was unremarkable. On cranial nerve examination, the face was narrow and elongated, with mild bilateral ptosis, bifacial weakness with wasting of the temporalis muscles, and mild frontal balding. Extraocular movements were full. Early cataracts were noted bilaterally. Neck flexors and distal hand and foot muscles were slightly weak. Marked percussion myotonia of the tongue and thenar muscles was noted, with marked hand grip myotonia that improved with repeated contractions. Deep tendon reflexes were depressed in the lower extremities bilaterally, with plantar flexor responses. Sensation and coordination were normal throughout. Laboratory studies were notable for a mildly elevated CK level (three times normal), normal electrolyte levels and thyroid function studies, and normal electrocardiographic findings. 

Summary The history is that of a young man in his late 20s with mild distal weakness and difficulty releasing his hand grip. Neurologic examination is notable for a normal mental status; a long, narrow face with bilateral ptosis, bifacial weakness, temporal wasting, frontal balding, early cataracts, mild neck flexion, and distal weakness; hypoactive reflexes in the lower extremities; and percussion and grip myotonia of distal muscles. The myotonia improves with repeated contractions. In summary, there is clinical evidence of a dystrophic muscle disorder with key features of distal weakness, myotonia, and extramuscular manifestations including cataracts. Family history is notable for maternal diabetes and cataracts. The CK level is mildly elevated. Before proceeding to electrodiagnostic testing, the possibility of a dystrophic myotonic muscle disorder (the most likely diagnosis being DM1, given the distal weakness) should be considered. On nerve conduction studies, the right median, ulnar, and tibial motor and F response studies reveal normal CMAP amplitudes, distal motor latencies, and conduction velocities. The right median, ulnar, and sural sensory studies are normal, which is expected given the normal sensation on clinical examination. The short exercise test, stimulating the wrist and recording from ADM, shows a drop in the CMAP amplitude immediately after exercise

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 707 CASE 39.1  Nerve Conduction Studies.

Nerve Stimulated

Amplitude Motor = mV; Sensory = μV Stimulation Site

Recording Site

RT

LT

Conduction Velocity (m/s)

F-­wave Latency (ms)

NL

RT

NL

RT

56

≥49

28

≤31

≥49 ≥49

31

≤32

58 62

Latency (ms)

NL

RT

LT

LT

Median (m)

Wrist APB Antecubital fossa APB

10.2 10.1

≥4

3.6 8.2

≤4.4

Ulnar (m)

Wrist Below elbow Above elbow

ADM ADM ADM

12.6 12.2 12.1

≥6

2.9 6.9 8.4

≤3.3

Median (s)

Wrist

Index finger

28

≥20

3.2

≤3.5

53

≥50

Ulnar (s)

Wrist

Little finger

24

≥17

2.8

≤3.1

51

≥50

Tibial (m)

Ankle Popliteal fossa

AHB AHB

6.2 5.6

≥4

5.2 12.6

≤5.8

46

≥41

Sural (s)

Calf

Posterior ankle

9

≥6

3.9

≤4.4

47

≥40

LT

NL

Short Exercise Test: Ulnar (m)

Wrist

ADM

Immediate drop in baseline CMAP amplitude by 50% on first trial of exercise, which recovers over 2 minutes. Next trial produces similar results. Third and fourth trials produce no drop in CMAP amplitude after short exercise.

Note: All sensory latencies are peak latencies. All sensory conduction velocities are calculated using onset latencies. The reported F-­wave latency represents the minimum F-­wave latency. ADM, Abductor digiti minimi; AHB, abductor hallucis brevis; APB, Abductor pollicis brevis; CMAP, compound muscle action potential; LT, left; m, motor study; NL, normal; RT, right; s, sensory study.

CASE 39.1  Electromyography Needle Examination. Spontaneous Activity Muscle

Insertional Fibrillation Activity Potentials

Voluntary Motor Unit Action Potentials Configuration

Fasciculation Potentials

Activation

Recruitment

Duration

Amplitude

Polyphasia

Right first dorsal interosseous

Myo

0

0

NL

Early

−1

−1

+1

Right abductor pollicis brevis

Myo

0

0

NL

Early

−1

−1

+1

Right extensor digitorum communis

Myo

0

0

NL

NL

NL

NL

NL

Right biceps brachii

NL

0

0

NL

NL

NL

NL

NL

Right medial deltoid

NL

0

0

NL

NL

NL

NL

NL

Right C7 paraspinal

NL

0

0

NL

NL

NL

NL

NL

Right C8 paraspinal

NL

0

0

NL

NL

NL

NL

NL

Right tibialis anterior

Myo

0

0

NL

Early

−1

−1

NL

Right medial gastrocnemius

NL

0

0

NL

NL

NL

NL

NL

Right vastus lateralis

NL

0

0

NL

NL

NL

NL

NL

Muscle cooling to 20°C: No effect on needle EMG. EMG, Electromyography; Myo, myotonic discharges; NL, normal.

708

SECTION VIII   Clinical Disorders

that recovers after 2 minutes. After the third trial of short exercise, the immediate drop in amplitude is no longer noted. This pattern is different from paramyotonia congenita, in which the drop in CMAP amplitude may persist but recovers slowly over 1 hour, especially in a cooled muscle. On needle EMG study, myotonic discharges are noted in the right distal hand, extensor forearm, and tibialis anterior muscles but not in the more proximal and paraspinal muscles. MUAPs in distal muscles are brief in duration and low in amplitude, with an early recruitment pattern. These findings are characteristic of a dystrophic myotonic muscle disorder. No effect of muscle cooling is seen. We now are ready to formulate our electrophysiologic impression. IMPRESSION: The electrophysiologic findings are consistent with a myopathy with myotonic features and a distal predominance, as seen in myotonic dystrophy type 1. The history, physical examination, and laboratory studies are consistent with myotonic dystrophy. The electrodiagnostic studies show the presence of myotonic discharges with a distal predominance, in the context of myopathic MUAPs and early recruitment, consistent with DM1. This patient was seen in consultation with an ophthalmologist, who confirmed the presence of posterior subcapsular cataracts. DNA testing confirmed the presence of an abnormal expansion of the CTG repeat in the DMPK gene on chromosome 19q in the patient, his sister, and his mother. The repeat expansion was slightly larger in the patient than in his mother, likely accounting for the earlier onset and greater severity of symptoms. 

Case 39.2 History and Physical Examination A 35-­year-­old woman was referred for generalized muscle stiffness first noted around age 5 years. The stiffness was worse after rest or in the cold and improved with activity such as after walking a few steps. Family history was notable for her father and one brother having similar symptoms. A paternal aunt and several first cousins had similar symptoms. On examination, her mental status was unremarkable. On cranial nerve examination, the face was notable for fairly prominent masseter muscles. There was no bulbofacial weakness or ptosis. Forceful eye closure produced a lid lag. The muscles were very well developed throughout, especially in the proximal arms, thighs, and calves, with good muscle strength in the neck and upper and lower extremities bilaterally. Marked percussion and hand grip myotonia were apparent but diminished after a few contractions. Deep tendon reflexes were normal throughout, with flexor plantar responses. Sensation and coordination were normal throughout. Laboratory study findings were notable for a normal CK level, electrolyte levels, and thyroid function studies. 

Summary The history is that of a woman who presents with generalized muscle stiffness exacerbated by cold and relieved with repeated muscle contractions, dating back to early childhood. The neurologic examination reveals no weakness, but eyelid, percussion, and grip myotonia and well-­developed musculature are obvious. There is a strong family history of similarly affected family members, with an autosomal dominant pattern of inheritance. In summary, there is evidence of myotonia and large muscles in the absence of weakness or extramuscular manifestations. Therefore, before proceeding to electrodiagnostic testing, the possibility of a myotonic muscle disorder without dystrophic changes should be considered. On nerve conduction studies, the left median, ulnar, and tibial motor and F response studies reveal normal CMAP amplitudes, distal motor latencies, and conduction velocities. The left median, ulnar, and sural sensory studies are normal, which is expected given the clinical examination. The short exercise test, stimulating the wrist and recording from ADM, shows a drop in the CMAP amplitude immediately after exercise that recovers after 1–2 minutes. This pattern is seen in myotonic dystrophy and myotonia congenita, although some cases of recessive myotonia congenita may show a delay in recovery that becomes progressive over time. In paramyotonia congenita, the drop in amplitude recovers slowly over an hour, especially in a cooled muscle. On needle EMG, myotonic discharges are noted diffusely in the proximal and distal muscles of the left upper and lower extremities, including paraspinal muscles. MUAPs are normal throughout, and recruitment pattern is normal. Muscle cooling to 20°C has no appreciable effect on the needle examination. We now are ready to formulate our electrophysiologic impression. IMPRESSION: The electrophysiologic findings are consistent with a myotonic muscle disorder with no evidence of dystrophic features. The response on the short exercise test and lack of effect of muscle cooling are consistent with myotonia congenita. The history, physical examination, and laboratory studies are consistent with myotonia congenita. The electrodiagnostic studies show the presence of myotonic discharges, which are widespread and easily elicited throughout. No myopathic MUAPs suggesting a dystrophic process are noted. There is no effect of muscle cooling. Therefore, the electrophysiologic findings are consistent with a myotonic muscle disorder without dystrophic changes, suggesting a diagnosis of myotonia congenita. Although the clinical history may suggest paramyotonia congenita, the lack of effect of muscle cooling would rule against this diagnosis in favor of myotonia congenita. In addition, the fact that the patient’s stiffness improves rather than worsens with repeated contractions favors the diagnosis of myotonia congenita over paramyotonia congenita. 

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 709

CASE 39.2  Nerve Conduction Studies.

Nerve Stimulated

Amplitude Motor = mV; Sensory = μV Stimulation Site

Recording Site

Median (m)

Wrist Antecubital fossa

Ulnar (m)

RT

LT

NL

APB APB

9.6 9.4

≥4

Wrist Below elbow Above elbow

ADM ADM ADM

11.3 11.1 10.8

≥6

Median (s)

Wrist

Index finger

24

Ulnar (s)

Wrist

Little finger

21

Tibial (m)

Ankle Popliteal fossa

AHB AHB

Sural (s)

Calf

Posterior ankle

Latency (ms) RT

LT

NL

Conduction Velocity (m/s)

F-­wave Latency (ms)

RT

RT

LT

NL

3.4 ≤4.4 8.1

54

≥49

2.6 ≤3.3 6.6 8.2

57 64

≥49 ≥49

≥20

3.1 ≤3.5

54

≥50

≥17

2.8 ≤3.1

52

≥50

6.8 5.9

≥4

4.9 ≤5.8 11.2

50

≥41

14

≥6

3.6 ≤4.4

48

≥40

LT

NL

27

≤31

31

≤32

Short Exercise Test: Ulnar (m)

Wrist

ADM

Immediate drop in CMAP amplitude by 40% on first trial of exercise, which recovers over 2 minutes. After several trials, the CMAP drop is no longer seen.

Note: All sensory latencies are peak latencies. All sensory conduction velocities are calculated using onset latencies. The reported F-­wave latency represents the minimum F-­wave latency. ADM, Abductor digiti minimi; AHB, abductor hallucis brevis; APB, abductor pollicis brevis; CMAP, compound muscle action potential; LT, left; m, motor study; NL, normal; RT, right; s, sensory study.

CASE 39.2  Electromyography. Spontaneous Activity

Voluntary Motor Unit Action Potentials Configuration

Insertional Activity

Fibrillation Potentials

Fasciculation Potentials

Left first dorsal interosseous

Myo

0

0

NL

NL

NL

NL

NL

Left abductor pollicis brevis

Myo

0

0

NL

NL

NL

NL

NL

Left pronator teres

Myo

0

0

NL

NL

NL

NL

NL

Left extensor indicis proprius

Myo

0

0

NL

NL

NL

NL

NL

Left biceps brachii

Myo

0

0

NL

NL

NL

NL

NL

Left medial deltoid

Myo

0

0

NL

NL

NL

NL

NL

Left C7 paraspinal

Myo

0

0

NL

NL

NL

NL

NL

Left tibialis anterior

Myo

0

0

NL

NL

NL

NL

NL

Left medial gastrocnemius

Myo

0

0

NL

NL

NL

NL

NL

Left vastus lateralis

Myo

0

0

NL

NL

NL

NL

NL

Muscle

Muscle cooling to 20°C: No effect on needle EMG. EMG, Electromyography; Myo, myotonic discharges; NL, normal.

Activation Recruitment

Duration

Amplitude Polyphasia

710

SECTION VIII   Clinical Disorders

Summary

Case 39.3

The history is that of a young man who presents with episodic weakness dating back to early childhood, lasting minutes to hours, exacerbated by cold, and noted most often on waking. The neurologic examination reveals no weakness, but there is percussion myotonia. There is a strong family history of similarly affected individuals, with an autosomal dominant pattern of inheritance. In summary, there is evidence of episodic weakness and myotonia in a young male, with no evidence of fixed weakness or extramuscular manifestations. Therefore, before proceeding to electrodiagnostic testing, the possibility of an inherited periodic paralysis syndrome should be considered. Nerve conduction studies were carried out during an attack-­free interval. The right median, ulnar, and tibial motor and F response studies reveal normal CMAP amplitudes, distal motor latencies, and conduction velocities. The median, ulnar, and sural sensory studies are normal, which is expected given the normal sensory examination. The short exercise test, stimulating the wrist and recording from ADM, is normal. The prolonged exercise test, stimulating the wrist and recording from ADM, shows an initial increment in CMAP amplitude of 20%, followed by a 55% drop in CMAP amplitude that reached a nadir after 40 minutes and recovered to baseline after approximately 1 hour.

History and Physical Examination A 19-­year-­old male was referred for recurrent episodes of weakness that began in childhood. The episodic weakness usually was noted on waking in the morning and lasted minutes to hours, affecting proximal and distal muscles of the upper and lower extremities but never affecting respiration or bulbar muscles. Episodes of weakness often were accompanied by pain in his legs. Family history was notable for his father, one brother, and one sister having similar symptoms. A paternal aunt, grandfather, and several first cousins had similar symptoms. On examination, his mental status was unremarkable. On cranial nerve examination, there was no bulbofacial weakness or ptosis. There was normal muscle strength in the neck and upper and lower extremities bilaterally. Percussion myotonia was noted over the thenar muscles. Deep tendon reflexes were normal throughout with flexor plantar responses. Sensation and coordination were normal throughout. There were no dysmorphic facial features or unusual physical features. Laboratory studies were notable for a normal CK level, electrolyte levels, and thyroid function studies. However, the potassium level had been noted to be slightly elevated during episodes of weakness. 

CASE 39.3  Nerve Conduction Studies. Amplitude Motor = mV; Sensory = μV

Latency (ms)

Nerve Stimulated

Stimulation Site

Recording Site

RT

NL

RT

Median (m)

Wrist Antecubital fossa

APB APB

8.4 8.2

≥4

3.4 8.1

≤4.4

Ulnar (m)

Wrist Below elbow Above elbow

ADM ADM ADM

10.6 10.4 10.2

≥6

2.8 6.8 8.2

≤3.3

Median (s)

Wrist

Index finger

24

≥20

3.1

Ulnar (s)

Wrist

Little finger

21

≥17

Tibial (m)

Ankle Popliteal fossa

AHB AHB

5.1 4.2

≥4

Sural (s)

Calf

Posterior ankle

12

≥6

LT

LT

NL

Conduction Velocity (m/s) RT

LT

NL

54

≥49

56 64

≥49 ≥49

≤3.5

52

≥50

2.7

≤3.1

50

≥50

5.2 12.5

≤5.8 44

≥41

3.8

≤4.4

46

≥40

F-­wave Latency (ms) RT

LT

NL

28

≤31

31

≤32

Short Exercise Test: Ulnar (m)

Wrist

ADM

No drop of CMAP amplitude after short exercise.

ADM

Immediate increment of CMAP amplitude by 20%. Subsequent drop of CMAP amplitude by 55% with lowest CMAP at 40 minutes. Recovery to baseline at 60 minutes.

Prolonged Exercise Test: Ulnar (m)

Wrist

Note: All sensory latencies are peak latencies. All sensory conduction velocities are calculated using onset latencies. The reported F-­wave latency represents the minimum F-­wave latency. ADM, Abductor digiti minimi; AHB, abductor hallucis brevis; APB, abductor pollicis brevis; CMAP, compound muscle action potential; LT, left; m, motor study; NL, normal; RT, right; s, sensory study.

Chapter 39 • Myotonic Muscle Disorders and Periodic Paralysis Syndromes 711 CASE 39.3  Electromyography. Spontaneous Activity Muscle

Insertional Activity

Voluntary Motor Unit Action Potentials Configuration

Fibrillation Potentials

Fasciculation Potentials

Activation

Recruitment

Duration

Amplitude

Polyphasia

Right first dorsal interosseous

NL

0

0

NL

NL

NL

NL

NL

Right extensor digitorum communis

Myo

0

0

NL

NL

NL

NL

NL

Right biceps brachii

Myo

0

0

NL

NL

NL

NL

NL

Right medial deltoid

Myo

0

0

NL

NL

NL

NL

NL

Right triceps

Myo

0

0

NL

NL

NL

NL

NL

Right C7 paraspinal

Myo

0

0

NL

NL

NL

NL

NL

Right tibialis anterior

Myo

0

0

NL

NL

NL

NL

NL

Right medial gastrocnemius

Myo

0

0

NL

NL

NL

NL

NL

Right vastus lateralis

NL

0

0

NL

NL

NL

NL

NL

Muscle cooling to 20°C: No effect on needle EMG. EMG, Electromyography; Myo, myotonic discharges; NL, normal.

On needle EMG study, myotonic discharges are noted in distal and proximal muscles of the upper and lower extremities. The MUAPs are normal throughout, and recruitment pattern is normal. Muscle cooling to 20°C has no appreciable effect on the needle examination. We now are ready to formulate our electrophysiologic impression. IMPRESSION: The electrophysiologic findings are consistent with a myotonic muscle disorder with no evidence of dystrophic features. The drop ­in amplitude with prolonged exercise testing and myotonic discharges noted on needle EMG are compatible with a diagnosis of hyperkalemic periodic paralysis. The history, neurologic examination, and laboratory findings are consistent with hyperkalemic periodic paralysis. The electrodiagnostic studies show the presence of myotonic discharges in distal and proximal muscles, with normal MUAPs, consistent with a myotonic muscle disorder without dystrophic changes. In addition, the prolonged exercise test shows a characteristic decline in CMAP amplitude over time. Although the prolonged exercise test does not distinguish hypokalemic from hyperkalemic periodic paralysis, the presence of myotonia points toward hyperkalemic periodic paralysis, as myotonia is only very rarely seen in the hypokalemic form of periodic paralysis. Although the periodic weakness and abnormal prolonged exercise test also might suggest ATS, myotonia is not a feature of this syndrome, and there is

no note made of the characteristic facial features seen in this syndrome nor of any abnormality on electrocardiogram in the patient or affected family members. Although periodic weakness may also be seen in paramyotonia congenita, the lack of effect of muscle cooling, the normal short exercise test, and the abnormal prolonged exercise test rule against this diagnosis in favor of hyperkalemic periodic paralysis.

Suggested Readings Aminoff MJ, Layzer RB, Satya-­Murti S, et al. The declining electrical response of muscle to repetitive nerve stimulation in myotonia. Neurology. 1977;27:812. Arsenault ME, Prévost C, Lescault A, et al. Clinical characteristics of myotonic dystrophy type 1 patients with small CTG expansions. Neurology. 2006;66:1248–1250. Brooke MH. A Clinician’s View of Neuromuscular Disease. Baltimore: Williams & Wilkins; 1986. Cannon SC. Channelopathies of skeletal muscle excitability. Compr Physiol. 2015;5(2):761–790. Griggs RC, Mendell JR, Miller RG. Evaluation and Treatment of Myopathies. Contemporary Neurology Series. Philadelphia: FA Davis; 1995. Kuntzer T, Flocard F, Vial C, et al. Exercise test in muscle channelopathies and other muscle disorders. Muscle Nerve. 2000;23(7):1089–1094. Logigian EL, Ciafaloni E, Quinn LC, et al. Severity, type, and distribution of myotonic discharges are different in type 1 and type 2 myotonic dystrophy. Muscle Nerve. 2007;35:479–485.

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SECTION VIII   Clinical Disorders

Machuca-­Ttzili L, Brook D, Hilton-­Jones D. Clinical and molecular aspects of the myotonic dystrophies: a review. Muscle Nerve. 2005;32:1–18. McManis PG, Lambert EH, Daube JR. The exercise test in periodic paralysis. Muscle Nerve. 1986;9:704. Michel P, Sternberg D, Jeannet P, et al. Comparative efficacy of repetitive nerve stimulation, exercise, and cold in differentiating myotonic disorders. Muscle Nerve. 2007;36:643–650. Miller TM. Differential diagnosis of myotonic disorders. Muscle Nerve. 2008;37:293–299. Papadimas GK, Kekou K, Papadopoulos C, Kararizou E, Kanavakis E, Manta P. Phenotypic variability and molecular genetics in proximal myotonic myopathy. Muscle Nerve. 2015;51(5):686–691. Ptacek LJ, Johnson KJ, Griggs RC. Genetics and physiology of the myotonic muscle disorders. N Engl J Med. 1993;18:482. Ricker K, Koch MC, Lehmann-­Horn F, et al. Proximal myotonic myopathy: a new dominant disorder with

myotonia, muscle weakness and cataracts. Neurology. 1994;44:1448. Ruff RL, Shapiro BE. Disorders of skeletal muscle membrane excitability: myotonia congenita, paramyotonia congenita, periodic paralysis and related syndromes. In: Katirji B, Kaminski HJ, Ruff RL, eds. Neuromuscular Disorders in Clinical Practice. New York: Springer; 2014. Shapiro BE, Brown RH. Myotonia and periodic paralysis. In: Samuels MA, Feske S, eds. Office Practice of Neurology. 2nd ed. New York: Churchill Livingstone; 2003. Simmons DB, Lanning J, Cleland JC, et al. Long exercise test in periodic paralysis: a Bayesian analysis. Muscle Nerve. 2019;59(1):47–54. Statland JM, Fontaine B, Hanna MG, et al. Review of the diagnosis and treatment of periodic paralysis. Muscle Nerve. 2018;57(4):522–530. Streib EW. AAEE minimonograph, no. 27: Differential diagnosis of myotonic syndromes. Muscle Nerve. 1987;10:603.

SECTION IX • Electromyography in Special Clinical Settings

Approach to Electrodiagnostic Studies in the Intensive Care Unit The majority of electrodiagnostic (EDX) studies are performed on outpatients, even in those electromyography (EMG) laboratories that are physically located within a hospital. However, an increasing number of EDX studies are done on patients in the intensive care unit (ICU). In the ICU setting, the patients typically are profoundly ill, often with several serious overlapping medical problems. Most are intubated and receiving mechanical ventilation, which prevents them from traveling to the EMG laboratory, necessitating a portable study. EDX studies are most often requested in the ICU for the following indications:    • T  he patient presents with rapidly progressive weakness, with or without sensory symptoms, often leading to respiratory compromise and intubation. In these patients, the referring physician easily recognizes that the patient likely has a primary neurologic disorder. However, this group of patients is much less common than the following scenarios. • The patient is admitted to the ICU with a serious nonneurologic medical illness. Many have sepsis and/or multiple organ failure. Most are intubated and require sedation or pharmacologic paralysis with neuromuscular junction–blocking agents (NMBAs) while on the ventilator. When the primary medical conditions are treated and begin to recover, and sedatives and other drugs are weaned, the patient begins to awaken and is able to cooperate. It is at this point that the medical staff recognizes that the patient has profound weakness of the extremities, often with flaccid tone and areflexia. • This scenario overlaps with the preceding one. As the primary medical conditions are treated and begin to recover, the sedatives and other drugs are weaned in preparation for extubation. However, despite apparently intact cardiac and pulmonary function, the patient fails to wean off the ventilator. The question then arises if there is a neuromuscular disorder that is preventing extubation.

DIFFERENTIAL DIAGNOSIS OF NEUROLOGIC WEAKNESS IN THE ICU

Neurologic causes of profound weakness in an ICU patient include disorders of the central nervous system (CNS) and the peripheral nervous system (PNS) (Box 40.1). Some of

40

these are primary neurologic disorders that result in admission to the ICU, whereas others occur while the patient is hospitalized for unrelated medical conditions (Box 40.2). One of the most common CNS diagnoses leading to weakness in the ICU is encephalopathy. Encephalopathy in the ICU often is multifactorial, secondary to a multitude of causes including electrolyte and metabolic disturbances, sepsis, and medications. Other CNS disorders can manifest as generalized weakness, including stroke, especially of the posterior circulation, seizures, anoxia, subarachnoid hemorrhage, and infectious meningitis. The spinal cord is part of the CNS, and spinal cord disorders can also present as generalized weakness. Infarction,

Box 40.1  Neurologic Differential Diagnosis of Weakness in the Intensive Care Unit Central Nervous System Brain Encephalopathy Infarction Seizures Anoxia Subarachnoid hemorrhage Spinal cord Infarction Demyelination Trauma Peripheral Nervous System Anterior horn cell Paralytic poliomyelitis Amyotrophic lateral sclerosis (rare unless there is a coexistent exacerbating factor) Nerve Guillain-­Barré syndrome Critical illness polyneuropathy Porphyria Toxins Neuromuscular junction Botulism Myasthenia gravis Persistent drug-­induced neuromuscular junction blockade Toxic Lambert-­Eaton myasthenic syndrome (rare unless there is a coexistent exacerbating factor) Muscle Critical illness myopathy Adult-­onset acid maltase deficiency myopathy Inflammatory myopathy (severe) Toxic Periodic paralysis

713

714

SECTION IX    Electromyography in Special Clinical Settings

Box 40.2  Recognition of Neuromuscular Disorders by Presentation in the Intensive Care Unit Initial Presentation: Primary Rapidly Progressive Weakness With or Without Respiratory Weakness Paralytic poliomyelitis GBS Porphyria Severe toxic neuropathy Botulism MG (uncommon unless there is a coexistent exacerbating factor) Toxic myopathy with rhabdomyolysis Periodic paralysis (respiratory weakness rare) Initial Presentation: Primary Respiratory Failure in Isolation Paralytic poliomyelitis (uncommon) MG (uncommon) GBS (uncommon) Adult-­onset acid maltase deficiency myopathy Bilateral phrenic neuropathies (postinfectious) Generalized Weakness Discovered as the Patient Is Recovering From Medical/Surgical Condition CIM CIP Persistent NMJ blockade Failure to Wean as the Patient Is Recovering From Medical/ Surgical Condition CIM CIP Unilateral/bilateral phrenic neuropathies (especially after thoracic surgery) Persistent NMJ blockade (rare) MG (if pneumonia provoked the admission) ALS (if pneumonia provoked the admission) LEMS (if calcium channel blockers or NMBAs were given) Charcot-­Marie-­Tooth, type 2C ALS, Amyotrophic lateral sclerosis; CIM, critical illness myopathy; CIP, critical illness polyneuropathy; GBS, Guillain-­Barré syndrome; LEMS, Lambert-­Eaton myasthenic syndrome; MG, myasthenia gravis; NMBAs, neuromuscular junction–blocking agents; NMJ, neuromuscular junction.

demyelination, or unrecognized trauma in the high cervical cord can present acutely as a flaccid quadriparesis with decreased or absent reflexes and loss of sensation. Remember that an acute CNS disorder often is associated initially with decreased tone and reduced reflexes (i.e., cerebral or spinal shock) and can mimic a PNS problem early on. In the PNS, profound weakness can occur from a lesion anywhere in the motor unit, from the motor neuron (anterior horn cell) to the motor nerve, neuromuscular junction (NMJ), and muscle. Acute motor neuron disease is very uncommon and occurs only in the setting of paralytic poliomyelitis. As discussed in Chapter 31, poliomyelitis is a clinical syndrome that occurs from infection by several viruses, with West Nile and other viruses now added to the list. Acute flaccid myelitis (AFM) occurs mostly in children, primarily associated with Enterovirus D68 (EV-­D68), as discussed in Chapter 31. Patients with chronic motor neuron disorders, such as amyotrophic lateral sclerosis (ALS), occasionally present to the ICU when the neurologic condition has not been previously recognized or diagnosed, and the patient comes to medical attention because of a concurrent acute medical problem, usually pneumonia. The typical

scenario is that of a patient with bulbar-­onset ALS who has undergone an exhaustive medical evaluation looking for a gastrointestinal or otolaryngologic etiology of the speech and swallowing dysfunction. The impaired speech and swallowing eventually lead to aspiration and an accompanying pneumonia, which when superimposed on respiratory muscle weakness from the unrecognized ALS quickly leads to respiratory compromise and the need for intubation. It is only then, in the ICU, as the patient is recovering from the pneumonia but cannot be weaned from the ventilator, that it becomes more apparent that there is more generalized weakness that had not been appreciated earlier. Moving down the motor unit, the most well-­known acute neuropathy that results in marked weakness and respiratory compromise is Guillain-­Barré syndrome (GBS). GBS is an acquired motor and sensory polyradiculoneuropathy that usually is demyelinating. Other variants have been described, including axonal forms, one of which is motor and sensory, and the other pure motor. GBS probably has an autoimmune etiology, often triggered by an infection either days or a few weeks earlier. Patients typically present with ascending numbness and weakness over several days, often with simultaneous paresthesias of the fingers and toes. Weakness may affect bulbofacial and respiratory muscles. Some patients present more abruptly, over hours, with associated early respiratory weakness. Other than GBS, it is rare to see an acute neuropathy as the cause for admission to the ICU. Notable exceptions include porphyria and some toxic (e.g., arsenic) neuropathies, which can mimic the presentation of GBS. The most common severe neuropathy seen in the ICU patient is critical illness polyneuropathy (CIP). CIP usually occurs in patients within 1–3 weeks of ICU admission who have been admitted for a primary medical illness, most often sepsis, systemic inflammatory response syndrome (SIRS), and multiple organ failure. In contrast to GBS, which is usually demyelinating, CIP is an axonal sensorimotor polyneuropathy thought to be due to a complication of SIRS. SIRS is a severe systemic inflammatory response that can be caused by sepsis but is also seen in other settings, including trauma, burns, major organ failure, and/or as a consequence of major procedures. SIRS is thought to be present in most patients hospitalized in the ICU for longer than 1 week. In SIRS, significant cellular and humoral responses are thought to alter the microcirculation in the body, including the microcirculation to nerve and muscle. These responses include changes in endothelial and inflammatory cells, in addition to the expression of numerous cytokines and coagulation factors, among other changes. In prospective studies of ICU patients studied with serial nerve conduction studies, CIP can occur as early as within 3 days after the onset of sepsis. In most patients, CIP is preceded by a septic encephalopathy (aka, toxic metabolic encephalopathy), which is extremely common in ICU patients. CIP usually comes to medical attention only when the patient begins to improve from their primary medical illness but is found to have profound weakness and sensory loss or fails to wean from the ventilator. As CIP results in axonal degeneration, recovery is typically very slow and

Chapter 40 • Approach to Electrodiagnostic Studies in the Intensive Care Unit 715

often incomplete, especially in severe cases. Indeed, in some cases, clinical and electrophysiologic evidence of CIP may remain for years after an ICU admission; rare patients remain profoundly disabled. CIP is reported to be very common in ICU patients and can occur by itself, or more commonly in association with critical illness myopathy (CIM). Indeed, the two are recognized together so commonly, depending on how closely the patient is examined clinically and electrically, that some have advocated for the term critical illness polyneuromyopathy to describe the neuromuscular syndrome that commonly occurs in the ICU. In one study of ICU patients with SIRS, 50% developed a neuromuscular disorder. Of these, 80% had both CIP and CIM, 10% had CIP alone, and 10% had CIM alone. Even more remarkable, in another study, abnormal EDX findings were present in up to 90% of patients admitted to an ICU for various reasons, especially sepsis and multiorgan failure. In addition to severe polyneuropathies, mononeuropathies of one or both phrenic nerves can directly result in respiratory compromise. Many of these patients are seen in the ICU. Phrenic neuropathies may be idiopathic, presumably autoimmune and postinfectious, similar in etiology to other mononeuropathies such as Bell’s palsy. In addition, phrenic neuropathy can occur rarely as part of neuralgic amyotrophy, either in isolation or more commonly as part of a more widespread pattern of multiple mononeuropathies. The other situation where unilateral or bilateral phrenic neuropathies occurs is as a complication of thoracic surgery. Some cases of phrenic neuropathy following coronary artery bypass surgery may be due to cold-­ induced injury occurring secondary to the use of topical cooling with ice slush used during surgery for prevention of myocardial ischemia. Moving next to the NMJ, several disorders should be considered in the ICU setting. The one disorder of NMJ that presents acutely as rapidly progressive weakness in an adult is botulism. The typical presentation is one of descending paralysis, often associated with gastrointestinal and autonomic symptoms. Of course, a large number of chemical and biologic toxins can poison the NMJ acutely, among them organophosphates, spider venom, and “nerve gas.” Although myasthenia gravis (MG) typically is diagnosed in an outpatient presenting with ptosis, double vision, slurred speech, and fluctuating weakness, an occasional previously undiagnosed patient may present to the ICU in acute primary respiratory failure. This situation can occur from selective involvement of the diaphragm and other muscles of respiration or, similar to the patient with unrecognized ALS, from bulbar weakness leading to aspiration and pneumonia, quickly followed by respiratory failure. Patients with Lambert-­Eaton myasthenic syndrome (LEMS) are distinctly uncommon in the ICU. First, the disorder is extremely rare. Second, the disorder usually presents subacutely over months, and respiratory muscles are not typically involved. Clinically, LEMS is most often confused with a myopathy. However, rare patients with LEMS present to the ICU as a failure to wean after elective

surgery. In these cases, LEMS probably is unmasked when the patient receives a calcium channel blocker or an NMBA at the time of surgery. Rare patients without any underlying NMJ or muscle disorder fail to extubate as a result of delayed clearance of an NMBA given during anesthesia in preparation for surgery. Most often, these patients have renal insufficiency or frank renal failure and thus fail to clear the NMBA effectively from their system. The most common paralytic agent reported is vecuronium. The final component of the motor unit is the muscle. By far, the most common muscle disorder seen in the ICU is CIM, also known as acute quadriplegic myopathy, thick myosin filament myopathy, and intensive care myopathy, among many other names. CIM occurs most often in the setting of high-­dose intravenous steroids used in conjunction with NMBAs. Rarely, it is seen in association with only one of the two; exceptional cases have been reported in sepsis and multiple organ failure in the absence of steroids and NMBAs. Pathologically, there is dissolution of the thick myosin filaments in most cases. Rarely, there is a necrotizing myopathy on muscle biopsy. One of the most common clinical situations in which CIM occurs is in patients with status asthmaticus, with estimates as high as a third of patients developing some component of CIM. These patients typically are intubated and treated with high-­dose intravenous methylprednisolone. Because intubation often is difficult in these patients, pharmacologic paralysis with NMBAs is common. As the asthma improves, it becomes apparent that the patient is flaccid, areflexic, and profoundly weak. Once intubated, the patient may fail to wean for a prolonged period of time. CIM recovers in most patients in 3–6 months. However, in patients with SIRS, CIM often occurs in conjunction with CIP. When both are present, the recovery is much longer and may result in permanent disability because of the CIP component. Other myopathies seldom cause respiratory arrest or severe generalized weakness in the ICU. Rarely, severe cases of inflammatory myopathy (i.e., polymyositis or dermatomyositis) may result in profound generalized weakness. Likewise, severe toxic myopathies are uncommon in the ICU, although rare cases of rhabdomyolysis associated with alcohol, drugs, or other toxins can present as profound weakness. Periodic paralysis, especially hypokalemic periodic paralysis, presents as severe, rapidly evolving weakness during an attack, but only rarely affects the respiratory muscles. Finally, although extremely rare, the myopathy associated with adult-­onset acid maltase deficiency characteristically affects respiratory and abdominal muscles and can present as a primary neuromuscular cause of respiratory insufficiency. 

ELECTRODIAGNOSTIC STUDIES IN THE ICU: TECHNICAL ISSUES

There are a number of challenging technical issues unique to performing EDX studies in the ICU (Table 40.1). Some are related to patient factors, whereas others involve

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Table 40.1  Technical Problems in the Intensive Care Unit. Problem

Guidelines/Recommendations

Poor cooperation—cannot place their limb in an optimal position

Need a second person to help immobilize the limb

Poor cooperation—heavily sedated

Do the entire study except for the portion of the needle EMG looking at MUAPs; inquire if sedation can be temporarily reduced. Some agents, such as propofol, can be easily adjusted

Poor cooperation—cannot perform 10 seconds of exercise

Use 50-­Hz repetitive nerve stimulation

Poor cooperation—cannot activate muscles for needle EMG

Choose muscles that will contract reflexively when withdrawing from a painful stimulus

Cannot roll on side for the sural sensory study

One person holds the leg with the knee flexed, taking care not to touch recording electrodes, while the second person stimulates

Cannot roll on side to sample gluteal muscles

Study the tensor fascia lata or gluteus medius; they are in the lateral thigh when supine

Cannot roll on side to sample posterior shoulder girdle muscles

Study the medial or anterior deltoid

Cannot roll on side to sample paraspinal muscles

Omit; if absolutely necessary, need additional personnel to help roll the patient

Cannot roll over to the prone position for the H reflex

Omit the H reflex; if absolutely necessary, can be performed supine

External pacemaker wire present

Do not do any electrodiagnostic studies—risk of electrical injury too high

Subclavian or internal jugular central line present

Study contralateral side; if not possible, avoid proximal stimulation (i.e., axilla and Erb’s point)

Excessive electrical noise

Use coaxial cables; good skin preparation; proper use of electrode gel; turn off other devices if possible; operator and patient should not touch the metal bed.

Poor access to median/ulnar nerves at the wrist or elbow due to lines

Choose the contralateral side if possible; stimulate the median nerve in the mid-­arm instead of the antecubital fossa

  

EMG, Electromyography; MUAP, motor unit action potential.

central and intravenous lines and electrical equipment that interfere with the performance of the study. While good patient rapport and cooperation are indispensable to the efficiency and reliability of the EMG study in the outpatient setting, these goals are much more difficult, if not impossible, to accomplish with the ICU patient. Many ICU patients are encephalopathic and cannot cooperate with the EMG examination. They may become easily agitated, making both the nerve conduction and needle examination difficult to accomplish. On the other hand, patients who are intubated are often sedated with benzodiazepines or narcotics. Some may be placed in a pharmacologic coma with propofol or barbiturates. Although such patients may not be agitated, they are unable to cooperate with routine nerve conduction and EMG studies. Neither the agitated patient nor the sedated patient is able to give the electromyographer proper feedback during the study, for example whether he or she is feeling the stimulus during the nerve conduction studies. Nor can such patients place their limbs in the correct position for the nerve conduction studies or the spontaneous activity assessment portion of the needle examination. Finally, they cannot cooperate with the examiner to activate their muscles when trying to assess motor unit action potentials (MUAPs) during the needle examination.

Because of these and other difficulties (described later), it is always recommended that two individuals perform the study together in the ICU. One person can run the EMG machine while the other performs the nerve conduction studies and needle examination, adjusting the patient’s limbs to the extent possible. Access to certain anatomic locations in the ICU can be difficult. The presence of arterial lines, especially at the wrist, often interferes with the ability to stimulate the distal median and ulnar nerves. Because the antecubital fossa is a common site for intravenous lines, the proximal median stimulation site may not be accessible. This can be remedied by moving more proximally toward the axilla where the median nerve can often be easily stimulated. The presence of intravenous lines in the antecubital fossa may also make it difficult to flex the elbow during ulnar motor conduction studies. As noted in Chapter 22, if ulnar motor conduction studies are not performed with the elbow in a flexed position, factitious slowing across the elbow may easily occur. Patients who are intubated or cannot cooperate due to encephalopathy or sedation will have great difficulty moving to certain positions that are required for some nerve conduction studies and needle EMG. Of the nerve conduction studies, the sural sensory potential is the one most at risk to be compromised because it is optimally performed with the

Chapter 40 • Approach to Electrodiagnostic Studies in the Intensive Care Unit 717

patient rolled onto his or her contralateral side. If the patient cannot be rolled onto the contralateral side or maintain that position, the study can be done with the patient supine and the leg flexed at the knee. This usually will require the assistance of another person to help hold the leg in place, and the waveform may still be suboptimal. Likewise, the tibial H reflex is best performed with the patient prone, which is essentially not possible in any ICU patient. If a central catheter is in place, proximal stimulation (i.e., axilla, Erb’s point, and nerve root) is relatively contraindicated in the ICU patient (see Chapter 43). During the needle EMG examination, it often is very difficult or impossible to sample certain muscles because of the patient’s inability to roll on his or her side. Most important among them are the gluteal, hamstring, posterior shoulder girdle, and paraspinal muscles. In addition to the technical problems posed by the patient in the ICU, several technical problems related to electrical devices in the ICU may compromise the EDX study. First, the typical ICU room is filled with numerous electrical devices that are potential sources of electrical noise. Electrical noise can obscure the nerve conduction potentials (especially sensory potentials, which are orders of magnitude smaller than motor potentials) and needle EMG potentials. Second, ICU patients lie in beds with metal frames and side restraints. These beds usually are electrical devices themselves, with motors, wires, and controls as part of the actual bed. Many of the electrical devices in the room are attached to the patient (e.g., electrocardiograph, blood pressure monitor, etc.). The presence of multiple electrical devices attached to the patient, each with its own ground electrode, increases the potential risk of an electrical injury if the EMG machine is not maintained or if proper protocol is not followed (see Chapter 43). Finally, the presence of any line that traverses through the patient’s skin and lies close to the heart (e.g., central catheter, external pacemaker) results in the so-­called “electrically sensitive patient.” In this situation, extremely small leakage currents from the EMG machine can pose a risk to the patient, whereas such small currents would be of no consequence to the typical outpatient (see Chapter 43). 

IMPORTANT ELECTRODIAGNOSTIC PATTERNS IN THE INTENSIVE CARE UNIT

A limited number of nerve conduction and needle EMG patterns are seen in the ICU, based on the neurologic conditions that may result in respiratory or generalized weakness requiring ICU admission (Table 40.2). Each pattern suggests a specific localization; in some cases, the pattern may suggest additional studies to be performed.

Nerve Conduction Studies Normal Motor and Sensory Conduction Studies With Normal F Responses This pattern usually implies that the PNS is intact and that the etiology of the weakness most likely is central. However,

this pattern can also occur in several neuromuscular conditions. The most important to exclude is a postsynaptic NMJ disorder (e.g., MG). Whereas presynaptic NMJ disorders typically have low motor amplitudes, most postsynaptic disorders usually are normal at baseline. Thus, in patients with generalized weakness and normal routine motor and sensory conduction studies, it is essential to perform slow (3 Hz) repetitive nerve stimulation in at least one nerve to look for a decremental response. One also must be careful when interpreting the significance of normal motor and sensory nerve conduction studies unless the process is at least 1 week old, which is sufficient time for wallerian degeneration to have occurred. Otherwise, this pattern cannot exclude an acute neuropathic process (i.e., anterior horn cell or peripheral nerve).  Normal Motor and Sensory Conduction Studies With Abnormal F Responses This is the characteristic pattern seen within the first few days of GBS. GBS typically begins at the root level as a demyelinating polyradiculopathy. As time proceeds, it turns into a demyelinating polyradiculoneuropathy. Thus nerve conduction studies often are normal initially, except for the F responses, which are delayed, impersistent, dispersed, or absent. In the case of absent F responses, however, there is one very important proviso before attributing absent F responses to proximal demyelination. Recall that the circuitry of the F response includes the anterior horn cell in the spinal cord. The anterior horn cell is susceptible to suprasegmental facilitatory influences. This is why the Jendrassik maneuver is useful in eliciting F responses. Likewise, the anterior horn cell is susceptible to suprasegmental inhibitory influences. Thus, if a patient is heavily sedated or in coma, absent F responses are of no significance and may be a normal finding in this population. Absent F responses can be considered a marker of proximal demyelination only if the patient is awake and alert.  Low or Absent Motor Responses With Normal Sensory Responses Although this pattern can be seen in polyradiculopathy, most often this pattern implies a pure motor disorder, at the level of the muscle, NMJ, or motor neuron. This pattern is distinctly unusual in most myopathies, which preferentially affect proximal muscles, which are not recorded in routine nerve conduction studies. Even in the unusual case of adult-­onset acid maltase deficiency, distal muscles are not affected. However, diffusely low motor responses are the classic pattern seen in CIM, which affects proximal and distal muscles. In addition, CMAP durations are often prolonged in CIM, thought to be due to slowing of muscle fiber conduction velocity. Low or absent motor responses with normal sensory responses is also the classic pattern seen in presynaptic NMJ disorders, such as botulism and LEMS. Finally, it is also the pattern seen in acute anterior horn cell disease, as occurs in paralytic poliomyelitis, if the nerve conduction studies are performed after 5 days of onset, when there has

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Table 40.2  Neurologic Diagnoses and Associated Electrodiagnostic Findings in the Intensive Care Unit. Disorder

Motor NCS

Sensory NCS

RNS

Needle EMG findings

Encephalopathy/ other central nervous system disorders

Normal; F responses may be absent if patient is sedated or in coma

Normal

Normal

Poor activation

ALS

Axonal loss pattern or normal

Normal

Rarely will decrement on slow RNS

Diffuse active denervation and reinnervation with decreased recruitment and activation of MUAPs

Poliomyelitis

Axonal loss pattern or normal

Normal

Normal

First weeks—decreased recruitment of normal configuration MUAPs; later active denervation followed by reinnervation

GBS

If demyelinating, absent F responses early in the course. Conduction block/ temporal dispersion at non-­entrapment sites. Prolonged latencies. Slowed conduction velocities.

Initially normal, later “sural sparing,” followed by low amplitudes and slowed velocities

Normal

First weeks—decreased recruitment of normal configuration MUAPs; later active denervation followed by reinnervation

CIP

Axonal loss pattern or absent

Axonal loss pattern or absent

Normal

Distal pattern of decreased recruitment with or without denervation and reinnervation, depending on the time course.

Phrenic neuropathy

Absent or low amplitudes on phrenic motor studies

Normal

Normal

Normal in limbs. If EMG of the diaphragm is done, it will show a neurogenic pattern

Botulism

Low amplitudes throughout

Normal

Decrement on slow RNS, increment on rapid RNS or brief exercise (however, the absence of an increment cannot exclude botulism)

Unstable or small, short, and polyphasic MUAPs with normal or early recruitment

MG

Normal

Normal

Decrement on slow RNS; repair of the decrement after brief exercise

Normal or unstable or small, short, and polyphasic MUAPs with normal or early recruitment

LEMS

Low amplitudes throughout

Normal

Decrement on slow RNS, increment on rapid RNS or brief exercise

Normal or unstable or small, short, and polyphasic MUAPs with normal or early recruitment

Persistent NMJ blockade

Low amplitudes throughout

Normal

Decrement on slow RNS

Normal or unstable or small, short, and polyphasic MUAPs with normal or early recruitment

CIM

Low amplitudes throughout

Normal

Normal

Small, short, and polyphasic MUAPs with normal or early recruitment; active denervation may be present

Adult-­onset acid maltase deficiency myopathy

Normal

Normal

Normal

Myotonic discharges and fibrillation potentials with small, short, and polyphasic MUAPs, restricted to paraspinal, abdominal, and very proximal muscles

Periodic paralysis

Low amplitudes during an attack

Normal

Normal

Normal; small short and polyphasic MUAPs late in the course; myotonic discharges may be present in hyperkalemic periodic paralysis

  

ALS, Amyotrophic lateral sclerosis; CIM, critical illness myopathy; CIP, critical illness polyneuropathy; EMG, electromyogram; GBS, Guillain-­Barré syndrome; LEMS, Lambert-­Eaton myasthenic syndrome; MG, myasthenia gravis; MUAP, motor unit action potential; NCS, nerve conduction studies; NMJ, neuromuscular junction; RNS, repetitive nerve stimulation.

Chapter 40 • Approach to Electrodiagnostic Studies in the Intensive Care Unit 719

been sufficient time for wallerian degeneration to occur. Because the differential diagnosis of this pattern includes a presynaptic NMJ disorder, it is essential to perform slow (3 Hz) and rapid (50 Hz) repetitive nerve stimulation. If the patient can cooperate, brief exercise testing should be used in lieu of 50 Hz stimulation, which is quite painful (see Chapter 6).  Low or Absent Motor and Sensory Responses The presence of abnormal sensory responses denotes that a neuropathy must be present. However, caution must be taken before attributing weakness in the ICU to the neuropathy, because many patients in the ICU have comorbidities that may cause an incidental neuropathy, such as preexisting diabetes, renal failure, or liver failure. If such preexisting comorbidities do not exist, however, then the presence of low or absent motor and sensory responses likely indicates a new peripheral neuropathy. If the conduction velocities and latencies are in the axonal range, this pattern is most suggestive of critical illness neuropathy. Although rare, one cannot exclude the possibility of the acute motor and sensory axonal neuropathy (AMSAN) variant of GBS. Another possibility to consider, although extremely rare, is one of the axonal variants of Charcot-­ Marie-­Tooth disease that involves limb, diaphragm, vocal cord, and intercostal muscles (type 2C). Rare patients with this disorder will decompensate from a respiratory illness, necessitating an ICU admission. As noted previously, one must always consider the possibility that the patient has a preexisting peripheral neuropathy with a new superimposed process affecting the motor neuron, NMJ, or muscle. In this case, the abnormal sensory potentials may not be related to the current presentation of weakness. For example, in a patient with diabetes admitted to the ICU with new onset of blurred vision and rapidly descending paralysis, with low or absent sensory and motor potentials on nerve conduction studies, the diagnosis of botulism must be considered. The abnormal sensory responses may be secondary to a peripheral neuropathy related to the patient’s diabetes. If this possibility is not considered and repetitive nerve stimulation studies or brief exercise are not performed, the correct diagnosis may be missed. Finally, when low or absent sensory potentials are seen in the ICU, it may be difficult to interpret these findings in the setting of electrical interference or other factors that might preclude recording small potentials. In these cases, one must always consider the possibility that the patient has a primary disorder of the motor neuron, NMJ, or muscle and that the absent sensory potentials are due to technical factors. In this case, repetitive nerve stimulation studies and brief exercise should be considered. This underscores the importance of always keeping in mind the patient’s clinical history and neurologic examination when performing EDX studies.  Motor and Sensory Nerve Conduction Studies With Demyelinating Features Demyelinating features include very prolonged or absent F responses, markedly prolonged distal motor latencies,

and markedly slowed conduction velocities. Additionally, asymmetry in conduction studies from side and side, especially if there is conduction block and/or temporal dispersion of motor nerves at non-­entrapment sites, usually signifies an acquired demyelinating neuropathy. In this case, the acute inflammatory demyelinating polyneuropathy variant of GBS should be considered if the condition is less than 4 weeks in duration or chronic inflammatory demyelinating polyneuropathy if more than 8 weeks in duration. If there is no conduction block, temporal dispersion, or significant asymmetry, caution must be taken, as one may have incidentally discovered an inherited demyelinating peripheral neuropathy (e.g., Charcot-­Marie-­Tooth, type I), unrelated to the etiology of the patient’s ICU admission. 

Needle Electromyography Decreased Recruitment With Normal Configuration Motor Unit Action PotentialMs This is the pattern seen in either an acute axonal lesion or a demyelinating lesion with conduction block. This pattern in an ICU patient with profound weakness is consistent with GBS, early CIP, or paralytic poliomyelitis. Caution must be taken in interpreting a decreased recruitment pattern. Patients who are weak from central causes may have poor activation of normal configuration MUAPs, resulting in an incomplete interference pattern on the EMG screen, which should not be confused with a decreased recruitment pattern (see the following).  Decreased Recruitment With Reinnervated Motor Unit Action Potentials This is the pattern of a subacute or chronic neuropathic disorder, typically many weeks and usually months in duration. This pattern would be expected in ALS, a preexisting polyneuropathy, or CIP in a patient who has had a prolonged hospitalization.  Short-­Duration, Low-­Amplitude Motor Unit Action Potentials This is the pattern seen in a myopathy, often associated with an early recruitment pattern. This pattern occurs in CIM and other severe myopathies. However, it is important to keep in mind that severe NMJ disorders can display a similar pattern. In this case, muscle fibers are not lost but blocked, resulting in fewer muscle fibers per motor unit. Because of the variability in the safety factor of the NMJ in these disorders, MUAPs often will be unstable, varying in configuration from potential to potential.  Decreased Activation Activation is the ability to fire the available MUAPs faster. Activation is a central process. Thus, decreased activation implies that the source of the weakness resides in the CNS. This can result from actual CNS disease, as well as sedation, pain, or poor cooperation. 

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Normal Recruitment, Activation, and Motor Unit Action Potential Morphology The problem with this pattern is the apparent lack of a clinical-­electrophysiologic correlation. If a patient is truly profoundly weak, the needle EMG examination should be abnormal, displaying decreased recruitment (neuropathic), decreased activation (central), or early recruitment and myopathic appearing MUAPs that signify either a myopathy or an NMJ disorder if there is blocking. In this situation, it is important to reexamine the patient and possibly reassess the needle EMG. If one is convinced that the findings are real, one should consider the possibility of an NMJ disorder, especially one that is presynaptic. Soon after activating their muscles, some patients with LEMS will quickly facilitate and their MUAPs will appear normal. 

NERVE CONDUCTION AND ELECTROMYOGRAPHIC PROTOCOL IN THE INTENSIVE CARE UNIT

When studying a patient in the ICU, one needs to perform EDX studies that address the possible differential diagnoses discussed earlier (Box 40.3). At a minimum, one motor nerve conduction study with its F response should be performed in an upper and lower extremity. In the lower extremity, the tibial motor nerve is preferable to the peroneal, as the tibial F responses are always easy to elicit. Indeed, most consider absent peroneal F responses to have little value as they can be a normal finding. Likewise, at least one sensory nerve conduction study should be done in an upper and lower extremity. Clearly, the sural sensory potential is the most challenging in the ICU patient. If the patient cannot turn on his or her side, the sural still can be studied provided two individuals are available. One person can hold the foot with the knee flexed allowing access to the posterior calf, taking care not to touch the recording electrodes, while the other individual works the stimulator. If any of the motor amplitudes are low, it is imperative to perform slow repetitive nerve stimulation looking for a decrement and rapid repetitive nerve stimulation looking for an increment. In a patient who can cooperate, 10 seconds of exercise is best substituted for rapid repetitive nerve stimulation, which is quite painful. However, if the patient cannot cooperate because of sedation or encephalopathy, then rapid (50 Hz) repetitive nerve stimulation is required to exclude a presynaptic NMJ disorder. It is reasonable to consider repetitive nerve stimulation in all patients who have weakness and normal sensory responses. Slow (3 Hz) repetitive nerve stimulation is a useful screen for both presynaptic and postsynaptic disorders. Although the overall sensitivity of repetitive nerve stimulation is in the 50%–70% range for MG, the sensitivity is much higher in the ICU patient with an NMJ disorder. By definition, if a patient is profoundly weak from MG, many muscle fibers must not be reaching threshold and are blocked. Any patient with MG with significant blocking will have abnormal repetitive nerve stimulation studies.

Box 40.3  Recommended Nerve Conduction and Needle Electromyography Protocol in the Intensive Care Unit Routine nerve conduction studies 1. At least one motor nerve conduction study with its corresponding F wave in an upper and lower extremity. In the lower extremity, the tibial nerve is preferred, as the F responses are normally present and easy to evoke 2. At least one sensory nerve conduction study in an upper and lower extremity  Routine needle electromyography 1. Lower extremity: at least one distal and one proximal muscle 2. Upper extremity: at least one distal and one proximal muscle Special considerations: • If adult-­onset acid maltase deficiency myopathy is in the differential diagnosis, sampling the paraspinal muscles is essential. • If the patient cannot cooperate, choose flexor muscles that can be activated reflexively as part of the withdrawal mechanism to a painful stimulus.  Repetitive nerve stimulation 1. Routine slow (3 Hz) repetitive nerve stimulation in at least one nerve 2. In any patient with absent, low, or borderline motor amplitudes, exercise for 10 seconds and repeat the distal stimulation to the corresponding nerve, looking for an abnormal increment. If the patient cannot cooperate with voluntary exercise, use 50 Hz stimulation looking for an abnormal increment, in at least one motor nerve  Other useful studies in selected situations: Direct muscle stimulation • Compare the compound muscle action potential amplitude from direct muscle stimulation with that obtained with nerve stimulation (differentiation between critical illness myopathy and critical illness polyneuropathy)  Phrenic motor studies (bilateral studies) • Assess integrity of the phrenic nerves

The approach to the needle EMG examination of the ICU patient is very similar to that of the pediatric patient. It is important to go where the money is. If possible, one needs to choose muscles that the patient is able to move. Obviously, information about spontaneous activity can be determined from any muscle at rest. However, differentiation among a central process, a neuropathic process, and an NMJ disorder requires assessment of activation, recruitment, and MUAP morphology. This can only be done by examining the MUAPs. If the patient is unable to move any muscle voluntarily because of sedation, encephalopathy, or profound weakness, then it is best to choose muscles that can be activated reflexively. For instance, the tibialis anterior muscle will activate as part of the normal withdrawal response to tickling the sole or applying pressure to a nail bed. In general, flexor muscles are easier to check because they are activated as a normal withdrawal reflex to pain.

Chapter 40 • Approach to Electrodiagnostic Studies in the Intensive Care Unit 721

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Additional Useful Studies in Selected Situations Direct Muscle Stimulation Both CIP and CIM often show reduced motor amplitudes. Because lower extremity sensory responses may be difficult to obtain in the ICU for technical reasons or because many patients in the ICU may have a preexisting neuropathy, nerve conduction studies may not be able to differentiate between CIP and CIM. In patients with CIM, muscle fibers often are inexcitable to direct muscle stimulation. In contrast, in neuropathic situations, the motor amplitudes may be low due to loss of axons, but the muscle fibers are fundamentally intact. Thus, in neuropathic conditions, muscle can be activated by direct stimulation. In some situations, therefore, it is possible to differentiate CIM from CIP using direct muscle stimulation (Fig. 40.1). Direct muscle stimulation is performed by placing a monopolar needle stimulating electrode (as the cathode) in the distal third of the muscle with a nearby subdermal needle electrode placed laterally as the anode. The muscle is stimulated using a 0.1 ms duration stimulus, gradually increasing current from 10–100 mA until a clear twitch is felt or seen. Based on where the twitch is seen, another subdermal needle electrode (active recording electrode) is placed 1–3 cm from the stimulation electrode, with a surface electrode placed several centimeters distally as the reference electrode. During stimulation, both the stimulating monopolar needle electrode and the active recording subdermal needle electrode can be adjusted to optimize the response at low levels of stimulation intensity. The stimulation intensity is increased until a maximal response, the direct muscle action potential (dmCMAP), is obtained. Next, using the same recording electrode montage, the nerve to the muscle is stimulated in the usual manner to obtain a nerve-­evoked compound muscle action potential (neCMAP). The dmCMAP is compared with the neCMAP. In CIM, the neCMAP/dmCMAP ratio is close to one, because both amplitudes are proportionally reduced. In CIP, the ratio is much lower and may be zero because of the disproportionately lower neCMAP compared with the dmCMAP. 

Phrenic Motor Study One possible mechanism in intubated patients who fail to wean from the ventilator is dysfunction of one or both phrenic nerves. The phrenic nerves are most often affected as a postinfectious process or as a complication of thoracic surgery. However, the phrenic nerves can also be affected by a severe diffuse polyneuropathy, including GBS and CIP. The phrenic motor study can be performed recording the diaphragm with the active electrode placed two fingerbreadths above the xiphoid process and the reference electrode 16 cm from the active electrode over the anterior costal margin. The nerve can be stimulated in the lateral neck either posterior to the sternocleidomastoid muscle, approximately 3 cm above the clavicle, or between the sternal and clavicular heads of the sternocleidomastoid just above the clavicle (Fig. 40.2). Unfortunately, a normal phrenic nerve conduction study evokes a CMAP of only a few hundred microvolts. Thus the presence of electrical noise, which is not uncommon in the ICU, can easily obscure the response. An intact phrenic motor response confirms the integrity of the phrenic nerve. However, several technical problems with this study must be taken into account, especially in the ICU. First, it often is difficult to perform phrenic conduction studies on obese individuals or those with a thick neck. Second, the study cannot be performed safely if the patient has an external pacemaker in place. Finally, if a central line is present, the study is contraindicated on the side with the catheter (see Chapter 43). This study is most helpful if responses on both sides are present and normal, or if one side is present and normal and the other side is abnormal or absent (Fig. 40.3). If both responses are absent or low in amplitude, it is difficult to draw a firm conclusion: possibly both responses are truly absent or low, or both responses are abnormal due to technical reasons. 

ULTRASOUND CORRELATIONS Although not limited to the ICU, there is one neuromuscular ultrasound study that has particular utility in the ICU, which is ultrasound of the diaphragm. As discussed earlier,

SECTION IX    Electromyography in Special Clinical Settings

722

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Fig. 40.2  Cross-­sectional anatomy: phrenic nerve stimulation site. The phrenic nerve is stimulated in the lateral neck either posterior to the sternocleidomastoid muscle or between the sternal and clavicular heads of the sternocleidomastoid just above the clavicle. Note that the phrenic nerve is deep to both the internal jugular vein and carotid artery. A, Artery; M, muscle; N, nerve; V, vein.

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3KUHQLFQHUYHVWXG\ Fig. 40.3  Phrenic neuropathy.  Phrenic motor studies in a patient with an elevated right hemidiaphragm, following right upper lobectomy. Note the lower amplitude and delayed response on the right compared with the left.

many of the indications for EDX studies in the ICU include assessment of respiratory muscle weakness and the failure to wean from the respirator. Neuromuscular etiologies of respiratory weakness include disorders of the anterior horn cell, peripheral nerve (generalized as in GBS and isolated as in the phrenic nerve), NMJ, and muscle. Ultrasound of the diaphragm is used (1) to assess the size of the muscle, (2) the degree of further thickening with inspiration, (3) the amount of excursion between inspiration and expiration, and (4) to assist in needle EMG of the diaphragm muscle itself.

Patients should be examined in the supine position. Supine is preferred over sitting for several reasons. Studies have shown that there is greater reproducibility and less side-­to-­side variability in the supine position. In addition, excursion of the diaphragm is greater in the supine compared with the sitting position for similar amounts of inspired air. Presumably, the abdominal organs located below the diaphragm slide more easily when supine. The diaphragm is a dome-­shaped muscle with a transverse septum/central tendon anteriorly and muscular body laterally and posteriorly. The area where the diaphragm lies adjacent to the ribcage is referred to as the zone of apposition (Fig. 40.4) and is the area where the diaphragm can best be visualized with ultrasound. During inspiration, the zone of apposition narrows as the dome-­shaped diaphragm descends and flattens (Fig. 40.5). The abdominal viscera (liver on the right, spleen on the left) normally lie just below the diaphragm at the zone of apposition. The chest wall and rostral diaphragm are lined by parietal pleura, whereas the inner abdominal wall is lined by peritoneum. These layers of connective tissue (pleura and peritoneum) cover the outer and inner borders of the diaphragm and are key in identifying the diaphragm with ultrasound. Using a high-­frequency linear probe in the sagittal or sagittal oblique plane, the diaphragm can be easily visualized between two adjacent ribs over the anterior axillary line, in the zone of apposition. Although the diaphragm can also be seen in the midaxillary line and the midclavicular line as well as over the posterior back, the anterior axillary line tends to be the optimal

Chapter 40 • Approach to Electrodiagnostic Studies in the Intensive Care Unit 723

location. The probe is placed over the inferior costal margin between the eighth and ninth ribs, or the seventh and eighth ribs. In this position, the probe can easily span two ribs, and visualize the hyperechoic bony margin of the ribs with their associated prominent posterior acoustic shadowing. Immediately below the skin is subcutaneous tissue. Deep to the subcutaneous tissue are two layers of intercostal muscles. Below the intercostal muscles is the diaphragm (Fig. 40.6). The diaphragm typically has a hyperechoic border both superiorly and inferiorly, which represent the parietal pleura and peritoneal membranes, respectively. In many patients, there may be a thin piece of hyperechoic connective tissue running in the center of the diaphragm.

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Fig. 40.4  Zone of apposition.  The area where the diaphragm lies adjacent to the ribcage is referred to as the zone of apposition. This is the area where the diaphragm can best be visualized with ultrasound. The chest wall and rostral diaphragm have a lining of parietal pleura (outer green line), whereas the inner abdominal wall is lined by peritoneum (inner green line). These layers of connective tissue (pleura and peritoneum) cover the outer and inner borders of the diaphragm and are key in identifying it with ultrasound. Note with the probe placed between two ribs on the right, the following tissues are seen from superficial to deep: skin, subcutaneous tissue, intercostal muscles, pleural lining, diaphragm, peritoneal lining, and liver.

Once the diaphragm is imaged, the size (i.e., thickness) of the muscle is measured at end expiration. In addition, the echogenicity of the diaphragm is assessed. Normal diaphragm has a similar echogenicity as other skeletal muscle. A normal thickness at end expiration is >2 mm. Any thickness below this, especially when associated with increased echogenicity, indicates atrophy and dysfunction of the diaphragm. The diaphragm is next observed during quiet inspiration and expiration. The patient is then asked to take deep breaths in and out while the diaphragm is visualized. Measurements of diaphragm thickness are then taken at the end of expiration and at the end of inspiration (Fig. 40.7). A “thickening ratio” percentage can then be calculated: ([thickness end inspiration – thickness end expiration]/[thickness end expiration] × 100). Normal diaphragm thickens in size >20% comparing end inspiration with end expiration. This is a very good objective test of diaphragmatic function, provided the patient can cooperate. It can be easily done on both the left and right sides. When one visualizes the diaphragm at the anterior axillary line, the liver is below the diaphragm on the right, and the spleen is below the diaphragm on the left. However, during deep inspiration, in some individuals, lung tissue will descend and “peel back” the diaphragm (Fig. 40.8). Remember the diaphragm is a dome-­shaped muscle. Thus, as it contracts, it flattens and moves downward. If the diaphragm dome moves down lower than the level of the probe, the diaphragm will disappear and will be replaced by homogeneous lung tissue. The next assessment of diaphragmatic function is excursion. For this assessment, M-­mode is used with a low-­frequency curvilinear probe (1–5 MHz range). The probe is placed subcostally at the midclavicular line. With the probe placed in this position, on the right side, the liver acts as an acoustic window. Beginning on the right side, when the probe is slightly rotated cranially, medially and posteriorly, a bright hyperechoic line is seen at the posterior side of the liver. This is the diaphragm. The index line of the M-­mode is placed over the bright hyperechoic line of the diaphragm. This echo is then recorded

Zone of apposition Expiration

Inspriation

Fig. 40.5  Zone of apposition changes with expiration and inspiration.  Left, At end expiration, the diaphragm is relaxed, dome shaped, and higher in the chest. The zone of apposition is large (black bracket). Right, During inspiration, the zone of apposition narrows as the dome shaped diaphragm descends and flattens.

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SECTION IX    Electromyography in Special Clinical Settings













Fig. 40.6  Normal diaphragm on ultrasound.  Left, Native image. Right, Same image with the diaphragm in red, intercostal muscles in purple, and bone echoes of the two ribs in green. Sagittal oblique view across the interspace between the seventh and eighth ribs at the anterior axillary line. The diaphragm typically has a hyperechoic border both superiorly and inferiorly. In many patients, there may be a thin piece of hyperechoic connective tissue running in the center of the diaphragm (light blue).



 



 



 



 

Fig. 40.7  Ultrasound of a normal diaphragm.  Top, Native images. Bottom, Same images with the diaphragm in red. Left, Inspiration. Right, Expiration. A normal thickness of the diaphragm is >2 mm at end expiration. The “thickening ratio” is calculated by comparing the thickness of the diaphragm at end inspiration with end expiration. Normal diaphragm thickens by >20% with end inspiration. In this case, the thickening ratio is 72%.

over time on M-­mode (Fig. 40.9) as the patient performs deep breathing for several cycles. Normally, the diaphragm moves toward the probe with inspiration. If the diaphragm moves away from the probe with inspiration (known as paradoxical movement of the diaphragm), this implies severe diaphragmatic dysfunction. The procedure is then repeated on the left side. However, the left side is frequently more challenging because there is no liver to act as an acoustic window. On the left side, the spleen is

used as an acoustic window, but the spleen is smaller and may not extend to the anterior axillary line. Thus obtaining a good acoustic window is much more challenging. When both sides are finished, the excursions are measured and compared from side to side. There is a normal range of excursion between inspiration and expiration. Normally, the left side moves more than the right side because the liver offers more resistance to movement on the right. Normal diaphragmatic excursion between

Chapter 40 • Approach to Electrodiagnostic Studies in the Intensive Care Unit 725

Fig. 40.8  Diaphragm and lung movement during deep inspiration.  Left, Sagittal oblique view across the interspace between the seventh and eighth ribs at the anterior axillary line, native images. Right, Same images with the diaphragm in. red, rib bone echo in (green), and lung tissue in (light blue). The top image is at the start of inspiration; the bottom image is at full inspiration. During deep inspiration, lung tissue can descend and “peel back” the diaphragm at some intercostal spaces. As the diaphragm is a dome-shaped muscle, it will flatten as it moves downward. If the ultrasound probe is at a level where the diaphragm dome moves lower than the probe, the diaphragm will disappear and will be replaced by homogeneous lung tissue.

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SECTION IX    Electromyography in Special Clinical Settings

Fig. 40.9  M-mode and excursion of the diaphragm.  Left, Normal patient. Right, Patient with near complete paralysis of the diaphragm. Each figure shows the B-mode image above with the M-mode image below. With the probe placed subcostally at the midclavicular line, the posterior diaphragm is seen as a bright line adjacent to the liver (red arrow) on B-mode. An index line (yellow arrow) is then placed so it intersects with the echo from the diaphragm. This is the line of ultrasound that is recorded over time in the M-mode image below. The bright line (green arrow) is the echo from the diaphragm over time. The patient performs deep breathing for several cycles. The normal range of excursion between inspiration and expiration is greater than 1.9 cm. In the normal patient on the left, the excursion was 3.1 cm; in the patient on the right with the near complete paralysis of the diaphragm, there was minimal excursion of 0.9 cm.

inspiration and expiration is >1.9 cm on each side. Any value >2.5 cm definitely excludes any diaphragmatic dysfunction. Comparing side to side, the left should normally move more than the right, but not by more than 50% on the left compared to the right. Movement more than 50% on the left compared with the right implies some dysfunction on the right. It is important to note that beyond baseline muscle thickness, assessing the thickness ratio and diaphragmatic excursion rely upon patient cooperation. Hence, these measures cannot be properly assessed in sedated patients. Likewise, if all breaths are delivered by the ventilator, these parameters cannot be assessed. Thickening ratio and excursion measurements are most useful when the patient’s respiratory status has improved to the point that they are on positive pressure support and weaning is being considered. M-­mode diaphragmatic studies can also be done during phrenic nerve conduction studies. In a study by Johnson and colleagues, the phrenic nerve was stimulated, recording the diaphragm CMAP, while simultaneously visualizing diaphragmatic excursion on M-­mode. Diaphragmatic excursion was actually a superior method of assessing phrenic nerve function when compared with phrenic nerve conduction studies. In general, CMAP amplitude and diaphragmatic excursion correlated well. There were no cases of an impaired phrenic CMAP amplitude without impaired diaphragmatic motion. However, there were some cases of abnormal diaphragmatic movement on ultrasound but with normal CMAP amplitudes on phrenic nerve conduction studies. This data strongly suggest that ultrasound may be

preferable to phrenic nerve conduction studies to optimally assess phrenic nerve function. Finally, ultrasound can be used either indirectly or directly during needle EMG of the diaphragm. One will note that in Chapter 13, needle EMG of the diaphragm was not included. It is true that the diaphragm can be a very useful muscle to study in patients with neuromuscular weakness. However, needle EMG of the diaphragm carries the potential complication of an inadvertent pneumothorax. Most often, patients who have a clinical indication for diaphragmatic EMG have respiratory issues at baseline. If a pneumothorax occurred, these patients would be even more respiratory compromised and much less likely to be able to tolerate such a complication. Thus, just as with any needle EMG study, one always needs to weigh the potential risks and benefits of doing the procedure. In our opinion, performing blind diaphragmatic EMG (although it is a well described and validated study) does not reach the necessary benefit/risk threshold. However, the benefit/risk ratio has increased with the use of ultrasound of the diaphragm when performing needle EMG. First, ultrasound can visualize the diaphragm muscle and indirectly aid in needle EMG placement. Ultrasound not only visualizes the diaphragm but also confirms that during inspiration the lung shadow does not appear. More importantly, it can measure the distance to the diaphragm from the skin surface. Thus, if the distance from the skin to the diaphragm is 20 mm, and a 25-­mm-­length needle is used, one can properly approximate how far the needle needs to go in to reach the diaphragm (Fig. 40.10). Just knowing this depth can be extremely helpful in getting to the right place

Chapter 40 • Approach to Electrodiagnostic Studies in the Intensive Care Unit 727

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Fig. 40.10  Diaphragmatic needle electromyography (EMG) and ultrasound.  Ultrasound can be used indirectly to aid needle EMG of the diaphragm. Ultrasound not only visualizes the diaphragm, but also confirms that during inspiration the lung shadow does not appear. More importantly, it can measure the distance between the skin surface and the diaphragm. Thus, if the distance from the skin to the diaphragm is 20 mm, and a 25-­mm-­length needle is used, one can properly approximate how far the needle needs to go in to reach the diaphragm.

and ensuring safety. In an extensive study of 150 individuals by Shahgholi and colleagues, the depth from the skin to the diaphragm ranged between 0.78 and 4.91 cm. As expected, as an individual’s body mass index increased, so did the distance to the diaphragm. This amount of variability among normal individuals reinforces the value of visualizing the diaphragm and measuring its depth before performing needle EMG. Second, ultrasound can also be used for direct needle EMG guidance. This indication is not unique to the diaphragm and can be done in the study of other muscles. In this situation, ultrasound is used simultaneously as the needle is placed into the muscle. Direct ultrasound guidance can be done using either the “in-­plane” or “out-­of-­plane” technique (Fig. 40.11). With the in-­plane technique, the needle is inserted at a very shallow angle at the middle of the end of the probe and kept parallel to the length of the probe. With this technique, the needle can be seen at all times as it passes through the subcutaneous tissue, underlying muscle, and eventually to the target of interest. This technique requires a longer needle and insertion of the needle at a much shallower angle than usual. In addition, because the width of the ultrasound beam is so narrow (i.e., the width of a credit card), it can be difficult to keep the entire needle on the screen at all times. With the out-­of-­plane technique, the needle is inserted at a much more acute angle, just adjacent to the middle of

Fig. 40.11  Direct needle electromyography guidance with ultrasound.  Ultrasound can be used simultaneously to guide the needle into the muscle. Direct ultrasound guidance can be done with either the “in-­plane” or “out-­of-­plane” technique. Right, Using the in-­plane technique, the needle is inserted at a very shallow angle at the middle of the end of the probe and kept parallel to the length of the probe. With this technique, the needle can be seen at all times as it passes through the subcutaneous tissue, underlying muscle, and eventually to the target of interest. Left, Using the out-­of-­plane technique, the needle is inserted at a much more acute angle just adjacent to the middle of the probe, aimed toward the probe. As the needle is advanced, the needle tip will eventually appear. This will be recognized as a bright hyperechoic spot on ultrasound. However, as the needle is advanced, that same bright hyperechoic spot remains the same. One cannot difference between the tip of the needle and the shaft of the needle. To do this technique correctly, one needs to identify the first time that the needle tip is seen, and then ever so slightly move the probe away from the needle, and insert the needle further until the needle tip is again first seen. This technique is known as “walking down” the needle until it reaches the area of interest

the probe aimed toward the probe. One needs to follow the image extremely closely. As the needle is advanced, the needle tip will eventually appear. The tip of the needle will be recognized as a bright hyperechoic spot on ultrasound. However, as the needle is advanced, that same bright hyperechoic spot remains the same. One cannot differentiate between the tip of the needle and the shaft of the needle. To perform this technique correctly, one needs to identify the first time the needle tip is seen, and then ever so slightly move the probe away from the needle, and insert the needle a bit further until the needle tip is again first seen. This technique is known as “walking down” the needle until it reaches the area of interest. As needles are hard and smooth, artifacts are often encountered. The most common is reverberation artifact for the in-­plane technique and comet tail artifact for the out-­of-­plane technique (see Chapter 17). There are several common clinical scenarios where ultrasound of the diaphragm can add key information. Patients with chronic unilateral phrenic palsies have atrophic and hyperechoic diaphragms on the affected side, which will not increase in thickness with inspiration. On M-­mode, there is little excursion compared with the contralateral side. If needle EMG of the diaphragm is done, acute and/or chronic neurogenic findings will be present. In cases of myopathy affecting respiratory function, both sides of the diaphragm may show atrophy and hyperechoic changes. However, in these cases, needle EMG of the diaphragm may show a myopathic pattern.

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SECTION IX    Electromyography in Special Clinical Settings

In addition, diaphragmatic ultrasound may be useful in assessing respiratory function in critical care patients, especially when attempting to wean from the ventilator. During mechanical ventilation in patients without any neuromuscular condition, the diaphragm has been shown to begin to atrophy within a few days. Reduced thickening ratios and diaphragmatic excursion are associated with a higher likelihood of being unable to wean. It is important to note that all the techniques described earlier for ultrasound of the diaphragm in the ICU can also be used in the occasional outpatient with respiratory insufficiency who is being evaluated for potential neuromuscular etiologies.

Suggested Readings Amirjani N, Hudson AL, Butler JE, Gandevia SC. An algorithm for the safety of costal diaphragm electromyography derived from ultrasound. Muscle Nerve. 2012;46(6):856–860. Bolton CF. Sepsis and the systemic inflammatory response syndrome: neuromuscular manifestations. Crit Care Med. 1996;24:1408–1416. Bolton CF. Critical illness polyneuropathy: a useful concept. Muscle Nerve. 1999;4:419–422. Bolton CF. Neuromuscular manifestations of critical illness. Muscle Nerve. 2005;32:140–163. Boon AJ, Alsharif KI, Harper CM, Smith J. Ultrasound-­guided needle EMG of the diaphragm: technique description and case report. Muscle Nerve. 2008;38(6):1623–1626. Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ. Two-­dimensional ultrasound imaging of the diaphragm: quantitative values in normal subjects. Muscle Nerve. 2013;47(6):884–889. Canella C, Demondion X, Delebarre A, et al. Anatomical study of phrenic nerve using ultrasound. Eur Radiol. 2010;20:659–665. Johnson NE, Utz M, Patrick E, et al. Visualization of the diaphragm muscle with ultrasound improves diagnostic accuracy of phrenic nerve conduction studies. Muscle Nerve. 2014;49(5):669–675. Khan J, Harrison TB, Rich MM, et al. Early development of critical illness myopathy and neuropathy in patients with severe sepsis. Neurology. 2006;67:1421–1425.

Kramer CL, Boon AJ, Harper CM, Goodman BP. Compound muscle action potential duration in critical illness neuromyopathy. Muscle Nerve. 2018;57(3):395–400. Lacomis D. Electrophysiology of neuromuscular disorders in critical illness. Muscle Nerve. 2013;47(3):452–463. Lacomis D, Giuliani MJ, Van Corr A, et al. Acute myopathy of intensive care: clinical, electromyographic, and pathologic aspects. Ann Neurol. 1996;40:645–654. Lacomis D, Smith TW, Chad DA. Acute myopathy and neuropathy in status asthmaticus: case report and literature review. Muscle Nerve. 1993;16:84–90. Lacomis D, Zochodne DW, Bird SJ. Critical illness myopathy. Muscle Nerve. 2000;23:1785–1788. Llamas-­Álvarez AM, Tenza-­Lozano EM, Latour-­Pérez J. Diaphragm and lung ultrasound to predict weaning outcome: systematic review and meta-­analysis. Chest. 2017;152(6):1140–1150. Ojha A, Zivkovic SA, Lacomis D. Electrodiagnostic studies in the intensive care unit: a comparison study 2 decades later. Muscle Nerve. 2018;57(5):772–776. Resman-­Gaspersc A, Podnar S. Phrenic nerve conduction studies: technical aspects and normative data. Muscle Nerve. 2008;37:36–41. Rich MM, Bird SJ, Raps EC, et al. Direct muscle stimulation in acute quadriplegic myopathy. Muscle Nerve. 1997;20:665–673. Rich MM, Teener JW, Raps EC, et al. Muscle is electrically inexcitable in acute quadriplegic myopathy. Neurology. 1996;46:731–736. Sarwal A, Walker FO, Cartwright MS. Neuromuscular ultrasound for evaluation of the diaphragm. Muscle Nerve. 2013;47(3):319–329. Segredo V, Caldwell JE, Matthay MA, et al. Persistent paralysis in critically ill patients after long term administration of vecuronium. N Engl J Med. 1992;323:524–528. Shahgholi L1, Baria MR, Sorenson EJ, et al. Diaphragm depth in normal subjects. Muscle Nerve. 2014;49(5):666–668. Ueki J, De Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax. 1995;50:1157–1161. Walker F, Cartwright MS. Neuromuscular Ultrasound. Saunders; 2011. Zochodne DW, Bolton CF, Wells GA, et al. Critical illness polyneuropathy: a complication of sepsis and multiple organ failure. Brain. 1987;110:819–841.

SECTION IX • Electromyography in Special Clinical Settings

Approach to Pediatric Electromyography In conjunction with the clinical examination, electrodiagnostic (EDX) studies frequently play a key role in the evaluation of neuromuscular disorders in infants and children. Indeed, there are a large number of neuromuscular disorders that present in the pediatric age group. In many of these cases, EDX studies are used to help guide further evaluation (e.g., muscle biopsy, genetic testing); less commonly, they can make a definitive diagnosis. A complete discussion of pediatric neuromuscular disorders and electrodiagnosis is beyond the scope and purpose of this chapter (see Suggested Readings). Although the fundamental principles of EDX studies are the same for pediatric and adult age groups, there are significant differences that the electromyographer needs to keep in mind when studying infants and children. These differences include both physiologic and nonphysiologic factors that may vary considerably between age groups. In addition, neuromuscular ultrasound can potentially be a very useful adjunct in assessing children with certain suspected neuromuscular disorders.

NEUROMUSCULAR DIAGNOSES ARE DIFFERENT IN CHILDREN COMPARED WITH ADULTS

The most common referral diagnoses to the typical electromyography (EMG) laboratory include radiculopathy, polyneuropathy, and carpal tunnel syndrome. However, adults are more commonly studied in the EMG laboratory, so this group of diagnoses reflects neuromuscular conditions seen in the adult age group. In contrast, the neuromuscular disorders seen in children often are different. For example, entrapment neuropathies are very common in adults but are extremely rare in children. Likewise, radiculopathy, probably the most common of all EMG referral diagnoses, is virtually unheard of in children, except in cases of trauma. Although peripheral neuropathies occur in children, they are most often genetic, whereas most peripheral neuropathies in adults referred to the EMG laboratory are acquired disorders, usually toxic, metabolic, inflammatory, or associated with other coexistent medical illnesses. Unlike adults, the more common diagnoses in children referred to the EMG laboratory are inherited disorders of the motor unit, including the anterior horn cell (e.g., spinal muscular atrophy), peripheral nerve (e.g., Charcot-­Marie-­Tooth [CMT]), or muscle (e.g., muscular dystrophy).

41

Children with neuromuscular disorders often present clinically as a delay in motor milestones. In many cases, it may not be clear from the symptoms and signs whether the etiology is central or peripheral. One of the best examples of this predicament is that of the floppy infant, in whom the differential diagnosis includes the entire length of the neuraxis, from brain to muscle. In this regard, EDX studies often are helpful in differentiating peripheral from central etiologies and, accordingly, guiding the subsequent evaluation in a useful and logical direction. 

MATURATION ISSUES When studying children, it is essential to appreciate what is normal for what age. This is especially important when interpreting conduction velocities and differentiating a normal conduction velocity from axonal loss or demyelination. Most adult electromyographers who study adults are well versed in the EDX criteria for demyelination:    • Conduction velocities less than 75% the lower limit of normal • Distal latencies and late responses greater than 130% the upper limit of normal • Conduction block, which signifies not only demyelination but acquired demyelination    However, infants and young children often have slowed conduction velocities that would be considered in the “demyelinating range” for adults. In most cases, this is not because infants and young children have demyelinated nerves; rather, they have nerves that have yet to be myelinated in the first place. The process of myelination is age dependent, beginning in utero, with nerve conduction velocities in full-­term infants approximately half that of adult normal values. Accordingly, nerve conduction velocities of 25–30 m/s are normal at birth. Conduction velocity rapidly increases after birth, reaching approximately 75% of adult normal values by age 1 year, and the adult range by age 3–5 years, when myelination is complete. Accordingly, when a child is studied in the EMG laboratory, it is essential that age-­based normal control values are used (Tables 41.1 and 41.2). One interesting aspect of myelin maturation is often observed during nerve conduction studies in the pediatric population. Many are familiar with the fact that

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SECTION IX    Electromyography in Special Clinical Settings

730

Table 41.1  Pediatric Motor Conduction Studies by Age. Median Nerve Age

DML (ms)

CV (m/s)

Peroneal Nerve

F (ms)

AMP (mV)

DML (ms)

CV (m/s)

F (ms)

AMP (mV)

16.12 (1.5)

3.00 (0.31)

2.43 (0.48)

22.43 (1.22)

22.07 (1.46)

3.06 (1.26)

7 days–l month

2.23 (0.29)a 25.43 (3.84)

1–6 months

2.21 (0.34)

34.35 (6.61)

16.89 (1.65)

7.37 (3.24)

2.25 (0.48)

35.18 (3.96)

23.11 (1.89)

5.23 (2.37)

6–12 months

2.13 (0.19)

43.57 (4.78)

17.31 (1.77)

7.67 (4.45)

2.31 (0.62)

43.55 (3.77)

25.86 (1.35)

5.41 (2.01)

1–2 years

2.04 (0.18)

48.23 (4.58)

17.44 (1.29)

8.90 (3.61)

2.29 (0.43)

51.42 (3.02)

25.98 (1.95)

5.80 (2.48)

2–4 years

2.18 (0.43)

53.59 (5.29)

17.91 (1.11)

9.55 (4.34)

2.62 (0.75)

55.73 (4.45)

29.52 (2.15)

6.10 (2.99)

4–6 years

2.27 (0.45)

56.26 (4.61)

19.44 (1.51) 10.37 (3.66)

3.01 (0.43)

56.14 (4.96)

29.98 (2.68)

7.10 (4.76)

6–14 years

2.73 (0.44)

57.32 (3.35)

23.23 (2.57) 12.37 (4.79)

3.25 (0.51)

57.05 (4.54)

34.27 (4.29)

8.15 (4.19)

aData

are provided as mean (SD). AMP, Amplitude; CV, conduction velocity; DML, distal motor latency; F, F latency. From Parano E, Uncini A, DeVivo DC, Lovelace RE. Electrophysiologic correlates of peripheral nervous system maturation in infancy and childhood. J Child Neurol. 1993;8:336–338.

Table 41.2  Pediatric Sensory Conduction Studies by Age. Median Nerve

Sural Nerve

CV (m/s)

AMP (μV)

CV (m/s)

7 days–l month

22.31 (2.16)a

6.22 (1.30)

20.26 (1.55)

9.12 (3.02)

1–6 months

35.52 (6.59)

15.86 (5.18)

34.63 (5.43)

11.66 (3.57)

6–12 months

40.31 (5.23)

16.00 (5.18)

38.18 (5.00)

15.10 (8.22)

1–2 years

46.93 (5.03)

24.00 (7.36)

49.73 (5.53)

15.41 (9.98)

2–4 years

49.51 (3.34)

24.28 (5.49)

52.63 (2.96)

23.27 (6.84)

4–6 years

51.71 (5.16)

25.12 (5.22)

53.83 (4.34)

22.66 (5.42)

6–14 years

53.84 (3.26)

26.72 (9.43)

53.85 (4.19)

26.75 (6.59)

Age

AMP (μV)

aData

are provided as mean (SD). AMP, Amplitude; CV, conduction velocity. From Parano E, Uncini A, DeVivo DC, Lovelace RE. Electrophysiologic correlates of peripheral nervous system maturation in infancy and childhood. J Child Neurol. 1993;8:336–338.

different white matter tracts in the central nervous system myelinate at different times. Indeed, one can often use the pattern of myelination on a brain MRI scan to correctly predict the age of a young child. Similarly, different fibers in the peripheral nervous system myelinate at different times as well. In the EMG laboratory, this often manifests as a bifid morphology (i.e., two separate peaks) on sensory nerve action potentials (SNAPs) in infants and children (Fig. 41.1). This bifid morphology is due to some fibers having already been fully myelinated (the first peak), whereas others have not and trail behind (i.e., the second peak). It is not unusual to see bifid SNAPs between the ages of 3 months and 4–6 years. These bifid SNAPs are a completely normal finding. Eventually, as the fibers in the second peak fully myelinate, the second peak moves to the left and merges with the first peak. This forms a larger sensory response, as is typically seen in adults.

—9 PV

Fig. 41.1  Sural sensory nerve action potential in a young child.  Note the bifid morphology. These bifid sensory responses are a completely normal finding between the ages of 3 months through 4–6 years. They occur as different populations of fibers myelinate at different times. Eventually, the group of fibers in the second peak will fully myelinate. At that point, the second peak will move to the left and merge with the first peak to form a larger sensory response.

Chapter 41 • Approach to Pediatric Electromyography 731

As with adults, the F response can be easily studied in children. Although the F response often is thought of as evaluating the proximal nerve segments, it assesses the entire length of the nerve, from the stimulation point to the spinal cord and back, and then past the stimulation point to the muscle. Thus, the F response latency depends not only on the conduction velocity and distal latency but also on the length of the limb. Because infants and children have slower conduction velocities than adults, one would expect the F responses to be very long. However, counterbalancing this is the very short limb length of a child compared with an adult. Thus, there are two opposing influences on the F response in children: limb length and conduction velocity. In infants and young children, the influence of the limb length is more overriding, resulting in F-­wave latencies that are much shorter in children than adults (typically in the range of 16–19 ms in the upper extremities). Thus, whenever an F response is performed on a child, it is essential to compare it with normal control values for the child’s age or height. The most important maturation issue for the needle EMG portion of the examination is the size of the motor unit. It is no surprise that the physical size of a motor unit of a newborn is much smaller than that of an adult. Transverse motor unit territory increases greatly with age, doubling from birth to adulthood, mostly because of the increase in individual muscle fiber size. Thus, normal motor unit action potentials (MUAPs) in infants typically are very small, representing the physical size of the motor unit. Indeed, in infants, it is often difficult to differentiate normal MUAPs from myopathic ones. This once again underscores that when one interprets EDX findings in children, including MUAPs, it is essential to use age-­based normal control values (Table 41.3). 

TECHNICAL ISSUES A large number of unique technical issues must be kept in mind when studying infants and children so that reliable and accurate data can be obtained. The first important issue is measurement of distances and its relationship to technical errors. Because a child’s limb is much smaller than an adult’s, much shorter distances are used. When short distances are used, a small error in measurement creates a much larger error in computed conduction velocities than when longer distances are used. For instance, in an adult, if the distance between the wrist and the elbow is measured at 20 cm but is off by 1 cm (i.e., the true measurement is 21 cm), this results in an error of 5% when calculating a conduction velocity. However, in a newborn baby, if the measured distance is 7 cm but is off by 1 cm (i.e., the true measurement is 8 cm), the error in conduction velocity increases to 14%. Thus one needs to be especially careful when measuring distances in children. Second, smaller electrodes often are needed in infants and young children because their limbs and muscles are so small. The typical bar electrode that has the active and reference contacts separated by 2.5 cm often is too large for most infants and small children (Fig. 41.2). Standard 10-­mm disc electrodes often will suffice for most ages, except for newborns, in whom smaller electrodes generally are needed. Likewise, the standard adult stimulator often is too large for infants and young children because of the size of the prongs and the distance between the cathode and anode. Often, it is preferable to use a pediatric-­sized stimulator so that the nerve of interest is more accurately stimulated (Fig. 41.3). Because a child’s limbs are so much smaller than an adult’s, one needs to take great care when stimulating the nerves. The stimulus intensity needs to be kept as low as

Table 41.3  Mean Motor Unit Action Potential Duration Based on Age and Muscle Group. Age of Subjects (yrs)

Arm Muscles (ms) Deltoid

Leg Muscles (ms)

Biceps

Triceps

Thenar

ADM

Quad, BF

Gastroc

Tib Ant

Per Long

EDB

Facial

0–4

7.9–10.1

6.4–8.2

7.2–9.3

7.1–9.1

8.3–10.6

7.2–9.2

6.4–8.2

8.0–10.2

6.8–7.4

6.3–8.1

3.7–4.7

5–9

8.0–10.8

6.5–8.8

7.3–9.9

7.2–9.8

8.4–11.4

7.3–9.9

6.5–8.8

8.1–11.0

5.9–7.9

6.4–8.7

3.8–5.1

10–14

8.1–11.2

6.6–9.1

7.5–10.3

7.3–10.1

8.5–11.7

7.4–10.2

6.6–9.1

8.2–11.3

5.9–8.2

6.5–9.0

3.9–5.3

15–19

8.6–12.2

7.0–9.9

7.9–11.2

7.8–11.0

9.0–12.8

7.8–11.1

7.0–9.9

8.7–12.3

6.3–8.9

6.9–9.8

4.1–5.7

20–29

9.5–13.2

7.7–10.7

8.7–12.1

8.5–11.9

9.9–13.8

8.6–12.0

7.7–10.7

9.6–13.3

6.9–9.6

7.6–10.6 4.4–6.2

30–39

11.1–14.9

9.0–12.1 10.2–13.7 10.0–13.4 11.6–15.6 10.1–13.5

9.0–12.1 11.2–15.1

8.1–10.9

8.9–12.0 5.2–7.1

40–49

11.8–15.7

9.6–12.8 10.9–14.5 10.7–14.2 12.4–16.5 10.7–14.3

9.6–12.8 11.9–15.9

8.6–11.5

9.5–12.7 5.6–7.4

50–59

12.8–16.7 10.4–13.6 11.8–15.4 11.5–15.1 13.4–17.5 11.6–15.2 10.4–13.6 12.9–16.9

9.4–12.2 10.3–13.5 6.0–7.9

60–69

13.3–17.3 10.8–14.1 12.2–15.9 12.0–15.7 13.9–18.2 12.1–15.8 10.8–14.1 13.4–17.5

9.7–12.7 10.7–14.0 6.3–8.2

70–79

13.7–17.7 11.1–14.4 12.5–16.3 12.3–16.0 14.3–18.6 12.4–16.1 11.1–14.4 13.8–17.9 10.0–13.0 11.0–14.3 6.5–8.3

ADM, Abductor digiti minimi; BF, biceps femoris; EDB, extensor digitorum brevis; Gastroc, gastrocnemius; Per long, peroneus longus; Quad, quadriceps; Tib ant, tibialis anterior. Reprinted with permission from Buchthal F, Rosenfalck P. Action potential parameters in different human muscles. Acta Psych Neurol Scand. 1955;30(1–2):125–131.

732

SECTION IX    Electromyography in Special Clinical Settings

%DU PP HOHFWURGH GLVFHOHFWURGHV Fig. 41.2  Pediatric electrodiagnostic studies and recording electrode size.  The standard bar electrode (left) and 10-­mm disc electrodes (middle) are compared to the size of an infant’s hand (right). Smaller electrodes may be needed in infants and young children because their limbs and muscles are so small. Standard 10-­mm disc electrodes often will suffice for most age groups, including infants. In newborns, however, smaller electrodes are needed. Other standard electrodes, like the bar electrode, are too large for a newborn or infant’s hand.

3HGLDWULF 6WDQGDUG ,QIDQW \HDUROG $GXOW VWLPXODWRU VWLPXODWRU Fig. 41.3  Pediatric electrodiagnostic studies and stimulator size.  The standard stimulator can be used for adults and most children. However, for infants and young children, it is preferable to use a pediatric-­sized stimulator so that the nerve of interest is more accurately stimulated.

possible, for patient cooperation and tolerance but also to prevent costimulation of nearby nerves. Costimulation of nerves is much more likely to occur in a young infant or child than in an adult, even at low intensities, because of the small size of the limb and the close physical proximity of the nerves to each other. During the needle EMG examination, additional technical issues arise. Because the physical size of the motor units in children is quite small, it is often very difficult,

even for the most experienced pediatric electromyographer, to differentiate normal MUAPs from myopathic MUAPs, especially in infants. Decreased recruitment and large MUAPs, as seen in neuropathic conditions, are much more straightforward and easier to appreciate in infants and children than normal or myopathic MUAPs in this population. Because individual muscle fibers are so small in infants and children, another common problem that arises in pediatric EMG is the differentiation between fibrillation potentials and endplate spikes. The endplate zone in infants takes up a disproportionately large territory of the muscle compared with adults. Thus, it is not uncommon to encounter endplate potentials when studying pediatric patients. Endplate spikes can easily mimic fibrillation potentials. One needs to pay especially close attention to the firing pattern (regular vs. irregular) and the initial waveform deflection (positive vs. negative) to properly differentiate fibrillation potentials from endplate spikes. Because fibrillation potentials signify active denervation, it is essential not to mistake endplate spikes for fibrillation potentials, especially in the pediatric population, where such findings may portend a particularly serious diagnosis, such as infantile spinal muscular atrophy (Werdnig-­Hoffmann disease). 

APPROACH TO THE CHILD AS A PATIENT

Although many adults are apprehensive of EDX studies, most tolerate the study well, with minimal discomfort. In adults, explaining the test in advance and as it proceeds is often one of the most helpful ways of allaying any fears and creating good patient rapport. However, a different approach must be taken to allay fears and create rapport with an infant or child in the EMG laboratory. As most children are accompanied by their parent(s), it is often extremely helpful to have a parent in the room with the child. The parent can help comfort the child and be a valuable asset to the electromyographer. The electromyographer also might consider removing his or her white coat before entering the examination room. Speaking with the child in a supportive and comforting manner, using uncomplicated words and phrases, will help allay the child’s fears. Of course, the task is much more difficult in infants, who cannot understand the situation, and in these cases, having a parent in the room is extremely valuable. There are a few helpful techniques that can be used with children to gain their cooperation. When performing the nerve conduction studies, the electromyographer can explain to the child that the stimulator will feel like a tap, buzz, or static electricity, similar to when he or she rubs their feet along the floor and then touches the refrigerator. It is best to avoid the word “shock” when explaining the nerve conduction part of the study, because the term likely has negative connotations for both children and adults. One extremely effective maneuver is to have the child hold the stimulator and

Chapter 41 • Approach to Pediatric Electromyography 733 7DUJHWSODVPDFRQFHQWUDWLRQ

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stimulate the examiner’s median nerve at the wrist, using a low-­stimulus current. In this way, the child can see the muscle twitch. More importantly, the child will see that the examiner is not distressed by the experience (hopefully). In children aged 5–10 years, we routinely have them stimulate our own nerves before we begin the study. One will find that the parent in the room often is also interested in knowing what the stimulator feels like on themselves. Regarding the needle part of the test, the word “needle” should always be avoided. No one likes needles, including children. Children are very familiar with needles, usually receiving one or more vaccinations almost every time they visit their pediatrician. It is best to use the word “electrode” or “microphone” when describing the needle part of the examination. If a child is told that a very small microphone is going to be put into his or her muscle so that he or she will be able to hear the muscles along with you, the child may become very interested and engaged in the test. The most difficult age for EDX studies is between the ages of 2 and 6 years. In the infant, who cannot understand and who also cannot move around very much, EDX studies usually can be done fairly easily and quickly, with minimal discomfort to the infant, with an assistant helping immobilize the limb being studied. However, in rambunctious toddlers, EDX studies can be very difficult without their cooperation. Indeed, in this age group, conscious sedation often is very helpful. In the past, a mild sedative such as chloral hydrate was often used. This form of sedation usually was inadequate, with the child often sleeping well on the ride home after the study but not during the study. In the modern day, conscious sedation with propofol (Diprivan), under the supervision of an anesthesiologist, can be used to obtain good data with minimal discomfort to the child. Propofol is an intravenous sedative-­hypnotic agent used for induction of anesthesia or for sedation. Its major advantage is that it produces hypnosis rapidly, usually within 40 seconds from the start of the injection. As with other rapidly acting intravenous anesthetic agents, the half-­time of the blood-­brain equilibration is approximately 1–3 minutes. While the child is sedated with propofol, nerve conduction studies and/or repetitive nerve stimulation studies can be performed easily. Likewise, the needle EMG study can be performed, looking for abnormal spontaneous activity, while the child is sedated. The propofol then can be turned down, and, as the child is coming out of the sedation, MUAPs can be analyzed (Fig. 41.4). Pediatric EMG nevertheless remains a challenge even if these recommendations are followed. The more experience one has with children, the easier the testing goes. In pediatric EMG, more than in any other situation, it is important to always follow the Willie Sutton rule: Go where the money is! One needs to carefully choose the nerves and muscles to study based on the following:    • Which studies are essential to help support or exclude a diagnosis?

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   0LQXWHV Fig. 41.4  Propofol plasma concentration kinetics.  Under the direction of an anesthesiologist, propofol can be used successfully to sedate young children undergoing electrodiagnostic studies. Its major advantage is that it produces a rapid hypnosis. Upon stopping the infusion, the concentration rapidly declines and the child begins to awaken within a few minutes. While the child is sedated, nerve conduction studies, repetitive nerve stimulation studies, and needle electromyography (assessing spontaneous activity) can be performed. As the child begins to awaken, motor unit action potentials can be analyzed. 



• W  hich nerve conduction studies are the fastest and easiest to perform? • Which muscles are the easiest to activate and the least painful to study?    For example, the median motor nerve is much easier to stimulate and record than the tibial motor nerve, which is difficult and painful to stimulate behind the popliteal fossa. Likewise, it is important to choose muscles that are less painful and easier to activate than others. For instance, the first dorsal interosseous (FDI) and the abductor pollicis brevis (APB) both are distal upper extremity C8–T1-­innervated muscles. However, the FDI is much less painful to sample than the APB. In children, it is always best to purposefully choose the least painful muscles to examine, unless it is absolutely necessary to examine a muscle that is known to be painful. In addition, it is important to choose muscles that are easy to activate. In children who cannot cooperate, it often is useful to choose muscles that can be activated by withdrawing to a sensory stimulus. For instance, tickling the foot will result in contraction of the tibialis anterior and hamstring muscles as the child reflexively pulls his or her leg away. One of the most important rules in pediatric EMG is: “Take what you can get, when you can get it!” When examining an adult, the electromyographer is accustomed to placing the needle electrode in the muscle, looking first at insertional and spontaneous activity, and then changing the gain to 200 μV per division while having the patient contract to look at the MUAPs. In a child, if one puts the needle electrode into a muscle and MUAPs are firing, do not try to get the child to relax the muscle. It is much more productive to quickly change the sensitivity to 200 μV per division and look at the MUAPs while they are firing because you might not get another chance! Do not expect to follow the same regular routine in a child that you normally would follow in an adult. 

734

SECTION IX    Electromyography in Special Clinical Settings

GOALS OF THE PEDIATRIC ELECTRODIAGNOSTIC EXAMINATION

The goals of the EDX study in infants and children are similar to those in adults. The first goal is to discern if a neuromuscular disorder is present. Differentiating between a central and peripheral cause of weakness is of prime importance to the referring physician. If the problem is peripheral, the next goal is to determine if the pathology is neuropathic, myopathic, or due to a disorder of the neuromuscular junction. This differentiation then allows for a more efficient and logical use of further laboratory testing. If the condition is neuropathic, the next goal is to determine if motor, sensory, or a combination of fibers is involved. This relies primarily on whether SNAPs are present, reduced, or absent. Take the example of a young child with diffuse denervation and reinnervation on needle EMG associated with low motor amplitudes on nerve conduction studies. Taken together, these findings denote a neuropathic process. If the SNAPs are normal, then the disorder most likely localizes to the anterior horn cells. Although these findings also might be seen in a pure motor neuropathy, this would be very unlikely in an infant or child. On the other hand, if the SNAPs are abnormal, then a peripheral neuropathy likely is present, which has a very different differential diagnosis and prognosis. If a peripheral neuropathy is present, the next important piece of information to discern from the EDX study is whether or not the pathology is demyelinating. Because so many pediatric peripheral neuropathies are genetic in nature, and because the demyelinating forms of CMT disease are the most common, the presence of conduction velocities in the demyelinating range has great importance. Of course, there also are instances of acquired demyelinating neuropathies in children, which can usually be distinguished from genetic forms of demyelinating neuropathy using the same guidelines that apply to adults (see Chapter 29). In general, there is a very good correlation between the results of EDX studies and the final diagnosis. This is especially true for neuropathic disorders (i.e., anterior horn cell disorders and peripheral neuropathy). They are also helpful but not as good for myopathic disorders, especially in children younger than age 2. As noted earlier, motor units in young children are normally quite small, making the differentiation between normal and myopathic MUAPs very demanding. In addition, some myopathies are fairly “bland” on needle EMG, most often the congenital myopathies. This is in contradistinction to muscular dystrophies and myositis, which are much more easily recognized as myopathic on needle EMG. 

TRENDS IN PEDIATRIC ELECTRODIAGNOSIS

One might think that in the present era of molecular genetics wherein DNA and other forms of genetic analysis are available for many of the inherited neuromuscular conditions (e.g., spinal muscular atrophy, many of the muscular dystrophies, and many forms of CMT disease), EDX studies would play less of a role than in the past. This is true for the infant or

child who has a classic phenotype of a well-­known inherited disorder. In these cases, especially if there is a definitive family history, the diagnosis can often be confirmed by genetic testing, without the need for EDX studies. However, this does not occur in all cases. In the evaluation of a child with weakness or a delay in motor milestones, EDX studies still play a major role in guiding the evaluation process in a logical and efficient manner. In addition, EDX studies continue to play a key role in the evaluation of both acquired (e.g., Guillain-­Barré syndrome and chronic inflammatory demyelinating polyneuropathy) and some inherited demyelinating neuropathies. For instance, Dejerine-­Sottas syndrome (DSS) is a term applied to a group of genetically heterogeneous demyelinating neuropathies that typically present in infancy or early childhood. DSS can easily mimic the clinical presentation of Werdnig-­Hoffman (spinal muscular atrophy type 1). However, DSS is associated with the slowest conduction velocities ever recorded in humans, typically less than 12 m/s and usually less than 6 m/s. The finding of such slowed conduction velocities on nerve conduction studies will immediately point to the diagnosis of DSS. Afterward, appropriate genetic testing can be undertaken looking for the known mutations associated with DSS, which include mutations of the MPZ, PMP22, and EGR2 genes, among others. One of the most interesting recent studies in pediatric EDX studies comes from Karakis and colleagues, who looked at referral and diagnostic trends over a decade at Boston Children’s Hospital, a large tertiary referral center. The proportion of children younger than age 5 who had EDX studies dropped markedly by approximately 50% over the decade, likely reflecting the increased availability of genetic testing and number of disorders that can be screened. However, the proportion of children older than age 10 years who had EDX studies more than doubled. The most common referral questions in this age group were polyneuropathy, followed by mononeuropathy, and then nonspecific musculoskeletal complaints. Radiculopathy and plexopathy were very uncommon. Interestingly, in their study, only 5% of patients required conscious sedation, likely reflecting the increased number of older children. The conclusion of their study was that EDX studies continue to play a pivotal role in childhood neuromuscular disorders, although the practice paradigm is shifting from younger to older children. Without doubt, the pediatric EDX study is much more challenging and difficult to perform than a similar study in an adult. However, being aware of the unique maturational and technical issues associated with studying infants and children and approaching the examination with a different philosophy will offer the electromyographer the same kinds of useful information that can be obtained in adults. 

ULTRASOUND CORRELATIONS Neuromuscular ultrasound has the potential to be a very useful adjunct in assessing children with suspected neuromuscular disorders. As the field of neuromuscular ultrasound is evolving, there are few ultrasound studies of

Chapter 41 • Approach to Pediatric Electromyography 735

Table 41.4  Nerve Cross-­sectional Area in Children. Age 0–3 years

Age 4–6 years

Age 7–11 years

Age 12–16 years

N

Mean (SD)

N

Mean (SD)

N

Mean (SD)

N

Mean (SD)

Median wrist

7

3.9 (1.1)

7

4.7 (1.0)

6

5.1 (0.2)

3

6.7 (0.6)

Median forearm

7

4.0 (0.9)

6

5.6 (1.9)

7

6.2 (1.5)

4

9.1 (2.3)

Ulnar wrist

2

2.5 (0.7)

2

4.5 (0.7)

2

3.5 (0.7)

6

5.8 (1.5)

Ulnar elbow

2

3.5 (0.7)

1

4.5 (0.7)

3

5.0 (2.0)

5

7.2 (1.3)

Radial groove

2

4.0 (0.0)

3

3.7 (1.5)

5

5.0 (0.7)

3

8.7 (1.5)

Sciatic leg

2

19.0 (2.8)

2

30.5 (7.8)

3

30.7 (7.5)

1

8.7 (1.5)

Fibular knee

2

7.0 (1.4)

1

9.0 (1.7)

4

10.0 (2.9)

3

6.7 (3.1)

Tibial knee

2

11.5 (2.1)

1

9.0 (1.7)

4

19.5 (6.6)

3

19.7 (9.0)

Tibial ankle

2

7.5 (0.7)

3

9.0 (1.7)

4

7.5 (2.5)

5

12.6 (2.1)

Note: The authors emphasized that there were few data points at each site for a given age. Therefore, these data should not be used to generate cutoff values for abnormal enlargement, but rather to provide a starting point for each laboratory to generate its own reference values. Adapted from Cartwright MS, Mayans DR, Gillson NA, Griffin LP, Walker FO. Nerve cross-­sectional area in extremes of age. Muscle Nerve. 2013;47(6):890–893.



1HUYH&6$PP

children, in contrast to the hundreds of papers now published every year dealing with adult neuromuscular conditions. However, since ultrasound is painless, it may offer particular advantages for infants and small children in whom EDX studies are particularly challenging. As discussed in Chapter 19, muscle is much darker on ultrasound in younger compared with older children. As an individual ages, the fascial planes between muscles become more obvious, and by age 5, muscle architecture on ultrasound is similar to that of an adult. Ultrasound has been most studied in children with muscular dystrophies. It should be no surprise that in many muscular dystrophies, abnormalities on muscle ultrasound worsen over time. Much of the work on ultrasound in muscular dystrophies has focused on whether the amount of increased echogenicity can be quantitated to use as a biomarker of disease. However, while pediatric neuromuscular ultrasound offers a similar advantage to that of adults in that it has the ability to easily screen many different muscle groups fairly quickly in one sitting, there has been very little work done with ultrasound as a diagnostic tool for pediatric muscle diseases. Theoretically, the yield of such screening could be great, as some inherited myopathies preferentially affect certain muscles while sparing others. In the case of nerve, ultrasound shares some fundamental characteristics with nerve conduction and needle EMG data, in that normal values are highly dependent on the age of the individual (Table 41.4). Compared with adults, there is very little normative data on nerves in pediatric ultrasound. Some studies have compared ultrasound in normal children with those with CMT type IA (CMT IA). As expected, nerves are much larger in children with CMT IA than in age matched controls (Fig. 41.5). Accordingly, ultrasound can be very useful in assessing for various hypertrophic neuropathies in children.

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$JH\HDUV Fig. 41.5  Scatterplot and line of best fit between nerve cross-­ sectional area (CSA) of the median nerve at the forearm and age in patients with CMT1A and controls.  Triangles represent individual data points for children with CMT1A and squares represent individual data points for controls. CMT1A, Charcot-­Marie-­Tooth disease type 1A. (From Yiu EM, Brockley CR, Lee KJ, et al. Peripheral nerve ultrasound in pediatric Charcot-­Marie-­Tooth disease type 1A. Neurology. 2015;10;84(6):569–574.)

In the case of mononeuropathy, the best way to overcome the lack of valid normative data is to compare side to side and use the patient as his or her own control. Of course, this is only applicable if the problem is limited to one side. In one particular set of pediatric neuromuscular disorders, ultrasound can be very useful. This occurs in the mucopolysaccharidoses (e.g., Hunter and Hurler syndrome, among others), as these patients are prone to carpal tunnel syndrome (Fig. 41.6). It is not infrequent that these children develop infiltration and enlargement of the median nerve at the wrist. It is much easier for such patients to undergo ultrasound screening for carpal tunnel syndrome than to undergo nerve conduction studies, especially if sedation is required.

736

SECTION IX    Electromyography in Special Clinical Settings

Suggested Readings

Fig. 41.6  Median neuropathy at the wrist in Hunter syndrome. A 40-­year-­old man with genetically confirmed Hunter syndrome on enzyme replacement therapy presented with bilateral hand numbness and tingling associated with marked atrophy of the thenar eminences and decreased sensation in the first three fingers and the lateral half of the fourth finger bilaterally. Top, Short axis view of the median nerve at the wrist (yellow arrow). The nerve is markedly enlarged (38 mm2) and hypoechoic with a loss of the normal fascicular pattern. Middle, Short axis view of the median nerve in the forearm (yellow arrow). The nerve is normal at 3 mm2. Accordingly, the wrist-­to-­ forearm ratio was severely elevated at 12.7 (NL < 3). Bottom, Long axis view of the median nerve at the wrist (red arrows). Again, note the enlarged and hypoechoic nerve with loss of the normal fascicular architecture. (Adapted from Alkhachroum AM, Preston DC. Ultrasound findings of carpal tunnel syndrome in a Hunter syndrome patient. Muscle Nerve. 2016;53(1):147–150.)

Alkhachroum AM, Preston DC. Ultrasound findings of carpal tunnel syndrome in a hunter syndrome patient. Muscle Nerve. Muscle Nerve. 2016;53(1):147–150. Cartwright MS, Mayans DR, Gillson NA, Griffin LP, Walker FO. Nerve cross-­sectional area in extremes of age. Muscle Nerve. 2013;47(6):890–893. Darras BT, Jones HR. Diagnosis of pediatric neuromuscular disorders in the era of DNA analysis. Pediatr Neurol. 2000;23:289–300. Gabreels-­Festen A. Dejerine–Sottas syndrome grown to maturity: overview of genetic and morphological heterogeneity and follow-­up of 25 patients. J Anat. 2002;200:341–356. Hellmann M, von Kleist-­Retzow JC, Haupt WF, et al. Diagnostic value of electromyography in children and adolescents. J Clin Neurophysiol. 2005;22(1):43–48. Jones HR, Bolton CF, Harper CM, et al. Pediatric Clinical Electromyography. Philadelphia: Lippincott Williams & Wilkins; 1996. Jones Jr HR, De Vivo DC, Darras BT, eds. Neuromuscular Disorders of Infancy, Childhood, and Adolescence: A Clinician’s Approach. Philadelphia: Butterworth Heinemann; 2003. Karakis I, Liew W, Darras BT, Jones HR, Kang PB. Referral and diagnostic trends in pediatric electromyography in the molecular era. Muscle Nerve. 2014;50(2):244–249. Parano E, Uncini A, DeVivo DC, et al. Electrophysiologic correlates of peripheral nervous system maturation in infancy and childhood. J Child Neurol. 1993;8:336–338. Rabie M, Jossiphov J, Nevo Y. Electromyography (EMG) accuracy compared to muscle biopsy in childhood. Child Neurol. 2007;22(7):803–808. Shklyar I, Geisbush TR, Mijialovic AS, et al. Quantitative muscle ultrasound in Duchenne muscular dystrophy: a comparison of techniques. Muscle Nerve. 2015;51(2):207– 213. Yiu EM, Brockley CR, Lee KJ, Carroll K, et al. Peripheral nerve ultrasound in pediatric Charcot-­Marie-­Tooth disease type 1A. Neurology. 2015;84(6):569–574.

SECTION X • Electronics and Instrumentation

Basics of Electricity and Electronics for Electrodiagnostic Studies

In the office, hospital, and home, we are surrounded by equipment, appliances, and many other devices powered by electricity. Although knowledge of electricity and electronics is not needed to watch television, talk on the telephone, or use a toaster, these examples are just the tip of the electrical and electronic iceberg in the world we live in as electromyographers. One might ask, is it really necessary to understand the basics of electricity and electronics to perform routine electrodiagnostic (EDX) studies? Although a degree in electrical engineering certainly is not needed, the answer clearly is yes. First, and most important, understanding the basics of electricity is essential to safely perform EDX studies and prevent potential electrical injuries to patients (see Chapter 43). Second, all of the responses recorded during nerve conduction studies and needle electromyography (EMG) are small electrical signals that are amplified, filtered, and then displayed electronically. Knowledge of electricity and electronics allows for a better understanding of what these potentials represent. Finally, and equally as important, knowledge of electricity and electronics is critical to understand and correct the variety of technical problems that frequently arise during EDX studies (see Chapter 8).

BASICS OF ELECTRICITY All atoms have a nucleus composed of positively (+) charged particles, protons, and particles with no charge, neutrons. Orbiting around the nucleus are negatively (−) charged particles, electrons. Most atoms have the same number of protons and electrons; the electrons remain bound in their orbit by their magnetic attraction to the protons (i.e., in magnetism, opposites attract).

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Electricity is formed when electrons are removed from their orbit and flow to adjacent atoms. Materials that allow electrons to move freely are known as conductors. In contrast, materials that inhibit the flow of electrons are known as insulators. Conductors typically are metals, most often copper. Insulators most often are rubber, plastic, or ceramic. To understand basic electrical circuits, one needs first to be acquainted with several important terms:    • Coulomb is the standard unit of electric charge, approximately equal to 6.24 × 1018 electrons. • Current, represented by the symbol I, is the actual flow of electrons. The ampere is a measure of current, designated by the letter A. An ampere is defined as 1 coulomb passing a point in a conductor in 1 second. Current can only flow when a complete circuit exists. • Voltage is the electromotive force required to make electricity flow through a conductor. This electromotive force results from a fundamental property of magnetism that oppositely charged particles attract each other. Any source with an excess of electrons (negatively charged particle) will be drawn to a source with a lack of electrons (positively charged particle). Voltage is designated by the symbol E. Its unit of measurement is volts, which is designated by the letter V.

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SECTION X   Electronics and Instrumentation

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• Resistance opposes the flow of electrons. Resistance is designated by the symbol R. The unit of measurement for resistance is Ohms, which is designated by the Greek letter Ω. All materials, even conductors, impede the flow of electrical current to some extent. In general, resistance increases with the length of the conductor and decreases as the cross-­section of the conductor increases.

Analogy Between Electricity and Water Because current and electrons cannot be seen, it may be difficult to relate to electricity and its basic definitions. One useful way of understanding electricity and its properties is to make an analogy to the flow of water. The analogy to water and plumbing often is easier to grasp and can be extrapolated to the understanding of electricity. :DWHU SUHVVXUH

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Water can be measured as a specific volume (e.g., a liter or gallon). Thus a gallon of water is analogous to a coulomb of electricity, an amount of charge. For water to flow, it must have some force that is driving or pushing it. This force can be gravity, in the case of water stored in a water tower, or a pump that mechanically propels the water. In either case, water is put under pressure. Pressure is measured as force per unit area, typically as pounds per square inch (psi). Thus, water pressure is analogous to voltage, the driving electromotive force. Water will flow if there is a pressure difference between two points (i.e., from an area of high pressure to low pressure). Likewise, electrons will flow if there is a difference in voltage between two points. Flow is the actual movement of water, which is measured as volume passing by a point in a specific time period (e.g., gallons per second). Thus flow of water is analogous to current, the movement of electrons, which is measured in amperes (1 coulomb passing a point in a conductor in 1 second). Lastly, resistance to water flow is determined by the physical characteristics of the pipes it is traveling through. Longer and especially narrow-­ diameter pipes impede the flow of water. Thus the mechanical resistance of a water pipe is analogous to the electrical resistance of a circuit.

The flow of water is determined by Poiseuille’s law: Flow =

Change in water pressure between two points Water resistance

At point D in the previous figure, the water pressure is essentially zero. Water is taken up by the pump and pressurized, resulting in a high pressure at point A. Water will now flow because it is under high pressure at point A and low pressure at point D. The water pressure at point B will still be high because the diameter of the pipe is so large that it offers little resistance to flow. However, the marked narrowing of the pipe between points B and C increases the resistance to flow. The higher the resistance, the less the flow. Conversely, the higher the water pressure difference, the more the flow. At point C, the water pressure is now very low. However, it must still be slightly higher than point D so that water will flow from point C to D. If extra water were to somehow get into the system and be a greater amount than the water pump could pump, it could easily be diverted to the reservoir (analogous to the ground, see later). 

Ohm’s Law The most important basic principle of electricity is Ohm’s law, which defines the relationship among current, voltage, and resistance in a circuit. Ohm’s law is directly analogous to Poiseuille’s law for water. For electrical circuits, Ohm’s law states that: Current =

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The figure above depicts a simple circuit consisting of a battery (E) (an electromotive source of electrons) connected to one resistor (R). The amount of current (I) flow is determined by Ohm’s law, I = E/R, where E is the voltage from the battery and R is the resistance. Also note the presence of the ground connection. The ground is ideally a true electrical zero. Most often, true grounds are physically connected to the earth (e.g., through a pipe).

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as shown, the value of E, I, or R can readily be determined by blocking the variable of interest (shaded in the figure) and looking at the relationship between the other two parameters. 



Kirchhoff’s Laws



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One of the confusing aspects of electricity is figuring out the direction that current actually flows. In the conventional flow notation, electric charges move from the positive (surplus) side of the battery to the negative (deficiency) side. However, as electricity comes about by the flow of electrons, which are negatively charged, the actual flow of electrons occurs from the negative to the positive. In the electron flow notation, electric charges move from the surplus of negative charges at the negative side of the battery to the positive side of the battery, which has a deficiency of negative electrical charges. Both notations are correct when used consistently. The conventional flow notation is used by most electrical engineers and found in most electrical engineering textbooks and will be used in this chapter.

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Kirchhoff ’s current law states that the algebraic sum of all the currents meeting at any point in a circuit must be zero. Put another way, the sum of incoming currents must equal the sum of outgoing currents. This law represents the conservation of charge. The number of electric charges that flow toward a point must equal the number of electric charges that flow away from that point.

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Kirchhoff ’s voltage law states that, in a closed circuit, the algebraic sum of all the voltage (i.e., potential) drops is equal to the electromotive source voltage of the circuit. The previous figure shows a battery with a voltage (VA) connected in series to three resistors (B, C, D). The current running through the three resistors results in a voltage drop across each resistor, VB, VC, and VD, respectively. Kirchhoff ’s voltage law requires that the sum of the voltage drops across all three resistors equals the voltage of the battery (i.e., VB + VC + VD = VA). 

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First, take the example of a simple circuit with a battery (E) connected to three resistors in series. From Kirchhoff ’s current law, the current (I) must be the same going through each resistor (i.e., current flowing into any point equals the current flowing out of that point). From Ohm’s law, a voltage drop will be present across each resistor (E = I × R). Thus, the voltage drops for the three resistors must be I × R1, I × R2, and I × R3, respectively. From Kirchhoff ’s voltage law, the voltage from the battery (E) must equal the sum of all the voltage drops across the three resistors (VB + VC + VD). With this information, applying simple algebra: E = V B + VC + VD

Kirchhoff's voltage law

E = I × R1 + I × R2 + I × R3

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Thus resistors in a series can be directly added together to calculate a net resistance. Take an example of the same circuit of a battery connected to a series of three resistors, using real values.

In the example above, the battery has a voltage of 100 V. The resistors have a resistance of 12, 10, and 3 Ω, respectively. Thus the total resistance of the circuit is the sum of the resistors (12 + 10 + 3) = 25 Ω. With this information, the current can be easily calculated from Ohm’s law: I=

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Knowing the current, the individual voltage drop across each resistor (48 V, 40 V, 12 V) can be calculated from Ohm’s law (E = I × R).  Resistors in Parallel When resistors in a circuit are placed in parallel, a net resistance can also be calculated using Ohm’s and Kirchhoff ’s laws. Ι

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Take the example of a simple circuit with a battery (E) connected to three resistors in parallel. From Kirchhoff ’s current law, the total current (I) must be the sum of the individual currents going through each resistor: I = I1 + I2 + I3

Chapter 42 • Basics of Electricity and Electronics for Electrodiagnostic Studies 741

From Ohm’ law, the voltage across each resistor can be calculated: V1 = I1 × R1 V2 = I2 × R2 V3 = I3 × R3

From Kirchhoff ’s voltage law, the voltage from the battery must equal the voltage drops along any closed circuit. Thus, the same voltage (E) from the battery must be present across each of the three resistors:

Direct Current and Alternating Current Direct current (DC) is current that always flows in the same direction. In DC, electrons flow uniformly from the power source through a conductor to a load (i.e., an electrical device) and back to the power source. The most common example of a DC power source is the battery. However, current also can be supplied as an alternating current (AC). In an AC, electrons follow the path of a sine wave, flowing first in one direction and then reversing. The current reverses polarity many times a second (measured as cycles per second [cps] or Hertz [Hz]). The most common example of AC is the conventional 60 Hz electricity in wall sockets in houses and offices. 

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Thus resistors in parallel reduce the total resistance, as opposed to resistors in series, which increase the total resistance. For instance, three resistors in series, each 100 Ω, result in a total resistance of 300 Ω. However, three resistors in parallel, each 100 Ω, result in a net resistance of 33 Ω. The analogy to water is as follows. Imagine a bucket full of water. The weight of the water creates a water pressure against the bottom of the bucket. If a hole is drilled through the bottom of the bucket, water will start to flow, based on how large the hole is (i.e., the resistance) and the water pressure in the bucket. If another hole is drilled nearby (i.e., in parallel), there are now two ways for water to escape (under the same pressure), and hence, the amount of water leaving the bucket (i.e., the current) will increase. Thus the two holes in parallel effectively decrease the resistance to water leaving the bucket. 



Because DC and voltage are constant, their measurements are straightforward. However, AC measurement is more complicated, because voltage and current are constantly changing values. There are several ways to measure AC, including measuring baseline to peak or peak to peak. A mean would not be useful, because the mean of an AC current is actually zero. However, the most common method of measuring AC is the root mean square (RMS) value. The RMS is calculated by dividing the waveform into many small increments. The value of each increment is squared and a mean of all the squares determined. Finally, the square root of the mean results in the RMS value. The RMS value is the most useful way of measuring AC because power in a circuit is defined as voltage multiplied by current: Power (watts) = E × I = E × E substituting E/R for I per Ohm's law R 2 =E R

Thus, power is proportional to the square of the voltage. Accordingly, for the same resistance, 1 volt RMS of AC delivers the same power as 1 volt DC. For the typical house or office AC, the RMS voltage is approximately 0.707 multiplied by the voltage measured between baseline and the maximum value. Thus, in the United States, 120 V RMS corresponds to approximately 170 V baseline to peak.

742

SECTION X   Electronics and Instrumentation

One natural question to ask is: why alternating current? Current constantly flowing back and forth in opposite directions many times a second seems confusing and counterintuitive. However, AC arises from all the common ways that electricity is generated. Whether the source is a windmill, hydroelectric, nuclear, coal, or natural gas, all ultimately result in a rotational mechanical movement (e.g., wind and hydro directly turning an axis; nuclear, coal, and natural gas heating water to steam which then turns a turbine). Electricity is then created by attaching a coil (a conductor shaped as a loop) to the mechanical rotation with the coil placed in a strong magnetic field. As the conductor rotates in the magnetic field, electricity is generated and flows to an attached load. The angle and direction of the coil in the magnetic field determine the amount and direction of the electricity. When the coil is perpendicular to the magnetic field and moving with the positive side of the coil up, the maximal current is generated (i.e., the top of the sine wave). However, when the coil is perpendicular to the magnetic field and moving with the negative side of the coil up, the maximal current is generated in the other direction (i.e., the bottom of the sine wave). When the coil is parallel to the magnetic field, no current is generated (the zero crossings of the sine wave). It is this rotation of a coil within a magnetic field that creates an AC with its characteristic sinusoidal waveform. 0DJQHWLFILHOG

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the following, capacitance and inductance share many fundamental properties but also have significant and important differences.

Capacitance Capacitance, represented by the symbol C, is a property of a circuit that allows it to store an electrical charge. The farad is a measure of capacitance, designated by the letter F. A capacitor is an electronic component made from a pair of conductive plates separated by a thin layer of insulating material (the insulating material is known as a dielectric). When a voltage is applied across the plates of a capacitor, electrons are forced onto one plate and pulled away from the other. The plate with an excess of electrons is negatively charged, whereas the opposite plate with a deficiency of electrons is positively charged. The amount of charge stored in a capacitor is proportional to the voltage across it as described by: Q=C×V

where Q is the charge in coulombs, C is capacitance in Farads, and V is voltage in volts. Because of the dielectric material between the plates, no actual current (i.e., flow of electrons) moves across the plate; however, there is an “apparent flow,” also known as a capacitive current.

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Beyond simple resistive circuits, one needs to move next to the basics of capacitance, inductance, and reactance. Although these concepts are more complicated, they have direct relevance to EDX studies regarding (1) low-­and high-­frequency filters and (2) stray leakage currents that potentially pose a risk of electrical injury to patients undergoing EDX studies (see Chapter 43). Although capacitance and inductance are present in DC circuits, they are more germane to AC circuits. The concept of reactance is only applicable to AC circuits. As noted in

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Chapter 42 • Basics of Electricity and Electronics for Electrodiagnostic Studies 743

current in the conductor. When the electrons arrive at the negative plate, they do not actually cross the plate.

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At that time, no further apparent current will flow. The capacitor will be fully charged, and an electric field will exist between the two plates. The rate of accumulation of charge (and the resulting voltage) at a capacitor occurs exponentially, based on the equation: Voltage = 1 − e − t / RC

where t is time e (natural logarithm base) is 2.718281828459045235 R is resistance of the circuit in Ohms C is capacitance in Farads Note that, in the above equation, the time required for voltage to rise to its maximum value in a circuit is dependent on the product of resistance (R) multiplied by capacitance (C). This product (RC) is known as the time constant of a capacitive circuit. When t = RC Voltage at the capacitor = 1 − e −1 = 0. 632 = 63. 2 %

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Thus, one time constant (RC) defines the time it takes for the voltage across a capacitor to reach 63.2% of its maximum value. During the second time constant, voltage will rise to 63.2% of the remaining 36.8%, or a total of 86.4%. It takes about five time constants for voltage across the capacitor to reach its maximum value. Once fully charged, what happens if the power source is then turned off? The opposite occurs. The capacitor will discharge, with the excess electrons now flowing away (i.e., in the opposite direction than during charging) from the negative plate of the capacitor. Again, an apparent capacitive current will occur on the other side of the circuit and continues until the capacitor is fully discharged. The discharge of a capacitor follows a similar exponential fall, described by the equation: ( ) Voltage at the capacitor = e − t / RC 

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Thus, after one time constant, the voltage across the capacitor will have dropped to 36.8% of its original value. Again, it takes approximately five time constants for a capacitor to completely discharge. In a DC circuit, when the circuit initially is turned on, current flows. However, after five time constants, the capacitor is fully charged and no further current occurs. At this point, the capacitor effectively acts as an open circuit. Understanding these properties of a capacitor in a simple DC circuit allows one to extrapolate to what occurs in an AC circuit. Take the example of an AC circuit where the frequency of the current is much faster than the frequency 1/RC. When current is first applied to a capacitive circuit, it flows readily because of the apparent or capacitive current. If the AC then reverses before the capacitor is fully charged, a capacitive or apparent current will flow in the opposite direction. Thus in essence, a capacitor is effectively a short circuit for high frequencies. Conversely, if the frequency of

744

SECTION X   Electronics and Instrumentation

the current is much slower than the frequency 1/RC, the capacitor can fully charge before the current reverses. Thus a capacitor can act like an open circuit for low frequencies. These properties can be used to an advantage in designing low and high filters (see the following sections). In an AC circuit, also note that a capacitor constantly charges and discharges. When charge accumulates between the two plates of the capacitor, an electric field develops between the plates. Thus, in an AC circuit, there is a constantly expanding and collapsing electrical field around a capacitor. Other conductors near this changing electrical field may develop capacitive currents. This is of importance in understanding the concept of stray capacitance and the risks of leakage currents (see the following sections). 

Inductance

Similar to the calculation for capacitance, the resulting current in a circuit with an inductor occurs exponentially and is described by the following equation: Current = 1 − e

− t/L R

where t is time e (natural logarithm base) is 2.718281828459045235 L is inductance in Henries R is resistance of the circuit in Ohms Note that, in the above equation, the time required for current to rise to its maximum value in a circuit is dependent on the value of inductance divided by resistance. This value (L/R) is known as the time constant of an inductive circuit. When t = L / R

The property of an electrical circuit that causes it to oppose any change in current is known as inductance. Inductance is designated by the symbol L and is measured in henries (H). Inductance is somewhat similar to mechanical inertia, which must be overcome to get a mechanical object moving or stopping. Whereas resistance opposes all current flow, inductance only opposes a change in current. If current increases, inductance tries to hold it down; conversely, if current decreases, inductance tries to hold it up.







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Inductance occurs as a result of magnetic fields induced by a current. Whenever current flows, a magnetic field develops around the conductor, known as an electromagnetic field. Moving a conductor through a magnetic field will induce a voltage in a conductor. Likewise, having a stationary conductor in a magnetic field that is either expanding or collapsing will also induce a voltage in the conductor. Thus, when current first begins to flow in a conductor, an expanding magnetic field develops. This expanding (i.e., changing) magnetic field induces a voltage in the conductor that opposes the flow of current, known as a counter electromotive force. This counter electromotive force results in a time delay for current to reach a steady value. Once a steady value is reached, the magnetic field around a conductor is static, and no further opposing voltage develops.

Current = 1 − e −1 = 0. 632 = 63. 2 %

Thus, one time constant (L/R) defines the time it takes for the current to reach 63.2% of its maximum value. During the second time constant, current will rise to 63.2% of the remaining 36.8%, or a total of 86.4%. It takes about five time constants for current to reach its maximum value. At steady state, what happens if the power source is then turned off? The opposite occurs. The electromagnetic field collapses and induces a counter electromotive force in the conductor, opposing the flow of current. The current flow follows a similar exponential fall, described by the equation: Current = e

− t/L R

Thus, after one time constant, the current will have dropped to 36.8% of its original value. Again, it takes approximately five time constants for current to completely dissipate. Once the current has reached a steady state (in this case zero), there will be no changing magnetic field, and no further opposing voltage will be induced. In a DC circuit, when the circuit is turned on, current flows but is initially impeded by inductance. However, after five time constants, the current reaches steady state and no further inductive voltage occurs. At this point, an inductor effectively acts as a short circuit. From understanding these properties of inductance in a simple DC circuit, one can extrapolate what happens in an AC circuit. Take an AC circuit where the frequency of the current is much slower than the frequency 1/(L/R). When current is first applied to the circuit, it is impeded due to inductance. However, after five time constants, the current has reached steady state and no further inductance occurs. Thus, for low frequencies, inductors allow current to flow and reach their maximum. However, in AC circuits with frequencies higher than 1/(L/R), the AC reverses before the current can reach its steady state. In this case, the inductor effectively attenuates high-­frequency currents from flowing.

Chapter 42 • Basics of Electricity and Electronics for Electrodiagnostic Studies 745

Thus, as a capacitor stores energy as charge in an electrical field, an inductor stores energy in the form of a magnetic field. Just like capacitance, inductance is dependent on the frequency. If the frequency is low, the current has more time to reach its maximal value, before the polarity of the sine wave reverses. Conversely, if the frequency is very high, the current has less time to reach its maximal value. Thus, inductance attenuates high frequencies much more than low frequencies; this is exactly the opposite of capacitance. Taken to the limit, an inductor is essentially a short circuit at low frequencies and an open circuit at high frequencies. In an AC circuit, current will be constantly flowing and then reversing, resulting in an expanding and collapsing magnetic field around any conductor. This can induce voltages in other conductors near this changing magnetic field, which is important to understanding the concept of stray inductance and the risks of leakage currents (see following sections). 

Reactance and Impedance In a purely resistive circuit, either DC or AC, opposition to current flow is termed resistance. However, in an AC circuit, current can also be opposed by inductance, capacitance, or both. Opposition to current flow from capacitance is the capacitive reactance, termed XC. The larger the capacitor, the smaller the capacitive reactance. Opposition to current flow from inductance is the inductive reactance, termed XL. The larger the inductor, the larger the inductive reactance. Similar to resistance, reactance is measured in Ohms (Ω). Thus, total reactance in an AC circuit depends on both inductive and capacitive reactances. Clearly, from the earlier discussion, inductive and capacitive reactances depend on frequency. In the case of inductance, reactance is much higher for high frequencies. Conversely, in the case of capacitance, reactance is much lower for high frequencies. Capacitive and inductive reactance can be calculated by the following equations: XC =

• I mpedance = Resistance, in circuits with no inductance or capacitance • Impedance = Resistance, in circuits where inductive reactance equals capacitive reactance • Inductive and capacitive reactances directly oppose each other. 

WAVEFORMS, FREQUENCY ANALYSIS, AND FILTERING

During nerve conduction studies and needle EMG, every displayed waveform represents a small bioelectrical potential (i.e., voltage) that is recorded, amplified, and then filtered. The last process, filtering, improves the quality of the recorded potential by preventing a wandering baseline and eliminating much unwanted electrical noise. To understand the process of filtering, one must first appreciate the frequency spectrum of any recorded waveform. The Fourier analysis is a mathematical construct that states that any waveform can be derived by adding a series of sine waves. The sine waves may vary by amplitude, frequency, or phase. One of the most illustrative examples is that of a square wave, which also can be constructed by adding a series of sine waves.

Take the above example of a square wave with a frequency of 3 Hz.

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where f is frequency, and L is inductance. Lastly, impedance, designated by the letter Z, is also measured in Ohms (Ω). Impedance incorporates the total opposition to current flow in an AC circuit, including resistance, capacitive reactance, and inductive reactance. Impedance is calculated using the following equation: Impedance ( Z) =

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Thus, from the above equation, one can appreciate several facts about impedance:   

If a smaller-­amplitude 9-­Hz sine wave is added to the 3-­Hz sine wave, the above waveform results. This is now starting to look somewhat like a square wave.

SECTION X   Electronics and Instrumentation

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If now an even smaller-­amplitude 15-­Hz sine wave is added to the two earlier sine waves, the resultant waveform above is generated. If one continues this analysis, the actual Fourier analysis for a square wave with a frequency (x) can be derived from the following equation: = sin(X) + 1/3sin(3X) + 1/5sin(5X) + 1/7sin(7X) + 1/9sin(9X) + 1/11sin(11X) + ...

The above waveform represents the Fourier reconstruction of 10 separate sine waves. Thus, as more waveforms with higher frequencies and smaller amplitudes are added, the reconstructed waveform continues to more closely approximate that of a true square wave. Thus, a 3-­Hz square wave contains the following frequencies: 3, 9, 15, 21, and 27 Hz, in addition to other higher frequencies.

A similar analysis can be performed for all waveforms recorded during routine EDX studies. The figure above shows the relative frequency components of a compound muscle action potential (CMAP) compared with that of a sensory nerve action potential (SNAP) (from Gitter and Stolov, 1995). Note that the SNAP has higher-­frequency components compared with the CMAP. Ideally, one would like an EMG machine to display the amplified bioelectric signal of interest exactly. However, if a signal is contaminated with electrical noise, it can be difficult to properly record and interpret it. In general, very low frequencies will contaminate the signal of interest by causing the baseline to wander and very high frequencies can easily obscure many small waveforms (e.g., SNAPs, fibrillation potentials). Thus it is desirable to filter out unwanted low and high frequencies while retaining the frequency spectrum of the actual waveform as much as possible. 

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followed by a resistor. In the above illustration and those that follow, the signal source will be modeled to generate either a low-­frequency, high-­frequency, or square wave input to the circuit. The input to the circuit is measured from point A (to a reference or ground), and the output of the circuit is measured from point B (to a reference or ground).

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Putting low-­and high-­frequency filters in tandem allows for a passband, whereby frequencies above and below the cutoff values are filtered out. However, no passband removes frequencies above or below a cutoff value with perfect precision. There is a normal roll-­off of the frequencies that pass through. In general, cutoff frequency values for both high and low filters are defined as the point where the power of the signal is reduced by 50% [i.e., approximately 0.707 of its voltage. Remember that power is proportional to the square of the voltage and that (0.707)2 = 0.50]. 

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Congratulations. You have almost reached the end of this chapter, but you still may be asking whether basic knowledge of electricity and electronics really is needed to perform EDX studies. The answer clearly is yes, because there are many practical implications for performing EDX studies based on the principles learned in this chapter. Most important among them are the following:    • Filters. Understanding that all waveforms, including those recorded during EDX studies, have their own unique frequency spectrum allows for the use of electronic filters to remove unwanted low-­and high-­ frequency noise while permitting the principal frequencies of the waveform to pass unaffected (i.e., passband). Although filters remove unwanted electrical noise, they also impact the waveform of interest and can alter certain characteristics of the waveform (especially amplitude for high-­frequency filters and duration for low-­frequency filters). • Tissue acting as a filter: nerve conduction studies. Skin and subcutaneous tissue act as a high-­frequency filter. Accordingly, if surface electrodes are not optimally placed directly over a nerve or muscle, much of the waveform’s higher frequencies will be filtered out. Amplitude is predominantly a high-­frequency response. SNAPs contain more high frequencies than CMAPs do. Thus, if the surface electrodes are not optimally placed, amplitudes on nerve conduction studies will be reduced, more so for SNAPs than for CMAPs. If a patient has limb edema, then even if the surface electrodes are optimally placed, the increased tissue and edema between the nerve or muscle and the recording electrode will result in an artificially low amplitude. • Tissue acting as a filter: needle EMG. During the needle EMG examination, tissue between the motor unit action potentials and the needle electrode also acts as a high-­frequency filter. Again, as amplitude is predominantly a high-­frequency response, MUAP amplitude can be markedly influenced by the distance between the needle and the motor unit. During needle EMG, the proper location to analyze an MUAP is reached when the major spike (i.e., the highest frequency component of the MUAP) is very short, less than 500 μs. This ensures that the needle is very

Chapter 42 • Basics of Electricity and Electronics for Electrodiagnostic Studies 749

close to the motor unit. Likewise, this property of tissue acting as a filter also explains why duration is a much better determinate of motor unit size than is amplitude. Duration is predominantly a low-­frequency function. Thus, tissue, which acts as a high-­frequency (low-­pass) filter, allows the low-­frequency components from distant muscle fibers of the same motor unit to be recorded. • Inductive electrical noise from the environment. How does a nearby radio or coffee maker result in electrical interference during EDX studies? Every power cord contains a 60-­Hz AC signal. Around that power cord is a continuously expanding and collapsing magnetic field. If a conductor (e.g., a recording electrode) is near that magnetic field, an inductive voltage can be generated on that lead, which then can be amplified, often saturating the amplifier and obscuring the signal of interest.   

• Importance of eliminating electrode impedance mismatch. Despite one’s best efforts, there will always be some electrical noise in every EMG laboratory, usually 60 Hz AC from nearby electrical equipment. However, if the impedances (which include resistance, capacitive reactance, and inductive reactance) of the active and reference electrodes are identical, then any current resulting from electrical noise contaminating the recording electrodes will create the same extraneous voltage on each lead (from Ohm’s law: Voltage = CurrentNoise × Impedance). Because all signals are amplified by way of a differential amplifier, the extraneous voltage will be canceled out. Several important techniques help ensure that the recording electrodes have the same impedance, among them, the use of a coaxial cable, good skin preparation, and an ample amount of conductive paste between each electrode and the skin. • Importance of the ground electrode. One might assume at first glance that there is no difference between the reference and the ground lead, both being at electrical zero. However, all voltages are relative potentials, determined by the difference between two points in a circuit. Thus, one can measure a potential of 10 V between a point on a circuit that is 10 V higher than the ground (which is at electrical zero). However, 10 V also can be measured in a circuit between a point that is 20 V above ground and another point that is 10 V above ground. Thus, in most electronic applications, there is usually a potential difference (i.e., a voltage) between the neutral or reference electrode, and the ground electrode.    $FWLYH Ι

The photo above is a real example of this problem from one of our laboratories. Note the ophthalmoscope hanging on the wall adjacent to the EMG table and the power cord next to it. Even in the off position, AC is present in the power cord, resulting in an unseen expanding and collapsing magnetic field. When recording electrodes were placed near the magnetic field, an induced current was generated in the leads. Sensory responses could not be recorded without excessive electrical noise unless the power cord plug was physically pulled out of the socket.    • The stimulator cable and the recording electrodes should not cross or be near each other. When the stimulator is discharged, a brief current flows through the stimulator, creating an expanding and then collapsing magnetic field around the stimulator cable. If the recording electrodes or their leads are near that field (especially if the cables are crossed and touching), an inductive voltage can easily be generated in the recording leads, resulting in a large stimulus artifact.

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SECTION X   Electronics and Instrumentation

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electrode disconnected. Note that with the ground electrode disconnected, there is a large superimposed 60-­H z electrical signal, making the sensory response barely visible.    • Leakage currents: stray capacitance and inductance. Although EMG machines are designed to minimize leakage currents, there will always be some leakage current on the machine chassis from stray capacitance and inductance. This is because any circuitry with ACs containing capacitors will have expanding and collapsing electrical fields. Likewise, any circuitry with ACs will have expanding and collapsing magnetic fields. If any part of the machine chassis is metal (i.e., a conductor) and near enough to electrical or magnetic fields from internal circuitry, stray capacitive or inductive currents potentially can be produced. These small leakage currents pose a potential electrical risk to certain vulnerable patient groups (see Chapter 43). With preventative maintenance of the machinery and by closely following specific protocols, these possible hazards can be eliminated (see Chapter 43).

SECTION X • Electronics and Instrumentation

Electrical Safety and Iatrogenic Complications of Electrodiagnostic Studies Electrodiagnostic (EDX) studies are generally well tolerated and rarely associated with any significant side effects. Most nerve conduction studies (NCSs) use surface stimulating and recording electrodes, which are not invasive. However, electrical current is applied to the patient when stimulating peripheral nerves. In patients with pacemakers, cardioverter-­ defibrillators, and other similar cardiac devices, this current may pose a risk under certain situations. In contrast, needle EMG is an invasive test and, rarely, may be associated with iatrogenic complications, most important of which are pneumothorax, bleeding, infection, and local injury. Use of neuromuscular ultrasound to guide needle EMG placement in muscles that are at high risk for pneumothorax when sampled is discussed in detail in Chapter 40. In addition, the patient is connected to the electromyography (EMG) machine via the recording electrodes during the NCSs and needle EMG study. Thus, during both portions of the examination, the patient is at risk from stray leakage currents. This risk is much higher in the so-­called electrically sensitive patient, a situation often encountered in the intensive care unit (see later).

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ELECTRICAL ISSUES All electrical devices, including EMG machines, require current to operate. Current is delivered from an electrical cord plugged into a wall receptacle (Fig. 43.1). A typical electrical receptacle in the United States contains three inputs: a black “hot” lead that carries 120 volts (V) of 60-­Hz alternating current, a white “neutral” lead near 0 V, and a green ground lead that is used to dissipate leakage currents. When a circuit is created, current flows from the hot lead to the EMG machine and then returns via the neutral lead, based on the amount of resistance between the two leads as determined by Ohm’s law (see Chapter 42). Every wire, including power cords, has some small resistance; thus, a small voltage develops on the neutral lead, which equals the current flowing multiplied by the resistance in the power cord (Fig. 43.2). The voltage increases with the length of the power cord and increases further if extension cords are added to the power cord. In addition, small voltage leaks are often present on the machine chassis, caused by stray capacitance and inductance from internal electronics (Fig. 43.3). Thus, leakage currents can be transmitted onto the patient either from stray voltages on the machine chassis or on the neutral (reference) lead. As the ground electrode is close to true electrical neutral, the ground lead allows a pathway for stray current leaks to dissipate.

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Fig. 43.2  Stray leakage current: reference lead.  Because every wire, including power cords, has some small resistance (R N), a small voltage (V N) develops on the neutral or reference lead as determined by Ohm’s law (V = I × R, where I is the current). The voltage increases with the length of the power cord and increases further if extension cords are added to the power cord. Thus the voltage on the reference electrode is not zero and is a potential source for a leakage current transmitted to a patient. (Adapted with permission from Kimura J. Electrodiagnosis in Diseases of Muscle and Nerve. Philadelphia: FA Davis; 1983:615–619.)

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The risk of electrical injury depends on the amount of leakage current and whether the circuit passes through the heart. A very small current (e.g., 200 microamperes [μA]) applied directly to the heart can result in ventricular fibrillation and death. However, the normal, healthy individual typically is well protected by two important mechanisms. First, dry and intact skin provides a high resistance. Second, the large volume of soft tissue that surrounds the heart dilutes any current applied to the body (e.g., a current applied from arm to arm degrades to 1/1000 of the original signal when it reaches the heart, due to the dissipation from surrounding tissues). The risk of electrical injury from leakage current increases in the following situations:    • Malfunctioning of the electrical equipment • Multiple electrical devices attached to the patient • Loss of the body’s normal protective mechanisms    The latter two (multiple electrical devices attached to the patient and loss of the body’s normal protective mechanisms) result in the “electrically sensitive” patient, a common situation in the intensive care unit. To prevent the possibility of an electrical injury during EDX studies, it is essential for equipment to be regularly maintained, to always use a ground electrode, and to follow simple guidelines when using electrical devices attached to the patient (Box 43.1). A wooden examining table is preferable to a metal table, as it does not conduct electricity (Fig. 43.4). Machines should be turned on before attaching electrodes to the patient and turned off after disconnecting the patient, to minimize the risk of power surges. Equipment should be periodically inspected by a biomedical engineer to measure leakage current and verify proper grounding. In general, the maximum amount of acceptable leakage current is 100 μA or less, measured from chassis to ground, and 50 μA or less from any input lead to ground. Extension cords should be avoided to reduce the risk of voltages developing on the reference electrodes. Ground electrodes should always be used to avoid current flows from reaching the patient. The ground needs to be placed on the same limb as the active electrodes so that leakage currents cannot flow in a path through the heart (Fig. 43.5A).

Fig. 43.4  Wooden bed and electrodiagnostic studies.  Wood does not conduct electricity; therefore, wooden examining tables are preferable to metal tables to ensure safety during electrodiagnostic studies.

Box 43.1  Measures to Ensure Proper Grounding • Always use a three-­hole power receptacle with a properly grounded outlet. • Unnecessary electrical equipment should be kept outside the EMG examining room. • Suspect improper grounding if: Equipment is wet or has been subjected to spillage of liquids Equipment has been physically damaged or has loose parts Equipment gives a tingling sensation when touched Equipment becomes hot or gives off an unusual odor or sound There is damaged or cracked insulation in the power cable • Use a wooden examining table if possible (metal conducts electricity) (Fig. 43.4). • Avoid patient contact with any metal objects or any part of the EMG machine. EMG, Electromyography. With permission from Al-­Shekhlee A, Shapiro BE, Preston DC. Iatrogenic complications and risks of nerve conduction studies and needle electromyography. Muscle Nerve. 2003;27:517–526.

The issue of an intact ground electrode and proper ground placement is most important when a patient is connected to other electrical devices. If the ground from the EMG machine is not functioning (i.e., ground fault), stray current from the EMG machine could flow to a ground electrode from a different electrical device. If the pathway included the heart and the amount of current was large enough, a cardiac arrhythmia could theoretically occur (Fig. 43.5B). However, most modern medical devices, including EMG machines, are designed with electrical isolation. With electrical isolation, the current generated by the stimulator and potentials recorded by the electrodes are physically separated from the main EMG device, which is connected to a wall current and an earth ground. This limits the possibility that leakage current from the main machine can travel to the patient and return via some other earth ground attached to the patient. Electrical isolation is accomplished optically: the

Chapter 43 • Electrical Safety and Iatrogenic Complications of Electrodiagnostic Studies 753

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electric signals from the amplifier are converted to light by a light-­emitting diode (LED). The brightness of the LED is proportional to the electric signal. A photodetector in the main device then picks up the light and converts it into an electric signal, which is then processed in the EMG machine. In this way, the electrical circuit in contact with the patient is physically separated from the electricity in the EMG machine. If leakage current from the EMG machine does reach a patient, the recording electrodes, including the ground electrode from the preamplifier, offer no physical path for the that current to flow through a patient to return to an earth ground.

Risk of Electrical Injury Central Lines and Electrical Wires One of the more common ways a patient can become electrically sensitive is when the normal protective function of

the skin is breached by intravenous lines and wires. This danger increases if the lines are actually in contact with or in close proximity to the heart, as occurs in central intravenous catheters (Fig. 43.6). Most dangerous is the presence of an external wire near or in the heart, such as occurs with placement of a temporary external pacemaker or during the use of a guidewire while placing or changing a central line. Skin resistance typically is several million Ohms (MΩ). A central catheter traversing the skin reduces this resistance to 300,000 Ohms. Any fluid spill where a catheter enters the body decreases the resistance even further. If a catheter has an internal guidewire, the resistance drops to 70 Ohms (Ω). An external pacemaker wire essentially has no resistance. In situations where the resistance is so low, small leakage voltages may result in small leakage currents, known as microcurrents. Whereas microcurrents are completely harmless in a patient with intact skin, they are potentially

SECTION X   Electronics and Instrumentation

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Fig. 43.6  Risk of electrical injury from central lines: stimulation sites to avoid.  One of the more common ways that a patient can become electrically sensitive is when the normal protective function of the skin is breached by intravenous lines and wires that are in contact with or in close proximity to the heart, as occurs in central intravenous catheters. Nerve conduction studies can be performed safely in these patients, provided certain precautions are taken, as noted in the text. Proximal stimulation sites should be avoided, most importantly at the axilla and Erb’s point.

very dangerous in an electrically sensitive patient (i.e., a patient with a central line, external pacemaker wires, etc.). Thus EDX studies should never be performed on patients with external wires in place (i.e., external pacing wire, guidewires, etc.) because the conductive pathway to the heart is so vulnerable. However, studies can be performed on patients with central lines provided certain precautions are followed. Equipment must be maintained. Ground electrodes must always be used. If an upper extremity must be studied, in general, it is preferable and safer to study the upper extremity contralateral to the side with the central line. If that is not possible, one should refrain from proximal stimulation sites (i.e., axilla, Erb’s point, and root). Likewise, one should never proceed if there is a fluid spill where the central catheter enters the skin. It is important to note, however, that there is NO contraindication to performing routine NCSs on patients with peripheral IVs. Studies have been reported that specifically address this question and they find that NCSs are completely safe in patients with peripheral IVs, regardless of whether they are infusing saline or any other solution. Although NCSs in patients with central lines have not demonstrated any adverse reactions, the numbers that have been studied are relatively small. Thus it remains reasonable to follow the precautions provided here.  Implanted Pacemakers and Cardioverter-­Defibrillators Patients with implantable cardiac pacemakers and cardioverter-­ defibrillators are at much lower risk from stray current leaks than patients with central lines or external wires in place, because these devices are implanted under the skin, which leaves the normal protective mechanism of the skin intact. Implantable pacemakers and cardioverter-­defibrillators both have electronic-­sensing and electronic-­delivery functions. Pacemakers are designed to treat bradycardia, as opposed to cardioverter-­ defibrillators,

which are primarily used for tachyarrhythmias, especially ventricular fibrillation. In theory, stimulation delivered during NCSs might be mistaken as an abnormal cardiac rhythm. If the stimulator has a pulse duration greater than 0.5 ms and a stimulus rate greater than 1 Hz, a demand pacemaker might theoretically confuse such a stimulus with the ECG signal. There is only a single case report of an implantable pacemaker failure thought to be related to peripheral nerve stimulation. Other studies have shown no pacemaker inhibition or dysfunction with NCSs. Less is known about implantable automatic cardioverter-­defibrillators (IACDs), which are now common. In theory, IACDs could be triggered by stimulation during NCSs, resulting in subsequent cardiac arrhythmias; however, there are no such reported cases. One study directly addressed the safety of NCSs, including stimulating Erb’s point, in patients with IACDs. Schoeck and colleagues studied 10 patients with pacemakers and 5 with IACDs. No electrical impulse was detected by either the atrial or ventricular amplifiers of the pacemakers or of the IACDs during median and peroneal NCSs. These studies included Erb’s point stimulation on the left side. The authors emphasized that all modern pacemakers and IACDs use bipolar leads wherein both leads (active and reference for sensing, and cathode and anode for stimulating) are imbedded in the cardiac wall. This is in contradistinction to the pacemakers used 25 years ago wherein a single wire lead was placed in the heart, and the metal body of the pacemaker in the chest served as the reference. In modern pacemakers and IACDs, the bipolar leads are very close together in the heart, and very far away from the surface, making any electrical contamination from NCSs extremely unlikely. Although the number of patients in this study was small, the results are reassuring that NCSs can be safely performed in patients with pacemakers and IACDs. If NCSs are performed in patients with implantable pacemakers or IACDs, several simple procedures are recommended to be followed to preserve safety (Box 43.2). Stimulation should not be performed near the actual implanted device. There should always be a minimum of 6 inches between the implanted device and the stimulator. Just as with NCSs performed in a patient with a central Box 43.2  Guidelines for Pacemakers and Implantable Cardioverter-­Defibrillators • Do not perform studies on patients with external pacer wires. • Ensure that all ground electrodes are functional. • Limit all electrodes, including the ground, to the extremity of interest, and keep all electrodes as far away from the heart as possible, without crossing cardiac devices or their wires. • Do not stimulate near the device (allow a minimum of 6 inches) and avoid ipsilateral proximal stimulation sites (i.e., axilla, Erb’s point, root stimulation). • Use a stimulus duration of 0.2 ms or shorter and a stimulus rate of 1 Hz or slower. Thus, the typical repetitive stimulation done during neuromuscular junction testing is best avoided. • Consult a cardiologist regarding performing studies in patients with an implantable automatic cardioverter-­defibrillator. • Laboratory emergency drugs should be available, including crash carts. With permission from Al-­Shekhlee A, Shapiro BE, Preston DC. Iatrogenic complications and risks of nerve conduction studies and needle electromyography. Muscle Nerve. 2003;27:517–526, with permission.

Chapter 43 • Electrical Safety and Iatrogenic Complications of Electrodiagnostic Studies 755

line, it is preferable to use the contralateral arm if possible. High stimulus intensities should be avoided and stimulus pulse duration should be 0.2 ms or less so that the stimulation is not misinterpreted as a QRS complex. Stimulation rates should be no greater than 1 Hz so as to prevent the theoretical risk that the stimulation is misinterpreted as a cardiac rhythm. Thus, the typical repetitive stimulation done during neuromuscular junction testing is best avoided. 

PNEUMOTHORAX Pneumothorax is the most potentially serious iatrogenic complication of needle EMG. At any time during or just after the EMG examination, unexpected chest pain, shortness of breath, or cyanosis in a patient should alert the electromyographer to the possibility of a pneumothorax. If such symptoms develop, a prompt chest x-­ray film is indicated to confirm the diagnosis, followed by urgent consultation with a thoracic surgeon as to whether a chest tube or observation is required. Use of neuromuscular ultrasound to aid in EMG needle placement in muscles at high risk for pneumothorax is discussed in detail in Chapter 40. Although rare, this complication has been most often reported when sampling the following high-­risk muscles (Fig. 43.7):    • Diaphragm. Needle EMG of the diaphragm is sometimes used to help determine whether respiratory insufficiency has a neuromuscular basis. However, because the pleural fold is in close proximity to the diaphragm, a relatively small error in needle position may increase the risk of inadvertent pleural puncture and possible pneumothorax. The decision to sample the diaphragm depends on the experience of the electromyographer along with weighing the risk of pneumothorax to the potential benefit in that particular patient. Because patients for whom this study is ordered often have respiratory problems that prompt the study to be ordered, they may be the least able to handle an additional respiratory complication. In Chapter 13, we purposely did not include the diaphragm as a routine muscle to study during needle EMG. In our opinion, the risk-­to-­benefit ratio of sampling this muscle by using surface landmarks is too high to justify its use as a routine

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muscle to be sampled. However, if ultrasound guidance is employed, safety of needle EMG of the diaphragm is assured. Ultrasound can be used either directly or indirectly to safely perform diaphragmatic needle EMG (see Chapter 40 for full discussion). • Serratus anterior. The serratus anterior muscle lies between the scapula and the chest wall and inserts laterally on the ribs. An inadvertent puncture through the muscle between the ribs may allow the needle to enter the pleural space. To reduce the possibility of pneumothorax, the muscle can be sampled with the electromyographer’s fingers placed in two adjacent inter-­rib spaces while the needle is inserted into the muscle directly over the rib. • Supraspinatus. The supraspinatus muscle lies within the supraspinous fossa of the scapula. The middle of the fossa may be very shallow in some individuals. Thus, if the muscle is sampled too deeply at this point, the needle may puncture the pleura (Fig. 43.8). Complica-





Fig. 43.7  Needle electromyography (EMG) and the risk of pneumothorax.  One of the most potentially serious complications of needle EMG is pneumothorax. Left, Although rare, this complication has been reported when sampling the following common muscles: (1) supraspinatus, (2) serratus anterior, (3) lower cervical paraspinal muscles, (4) rhomboids, and (5) thoracic paraspinal muscles. Right, Note the absence of normal lung markings due to pneumothorax. Arrows point to the collapsed right lung.

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SECTION X   Electronics and Instrumentation

tions can be prevented by either avoiding the muscle altogether or sampling it more medially in the supraspinous fossa. This is performed by first palpating the acromion, the spine of the scapula, and the vertebral border of the scapula. The needle is then inserted just above the spine of the scapula at a point three-­quarters of the distance from the acromion to the vertebral border of the scapula. Often, the supraspinatus can be avoided by sampling the infraspinatus instead. The infraspinatus muscle and infraspinous fossa are much larger than the supraspinatus and supraspinous fossa above. When screening for a suprascapular neuropathy, the infraspinatus muscle is the preferred muscle to study. Only if the infraspinatus muscle is abnormal is it then necessary to sample the supraspinatus to differentiate a lesion at the spinoglenoid notch from one at the suprascapular notch or above (see Chapter 34). • Rhomboids. The rhomboids are infrequently sampled. However, they are useful to study in two situations: (1) to differentiate a C5 from a C6 radiculopathy (the rhomboids are derived from the C4–C5 roots) and (2) to differentiate an upper trunk brachial plexopathy from a more proximal radiculopathy (the rhomboids are innervated by the dorsal scapular nerve, which arises directly from the ventral rami of the roots proximal to the brachial plexus). Because the rhomboids originate on the dorsal spine and insert onto the medial border of the scapula, a needle placed too deeply may pass through the rhomboids and thoracic paraspinal muscles, resulting in a pleural puncture. • Cervical and thoracic paraspinal muscles. The cervical paraspinal muscles are commonly sampled in the evaluation of cervical radiculopathy. Thoracic paraspinal muscles are one of the key sites to study in the evaluation of suspected motor neuron disease. These muscles can be safely studied, provided the needle placement is neither too lateral nor too deep. Considering the proximity of the thoracic paraspinal muscles to the lungs in the thorax, it is not unexpected that pneumothorax is a potential complication of thoracic paraspinal muscle sampling (Fig. 43.9). However, pneumothorax can also occur during EMG examination of the lower cervical paraspinal muscles or when an EMG needle is used for cervical nerve root stimulation. Some patients, especially Fig. 43.9  Thoracic paraspinal muscles and the risk of pneumothorax. Axial computed tomographic scan of a normal individual at the midthoracic level (left), with magnified view of the thoracic paraspinal muscles (right). Note the close proximity of the thoracic paraspinal muscles to the lungs. The correct location for sampling the paraspinal muscles is (B), just off the midline with the needle directed down and slightly medially. If the needle is placed too laterally (A) and directed deep and lateral, there is a risk of pneumothorax.

those who are thin with longer necks, may have lung tissue that reaches above the clavicle (Fig. 43.10). In one study of 23 patients, 22% had lung tissue above the level of the clavicle. The average distance between skin and lung in these individuals was 3.3 cm, a distance clearly within the reach of a conventional 37-­or 50-­mm EMG needle. This complication is easily prevented by ensuring that the needle remains close to the midline, within the bulk of the paraspinal muscles.    In a study by Kassardjian and colleagues at the Mayo Clinic, seven cases of symptomatic pneumothorax were seen over 18 years in the evaluation of 64,490 patients. The most common muscle sampled associated with pneumothorax was the serratus anterior (0.445%), followed by the diaphragm (0.149%). In these rare cases, the time period when patients became symptomatic ranged from during the performance of the EMG itself to up to 1 day later. 

BLEEDING Needle EMG is generally well tolerated, with minimal or no bleeding. Some patients develop minor bruising that resolves within a few days. However, the possibility of bleeding and subsequent hematoma formation is a theoretic risk any time a needle punctures the skin, whether it occurs during phlebotomy, vaccination, aspiration, or needle EMG examination of a muscle. Clearly, the chance of bleeding increases if a patient has certain risk factors (discussed in the following section). However, bleeding can occur in the absence of any known risk factors or without deviation from the usual performance of the examination. In one report from Caress and colleagues, a patient with a large asymptomatic paraspinal hematoma was discovered incidentally on MRI just after needle examination of the lumbar paraspinal muscles, which had been performed for evaluation of lumbar radiculopathy. By happenstance, the patient had an MRI of the lumbar spine scheduled immediately after the EMG. The patient was not anticoagulated and had no risk factors for increased bleeding. Following this case, a retrospective review of patients referred to the EMG laboratory followed by MRI the same day revealed four other patients with radiologically proven paraspinal

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Chapter 43 • Electrical Safety and Iatrogenic Complications of Electrodiagnostic Studies 757

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Fig. 43.10  Lower cervical paraspinal muscles and the risk of pneumothorax.  Left, In some individuals, the lung apex rises above the clavicle, where it may be punctured from a laterally placed electromyographic needle. Right, Axial computed tomographic scan of a normal individual at the C7–T1 vertebral level. Note that the correct location for sampling the paraspinal muscles is (B), just off the midline with the needle directed down and slightly medially. If the needle is placed too laterally (A) and directed deep and lateral, there is a risk of pneumothorax at this level in some individuals.

muscle hematomas, presumably as a result of the needle EMG examination. All patients were asymptomatic and had no history of anticoagulation or other known risk factors for bleeding. However, in a large study from Gertken et al., 370 patients who underwent EMG studies that included the paraspinal muscles and who then had an MRI scan at the concordant spinal level were examined. Of these patients, 168 MRIs were completed the same day as the EMG, and the remaining were completed within 7 days. A combined total of 431 spine segments were studied. No paraspinal hematoma was observed in any patient, including 139 patients taking aspirin, 10 on warfarin (INRs between 1.2 and 2.9), 8 on clopidogrel, and 4 patients who were on heparin, enoxaparin, or dalteparin. In a prospective study by Lynch et  al., EMG examination of the tibialis anterior muscle was followed by ultrasound to evaluate for the presence of a hematoma. Two of 101 patients on warfarin (INR values of 1.5 or above) had small, subclinical hematomas. Of 57 patients taking clopidogrel and/or aspirin, 1 patient was found to have a small, subclinical hematoma on ultrasound. None of the 51 control patients, who were not taking warfarin, aspirin, or clopidogrel, were found to have a hematoma by ultrasound. A prospective study by Boon et al. examined the incidence of hematoma, using ultrasound examination, after needle EMG of potentially “high-­ risk” muscles (cervical, thoracic, and lumbar paraspinals; tibialis posterior; flexor digitorum longus; flexor pollicis longus; iliopsoas). A total of 205 patients were studied: 58 on warfarin, 78 on aspirin/ clopidogrel, and 70 control patients taking none of these medications, with a minimum of 100 muscles per patient group. One patient in the aspirin/clopidogrel group had a subclinical hematoma in the tibialis posterior muscle, and

one patient in the warfarin group had a subclinical hematoma in the flexor pollicis longus (INR 2.3). No patient in the control group had a hematoma. There are also some case reports of bleeding following needle EMG in anticoagulated patients. In one anticoagulated patient (INR 2.5), a hematoma developed in the posterior calf along with a pseudoaneurysm of the posterior tibial artery. She improved with supportive care and holding the anticoagulation. In another case, a patient taking warfarin developed a large subcutaneous hemorrhage near an EMG needle insertion point. In addition, there are two case reports of EMG needle– induced laceration or injury to nearby blood vessels that resulted in bleeding and a subsequent compartment syndrome requiring urgent fasciotomy and surgical evacuation of the hematoma. In one case, the compartment syndrome occurred in the superficial posterior compartment of the lower leg, presumably as a result of puncturing a small vessel. In the other case, needle EMG of the flexor carpi radialis inadvertently injured the ulnar artery, resulting in a compartment syndrome of the forearm. In neither of these cases was the patient anticoagulated or regularly taking any anti-­platelet agents.

Risk of Bleeding Coexistent Medical Conditions Several medical conditions are associated with an increased risk of bleeding and pose a potential risk during needle EMG. Thrombocytopenia with platelet counts below 50,000/mm3 increases the chance of bleeding, and the risk increases markedly if the count drops below 20,000/mm3. Chronic renal failure is associated with dysfunctional platelets that increase the risk of bleeding. Patients with coagulopathies,

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either acquired (e.g., liver failure, disseminated intravascular coagulation) or inherited (e.g., hemophilia), are at a substantially higher risk of bleeding with invasive procedures.  Anticoagulation, Antiplatelet Agents, and Other Drugs Similar to other invasive procedures, the risk of bleeding with needle EMG increases with the use of several prescription drugs as well as some over-­the-­counter (OTC) agents. Patients who are anticoagulated or taking an antiplatelet agent are often referred to the EMG laboratory. Anticoagulation with either intravenous heparin, oral warfarin or the newer novel oral anticoagulants (NOACs) carries the highest risk of bleeding. However, aspirin, nonsteroidal antiinflammatory drugs (NSAIDs), and other antiplatelet agents (e.g., clopidogrel) also increase the risk of bleeding. All of these agents are in common use for cardiovascular and stroke protection. Aspirin and NSAIDs are in widespread use for many painful conditions. In addition, some common OTC herbal remedies (e.g., Saw Palmetto, Ginkgo biloba, garlic, Ginseng, Hsien-­Ho-­T’sao) have a mild anticoagulant effect that now is appreciated to increase the risk of bleeding with invasive procedures and surgery. 

Recommendations Needle Electromyography and Patients at Risk of Bleeding There is a paucity of evidence-­based medicine to help guide the electromyographer in dealing with a patient referred for EDX studies who has an increased risk of bleeding. However, keep in mind that it is not common practice to report bleeding complications from invasive procedures in such patients, and the lack of reports by no means indicates that such complications cannot and do not occur. In patients with hemophilia, thrombocytopenia, and similar coagulopathies, use of replenishing clotting factors or platelets is indicated prior to the procedure. Regarding patients taking antiplatelet agents, it is the general consensus that needle EMG can be performed safely on these patients and that these agents do not need to be held before the procedure. However, in a survey of 47 academic EMG laboratories with an ACGME-­approved fellowship, 19% of laboratories reported curtailing some portion of the needle EMG examination in patients taking antiplatelet agents. Due to the lack of guidelines and the theoretic risks of bleeding in anticoagulated patients, the patient who is anticoagulated with heparin, warfarin, or NOACs is the most problematic. In addition to the reviews and anecdotal case reports noted earlier, some information is available from anticoagulated patients who developed complications following other procedures that use needles. Compartment syndromes have been reported following venipuncture in the antecubital fossa. There is a single case report of a radial palsy following antecubital fossa venipuncture, presumably from a dissecting hematoma. However, in these cases, the risk of bleeding is expected to be higher than with needle EMG, where the goal is to avoid vascular structures rather than to enter them intentionally. In the lower extremity, gluteal compartment syndromes and compression of the sciatic

nerve have been reported following intramuscular injections in anticoagulated patients. On the other hand, intramuscular vaccinations in the deltoid (e.g., flu vaccine) are commonly given in anticoagulated patients without complication. Due to the theoretic risk of complications and concern about litigation if such a complication occurs, some electromyographers will not perform needle EMG on an anticoagulated patient. For many diagnoses, including carpal tunnel syndrome, ulnar neuropathy at the elbow, and peripheral neuropathy, useful information can be obtained from the NCSs alone. Nevertheless, without the needle EMG portion of the examination, some information will not be available to complete the picture (e.g., active vs. chronic denervation, the amount of denervation, etc.). On the other hand, some diagnoses rely principally on the findings obtained from the needle EMG examination, among them motor neuron disease, myopathy, and radiculopathy. If needle EMG is not performed on such patients, this may deny them the benefit of a procedure that might be the key to their diagnosis. It should be kept in mind that in the case of motor neuron disease and myopathy, needle EMG is a less invasive diagnostic procedure than muscle biopsy. In the survey of academic EMG laboratories mentioned earlier, only 21% reported a willingness to examine all muscles in anticoagulated patients. In others, some muscle groups were not examined in anticoagulated patients: 45% would not perform EMG on the cranial or facial muscles; 66% not on the paraspinal muscles; and 34% not on some limb muscles. Some electromyographers choose to stop the anticoagulation prior to the procedure. Before dental work and minor invasive procedures (e.g., colonoscopy), it is common practice to advise patients to stop their anticoagulation several days before the procedure and restart it immediately afterward. In patients who are anticoagulated to prevent thromboembolism, especially stroke, the decision to stop anticoagulation is complex. Because it takes a few days for warfarin to have an effect, using this strategy will leave the patient unprotected for several days. For two of the more common conditions for which anticoagulation is prescribed, i.e., nonvalvular atrial fibrillation and a mechanical heart valve, the estimated stroke risk without anticoagulation is appropriately 3% per year. Thus, a patient who is not protected by anticoagulation for 5–10 days incurs a risk of stroke between 1 in 1000 and 1 in 2000. Although this risk is low, it is not one in a million, and the risk-­to-­benefit ratio of stopping anticoagulation, even for such a brief period of time, must be taken into account. With the NOACs, the time off anticoagulation is much shorter. In general, if needle EMG is performed on an anticoagulated patient, the best strategy is to perform a limited needle EMG study using the following guidelines:    • U  se the smallest gauge EMG needle available (e.g., 25 gauge). • Limit the study to superficial muscles where prolonged compression over a puncture site can be performed if necessary. • Avoid deep muscles that cannot be manually com-

Chapter 43 • Electrical Safety and Iatrogenic Complications of Electrodiagnostic Studies 759

pressed and theoretically could result in a compartment syndrome if a hematoma developed. Most important among these are the antecubital fossa muscles (i.e., pronator teres and flexor carpi radialis), tibialis posterior, and flexor digitorum longus. • Avoid muscles where hematomas theoretically could compress adjacent neurologic structures. Most important among these are the gluteal muscles near the sciatic nerve and the paraspinal muscles near the exiting spinal nerves. • Avoid muscles with large arteries or veins located nearby so that inadvertent puncture of the vessel is not a risk. Most important among these are the flexor pollicis longus near the radial artery, the iliacus near the femoral artery/vein, and the antecubital fossa muscles near the brachial artery.    This approach has been used successfully by us and several of our EMG colleagues for many years without any complications. However, as in all invasive procedures, the potential benefits always need to be weighed against the potential risks in the individual patient before using any of these strategies in anticoagulated patients referred for an EDX procedure. 

INFECTION Electrodes and needles used for EDX studies carry the possible risk of transmitting infection between patients or between the electromyographer and the patient. Although this risk is higher during the needle EMG portion of the examination, skin preparation occasionally may abrade the skin, resulting in minor oozing or bleeding, potentially contaminating surface electrodes used for NCSs. As learned from the human immune deficiency virus (HIV) epidemic, one should always assume that infection is possible and follow universal precautions. Hand washing before and after a patient encounter is essential. Gloves should always be worn during potential exposure to blood, which occurs during every needle EMG examination. After every NCS, surface electrodes should be cleaned with a 1:10 dilution of bleach or 70% isopropyl alcohol. If reusable needle electrodes are used (i.e., single-­fiber needle electrodes), they should be autoclaved after every use, similar to any other surgical instrument. Note that standard autoclaving does not neutralize Jacob-­Creutzfeldt disease infection, and any reusable electrode used on such a suspected patient should be discarded. As discussed in Chapter 37, concentric needles are now most often used for single-­fiber EMG studies. One of the principal reasons is that patients will not accept any “reused” needle, despite surgical sterilization. Thus, from a practical point of view, all needles used in EDX studies are now single-­use needles, which are discarded after the study. Before needle EMG, the historical teaching has been to clean the skin with an alcohol wipe to reduce the chance of introducing a bacterial infection from the skin. This is no different from the nurse swabbing the skin with alcohol prior to administrating a vaccination. However, there is little to no data on this topic. In studies of diabetic patients who inject insulin,

Fig. 43.11  Reducing the risk of a needle stick.  The risk of a needle stick can be markedly reduced if the needle is not recapped using two hands, but rather placed safely out of the way when not in use. One successful approach is to use a foam rubber block attached to the preamp arm of the electromyographic (EMG) machine. The needle cap can be placed in the block, so that the needle can be recapped safely with one hand. There are also other commercially available needle holders that can be attached to the EMG machine.

the chance of a subsequent skin infection was not increased in those who did not use alcohol. However, insulin is subcutaneous, whereas needle EMG (and vaccinations) are deeper and intramuscular. Although it probably makes little difference, we continue to clean the skin with alcohol in most of our patients. Inadvertent needle sticks are a risk during needle EMG. Transmissible diseases, including HIV, as well as other infections, especially viral hepatitis, underscore the importance of hepatitis B vaccinations for all electromyographers. Similar to precautions used with any needle, the EMG needle should not be recapped using the contralateral hand. The risk of a needle stick is markedly reduced if the needle is placed safely out of the way when it is not being used (e.g., in between sampling muscles or when explaining the next muscle movement to the patient). In our laboratory, we successfully use a foam rubber block attached to the preamp arm of the EMG machine (Fig. 43.11). The block holds the needle cap so that the needle can be recapped safely with one hand. There are also other commercially available needle holders that can be attached to the EMG machine. Fortunately, there appears to be little risk of transmitting infection to the patient during NCSs and needle EMG. With the modern use of sterilized, single-­use needle electrodes, this complication has not been reported. However, there are several situations wherein the risk of infection with needle EMG is theoretically higher. An EMG needle should never be placed through an infected space (e.g., skin ulcer), to prevent the spread of infection into deeper tissues. The question of whether needle EMG is contraindicated in the feet of patients with diabetic neuropathy or vascular insufficiency is unresolved. Such patients are commonly advised by their physician to inspect their feet and to avoid minor infections that

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SECTION X   Electronics and Instrumentation

could potentially threaten the limb if the infection became severe. Although there are no such reported cases, it is reasonable to be very cautious when performing needle EMG on intrinsic foot muscles in patients with diabetes or significant peripheral vascular disease. Similarly, patients who have undergone axillary lymph node dissections (usually in the context of breast cancer surgery) are cautioned against blood drawing and similar procedures in the ipsilateral extremity because of the possibility that an infection could spread quickly in the setting of lymphedema and a reduced number of lymph nodes proximally. Although there are no reported cases of infection in such patients following needle EMG, reasonable caution should be exercised in such patients. Finally, the issue of using prophylactic antibiotics in patients at high risk for endocarditis should be addressed. Antibiotic prophylaxis is not recommended by the American Heart Association in patients undergoing needle EMG, where the risk is considered similar to phlebotomy. 

LOCAL INJURY Needle-­induced local injury rarely occurs. Theoretically, an EMG needle could directly injure a nerve from direct intraneural puncture. To our knowledge, there is no reported case of such an injury. In near-­nerve studies and during local anesthetic blocks, needle electrodes are intentionally placed very close to nerves, with intraneural placements not infrequently occurring without any sequelae. During routine needle EMG, there are several areas where nerves travel near or through the muscle of interest. Most important among these are the following:    • Sciatic nerve and the gluteus maximus • Superficial radial nerve and the flexor pollicis longus • Ulnar nerve and the flexor digitorum profundus • Median nerve and the pronator teres    Needle-­induced paresthesias of these nerves are encountered occasionally during routine needle EMG. When this occurs, the needle should immediately be withdrawn from the muscle, and one should wait for the paresthesias to resolve before continuing to sample an alternative muscle or the original muscle at a different site. Although there are no reported cases of EMG needle– induced nerve trauma, there are reports of nerve trauma from other types of needles, most often occurring during venipuncture as well as other procedures. The median, lateral antebrachial, medial antebrachial, and superficial radial sensory nerves are the ones most often reported to be damaged during venipuncture. 

HYPERSENSITIVITY REACTIONS Although patients can have allergic reactions to a variety of allergens, some encountered during diagnostic procedures, they are distinctly uncommon, with the exception of powdered latex gloves, which are now banned in the United States. However, there is one case report of a delayed hypersensitivity reaction to the needle EMG that resulted in blistering and granulomatous eruptions at all needle insertion

sites 2 days after the examination. Presumably, this occurred as a reaction to the metals contained in the EMG needle. 

ULTRASOUND CORRELATIONS Diagnostic neuromuscular ultrasound is completely safe. There are no iatrogenic complications associated with ultrasound. However, ultrasound can be used to prevent iatrogenic complications of needle EMG when studying certain muscles. As discussed in Chapter 40, ultrasound can be used either indirectly or directly during needle EMG of the diaphragm and other at risk muscles. By doing so, one markedly reduces the risk of a pneumothorax. The same procedure used for the diaphragm can be used for other muscles wherein inadvertent needle placement could result in a pneumothorax. The two best examples are the use of ultrasound to guide needle placement in the rhomboids (Fig. 43.12) and the serratus anterior (Fig. 43.13). First, ultrasound can visualize the muscle and help with direct needle EMG guidance, using either the in-­plane or out-­of-­plane technique (see Chapter 40 for details). Second, ultrasound can easily measure the distance to the muscle of interest from the skin surface. Similarly, the distance to the lung can also be easily measured. Knowing these depths can be extremely helpful in choosing the correct length needle and placing the needle in the right place, as one can properly approximate how far the needle needs to go in to reach the muscle, to ensure safety. These techniques are described in detail in Chapter 40. Lastly, in chronic conditions, ultrasound can directly assess muscle for denervation atrophy and may obviate the need for needle EMG examination; this can be especially helpful to avoid examining certain muscles with an EMG needle, which as noted earlier, may induce a pneumothorax. If a muscle is atrophic and hyperechoic on ultrasound, one recognizes that the muscle is abnormal and involved in a denervating process.

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Chapter 43 • Electrical Safety and Iatrogenic Complications of Electrodiagnostic Studies 761

Fig. 43.13  Ultrasound of the serratus anterior.  Top, Native image. Bottom, Same image with the serratus anterior in red, rib echo in green, and intercostal muscles in purple. Axial scan, over the chest at the mid-­axillary line. Beneath the skin and subcutaneous tissue, the serratus anterior is seen superficial to the rib and intercostal muscles.

With this information, needle EMG of the muscle is often superfluous. For example, in a traumatic case where the rhomboid is being studied to assess if the lesion is proximal to the brachial plexus, in some cases, the muscle is so atrophic, the needle could easily pass through the muscle without the electromyographer being aware. In such cases, an abnormal ultrasound image of the rhomboid muscle answers the question of whether that muscle is involved in the denervating process. Indeed, with muscles that are very close to the lung, needle EMG could increase the risk of pneumothorax, especially if the muscle is atrophic, and studying the muscle with neuromuscular ultrasound or with neuromuscular ultrasound guidance may be a better option. 

SUMMARY EDX studies as routinely performed often yield useful diagnostic information with minimal risks. However, it is essential that the electromyographer appreciate the known and theoretical complications discussed and follow the recommendations to minimize the chance of complications. Like all diagnostic tests, the electromyographer must always weigh the potential benefits of any EDX procedure versus the risks to the individual patient and use his or her best judgment.

Suggested Readings AAEM guidelines in electrodiagnostic medicine. Risks in electrodiagnostic medicine. Muscle Nerve. 1999;22:S53– S58.

Al-­Shekhlee A, Shapiro BE, Preston DC. Iatrogenic complications and risks of nerve conduction studies and needle electromyography. Muscle Nerve. 2003;27:517–526. Bolton CF. Electromyographic studies in special settings. In: Brown WF, Bolton CF, eds. Clinical Electromyography. 2nd ed. Stoneham, MA: Butterworth-­Heinemann; 1993:770– 774. Boon AJ, Gertken JT, Watson JC, et al. Hematoma risk after needle electromyography. Muscle Nerve. 2012;45:9–12. Butler ML, Dewan RW. Subcutaneous hemorrhage in a patient receiving anticoagulation therapy: an unusual EMG complication. Arch Phys Med Rehabil. 1984;65:733–734. Caress JB, Rutkove SB, Carlin M, et al. Paraspinal muscle hematoma after electromyography. Neurology. 1997;47:269–272. Cheema P, El-­Mefty O, Jazieh AR. Intraoperative haemorrhage associated with the use of extract of saw palmetto herb: a case report and review of literature. J Intern Med. 2001;250:167–169. Cronin EM, Gray J, Abi-­Saleh B, Wilkoff BL, Levin KH. Safety of repetitive nerve stimulation in patients with cardiac implantable electronic devices. Muscle Nerve. 2013;47(6):840–844. Cushman D, Henrie M, Vernon Scholl L, Ludlow M, Teramoto M. Ultrasound Verification of safe needle examination of the rhomboid major muscle. Muscle Nerve. 2018;57(1):61–64. Davison BL, Kosmatka PK, Ferlic RJ. Acute radial nerve compression following routine venipuncture in an anticoagulated patient. Am J Orthop. 1996;25:712–713. Farrell CM, Rubin DI, Haidukewych GJ. Acute compartment syndrome of the leg following diagnostic electromyography. Muscle Nerve. 2003;27:374–377. Gertken JT, Patel AT, Boon AJ. Electromyography and anticoagulation. PM&R. 2013;5:S3–7. Gertken JT, Hunt CH, Montes Chinea NI, et al. Risk of hematoma following needle electromyography of the paraspinal muscles. Muscle Nerve. 2011;44:439–440. Gruis KL, Little AA, Zebarah VA, et al. Survey of electrodiagnostic laboratories regarding hemorrhagic complications from needle electromyography. Muscle Nerve. 2006;34(3):356–358. Hawley RJ. Preventing complications of electromyography. Electromyogr Clin Neurophysiol. 2000;40:323–325. Honet JE, Honet JC, Cascade P. Pneumothorax after electromyographic electrode insertion in the paracervical muscles: case report and radiological analysis. Arch Phys Med Rehabil. 1986;67:601–603. Horowitz SH. Peripheral nerve injury and causalgia secondary to routine venipuncture. Neurology. 1994;44:962–964. Kassardjian CD, O’Gorman CM, Sorenson EJ. The risk of iatrogenic pneumothorax after electromyography. Muscle Nerve. 2016;53(4):518–521. Kleiter I, Dickel H, Soemantri SP, Börnke C. Allergic granulomatous skin reaction to electromyography needle. Muscle Nerve. 2014;50(5):867–868. LaBan MM, Petty D, Hauser AM, et al. Peripheral nerve conduction stimulation: its effect on cardiac pacemakers. Arch Phys Med Rehabil. 1988;69:358–362. London ZN. Safety and pain in electrodiagnostic studies. Muscle Nerve. 2017;55(2):149–159.

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London ZN, Mundwiler A, Oral H, Gallagher GW. Nerve conduction studies are safe in patients with central venous catheters. Muscle Nerve. 2017;56(2):321–323. Lynch SL, Boon AJ, Smith J, et al. Complications of needle electromyography: hematoma risk and correlation with anticoagulation and antiplatelet therapy. Muscle Nerve. 2008;38(4):1225–1230. Mellion ML, Buxton AE, Iyer V, et al. Safety of nerve conduction studies in patients with peripheral intravenous lines. Muscle Nerve. 2010;42(2):189–191. Pneumothorax Miller J. Complication of needle EMG of thoracic wall. N J Med. 1990;87:653. Nora LM. American Association of Electrodiagnostic Medicine guidelines in electrodiagnostic medicine: implanted cardioverters and defibrillators. Muscle Nerve. 1996;19:1359–1360. O’Flaherty D, Adams AP. Pacemaker failure and peripheral nerve stimulation. Anaesthesia. 1994;49:181. O’Flaherty D, Wardill M, Adams AP. Inadvertent suppression of a fixed rate ventricular pacemaker using a peripheral nerve stimulator. Anaesthesia. 1993;48:687–689. Parziale JR, Marino AR, Herndon JH. Diagnostic peripheral nerve block resulting in compartment syndrome. Am J Phys Med Rehabil. 1988;67:82–84. Pease WS, Grove SL. Electrical safety in electrodiagnostic medicine. PM&R. 2013;5:S8–13.

Preston D, Logigian E. Iatrogenic needle-­induced peroneal neuropathy in the foot. Ann Intern Med. 1988;109:921–922. Raj G, Kumar R, McKinney W. Safety of intramuscular influenza immunization among patients receiving long-­ term warfarin anticoagulation therapy. Arch Intern Med. 1995;155:1529–1531. Reinstein L, Twardzik FG, Mech Jr KF. Pneumothorax: complication of needle electromyography of supraspinatus muscle. Arch Phys Med Rehabil. 1987;68:561–562. Roberge RJ, McLane M. Compartment syndrome after simple venipuncture in an anticoagulated patient. J Emerg Med. 1999;17:647–649. Rosioreanu A, Dickson A, Lypen S, et al. Pseudoaneurysm of the calf after electromyography: sonographic and CT angiographic diagnosis. Am J Roentgenol. 2005;185:282–283. Sander HW, Quinto CM, Murali R, et al. Needle cervical root stimulation may be complicated by pneumothorax. Neurology. 1997;48:288–289. Schoeck AP, Mellion ML, Gilchrist JM, et al. Safety of nerve conduction studies in patients with implanted cardiac devices. Muscle Nerve. 2007;35(4):521–524. Starmer CF, McIntosh HD, Whalen RE. Electrical hazards and cardiovascular function. N Engl J Med. 1971;284:181–186. Vaienti L, Vourtsis S, Urzola V. Compartment syndrome of the forearm following an electromyographic assessment. J Hand Surg Br. 2005;30(6):656–657.

Appendix

NERVE CONDUCTION STUDIES: NORMAL ADULT VALUES Upper Extremity Studies Motor Studies

Record

Amplitude (mV)

Conduction Velocity (m/s)

Distal Latency (ms)

Median

Abductor pollicis brevis (APB)

≥4.0

≥49

≤4.4

7

Ulnar

Abductor digiti minimi (ADM)

≥6.0

≥49

≤3.3

7

Ulnar

First dorsal interosseous (FDI)

≥7.0

≥49

≤4.5

Variable (8–12a)

Radial

Extensor indicis proprius (EIP)

≥2.0

≥49

≤2.9

4–6

Nerve

aDistance

Distal Distance (cm)

measured with calipers. 

Antidromic Sensory  Nerve

Record

Amplitude (μV)

Conduction Velocity (m/s)

Distal Peak Latency (ms)

Distal Distance (cm)

Median

Digit 2

≥20

≥50

≤3.5

13

Ulnar

Digit 5

≥17a

≥50

≤3.1

11

Radial

Snuffbox

≥15

≥50

≤2.9

10

Dorsal ulnar cutaneousb

Dorsal D4–5 web space

≥8

≥50

≤2.5

8

cutaneousb

Lateral forearm

≥10

≥55

≤3.0

12

Medial antebrachial cutaneousb

Medial forearm

≥5

≥50

≤3.2

12

Lateral antebrachial aMany

consider ulnar antidromic sensory amplitudes that are higher than 10 μV to be normal in adults older than 60. bIn these less commonly performed studies, side-­to-­side comparisons, especially of amplitude, often are more useful than normal value tables, when symptoms and signs are limited to one side.

Palmar Mixed Nerve Studies  Nerve

Amplitude (μV)

Conduction Velocity (m/s)

Peak Distal Latency (ms)

Distance (cm)

Median mixed

≥50

≥50

≤2.2

8

Ulnar mixed

≥12

≥50

≤2.2

8

763

Appendix

764

F Responsesa  Nerve

Minimal F Latency (ms)

Median

≤31

Ulnar

≤32

Major Upper Extremity Motor Latencies from Erb’s Point Stimulation 

Nerve

aFor

tall or short patients, F responses must be normalized for height (see Chapter 4).

Median-­Ulnar Internal Comparison Studies 

Muscle

Latency (ms)

Distances (cm)a

Axillaryb

Deltoid

≤4.9

15–21

Musculocutaneousb

Biceps

≤5.7

23–29

Suprascapular

Supraspinatus

≤3.7

7–12

Suprascapular

Infraspinatus

≤4.3

10–15

aDistance

Studya

Significant Latency

Difference (ms)b

Median mixed Ulnar mixed

Palm to wrist Palm to wrist

≥0.4

Median motor

≥0.5

Ulnar motor

Wrist to second lumbrical Wrist to interossei

Median sensory Ulnar sensory

Wrist to digit 4 Wrist to digit 4

≥0.5

Median sensory Radial sensory

Wrist to digit 1 Wrist to digit 1

≥0.5

aFor

each paired study, identical distances are used for both the median and the ulnar study. bValues that exceed these cutoffs imply focal slowing and are useful in the electrodiagnosis of both median neuropathy across the carpal tunnel and ulnar neuropathy across Guyon’s canal.

Median Palmar Stimulation Studies 

Study

Significant Palm-­to-­Wrist Amplitude Ratioa

Median motor: wrist to abductor pollicis brevis Median motor: palm to abductor pollicis brevis

>1.2

Median sensory: wrist to digit 2 Median sensory: palm to digit 2

>1.6

aValues

measured with calipers. bThe axillary and musculocutaneous nerves also can be stimulated in the axilla, with typical distal motor latencies of up to 3.3 ms. Both axillary and Erb’s point stimulations often are technically difficult. In patients with symptoms limited to one side, comparing both latencies and amplitudes side to side always is preferable to using normal value tables. Data from Kraft GH. Axillary, musculocutaneous, and suprascapular nerve latency studies. Arch. Phys. Med. Rehab. 1972;53;382; and Currier DP. ­Motor conduction velocity of axillary nerve. Phys. Ther. 1971;51:503.

that exceed these cutoffs imply some element of conduction block of the median nerve across the carpal tunnel.

Phrenic Motor Studya  

Nerve Phrenic aFrom

Record Diaphragm

Amplitude (μV)

Distal Latency (ms)

597 ± 139 μV >320 μV

6.3 ± 0.8 1.5 ms is considered abnormal. 

bCompare

Notes: 1. All normal value tables assume controlled temperature and standard distances. 2. All motor and sensory amplitudes are measured from baseline to negative peak. 3. All sensory and mixed nerve distal latencies are peak latencies; however, all sensory and mixed nerve conduction velocities are calculated based on the onset latency. 4. Some values may have to be adjusted for extremes of height or age (see Chapter 8). 5. Comparison between the affected and unaffected limb often is very useful and may be more useful than normal value tables. 6. This is one set of normal values; others exist. Ideally, each laboratory should develop its own set of normal values.

Appendix 767

NERVE CONDUCTION STUDIES: NORMAL PEDIATRIC VALUES Motor Studies Median Nerve Age

DML (ms)

CV (m/s)

Peroneal Nerve

F (ms)

AMP (mV)

DML (ms)

CV (m/s)

F (ms)

AMP (mV)

(0.29)a

25.43 (3.84)

16.12 (1.5)

3.00 (0.31)

2.43 (0.48)

22.43 (1.22)

22.07 (1.46)

3.06 (1.26)

1–6 months

2.21 (0.34)

34.35 (6.61)

16.89 (1.65)

7.37 (3.24)

2.25 (0.48)

35.18 (3.96)

23.11 (1.89)

5.23 (2.37)

6–12 months

2.13 (0.19)

43.57 (4.78)

17.31 (1.77)

7.67 (4.45)

2.31 (0.62)

43.55 (3.77)

25.86 (1.35)

5.41 (2.01)

1–2 years

2.04 (0.18)

48.23 (4.58)

17.44 (1.29)

8.90 (3.61)

2.29 (0.43)

51.42 (3.02)

25.98 (1.95)

5.80 (2.48)

2–4 years

2.18 (0.43)

53.59 (5.29)

17.91 (1.11)

9.55 (4.34)

2.62 (0.75)

55.73 (4.45)

29.52 (2.15)

6.10 (2.99)

4–6 years

2.27 (0.45)

56.26 (4.61)

19.44 (1.51)

10.37 (3.66)

3.01 (0.43)

56.14 (4.96)

29.98 (2.68)

7.10 (4.76)

6–14 years

2.73 (0.44)

57.32 (3.35)

23.23 (2.57)

12.37 (4.79)

3.25 (0.51)

57.05 (4.54)

34.27 (4.29)

8.15 (4.19)

7 days–1 month

2.23

AMP, Amplitude; CV, conduction velocity; DML, distal motor latency; F, F latency. aData are provided as mean (SD). From Parano E, Uncini A, DeVivo DC, et al. Electrophysiologic correlates of peripheral nervous system maturation in infancy and childhood. J. Child. Neurol. 1993;8:336–338. 

Antidromic Sensory Studies Median Nerve Age

Sural Nerve

CV (m/s)

AMP (μV)

CV (m/s)

7 days–1 month

22.31

(2.16)a

AMP (μV)

6.22 (1.30)

20.26 (1.55)

9.12 (3.02)

1–6 month

35.52 (6.59)

15.86 (5.18)

34.63 (5.43)

11.66 (3.57)

6–12 month

40.31 (5.23)

16.00 (5.18)

38.18 (5.00)

15.10 (8.22)

1–2 years

46.93 (5.03)

24.00 (7.36)

49.73 (5.53)

15.41 (9.98)

2–4 years

49.51 (3.34)

24.28 (5.49)

52.63 (2.96)

23.27 (6.84)

4–6 years

51.71 (5.16)

25.12 (5.22)

53.83 (4.34)

22.66 (5.42)

6–14 years

53.84 (3.26)

26.72 (9.43)

53.85 (4.19)

26.75 (6.59)

AMP, Amplitude; CV, conduction velocity. aData are provided as mean (SD). From Parano E, Uncini A, DeVivo DC, et al. Electrophysiologic correlates of peripheral nervous system maturation in infancy and childhood. J. Child Neurol. 1993;8:336–338. 

NORMAL MOTOR UNIT ACTION POTENTIAL DURATION Mean Motor Unit Action Potential Duration Based on Age and Muscle Group Age of Subjects (yrs)

Arm Muscles (ms)

Leg Muscles (ms)

Deltoid

Biceps

Triceps

Thenar

ADM

Quad, BF

Gastroc

Tib Ant

Per Long

EDB

Facial

0–4

7.9–10.1

6.4–8.2

7.2–9.3

7.1–9.1

8.3–10.6

7.2–9.2

6.4–8.2

8.0–10.2

6.8–7.4

6.3–8.1

3.7–4.7

5–9

8.0–10.8

6.5–8.8

7.3–9.9

7.2–9.8

8.4–11.4

7.3–9.9

6.5–8.8

8.1–11.0

5.9–7.9

6.4–8.7

3.8–5.1

10–14

8.1–11.2

6.6–9.1

7.5–10.3

7.3–10.1

8.5–11.7

7.4–10.2

6.6–9.1

8.2–11.3

5.9–8.2

6.5–9.0

3.9–5.3

15–19

8.6–12.2

7.0–9.9

7.9–11.2

7.8–11.0

9.0–12.8

7.8–11.1

7.0–9.9

8.7–12.3

6.3–8.9

6.9–9.8

4.1–5.7

20–29

9.5–13.2

7.7–10.7

8.7–12.1

8.5–11.9

9.9–13.8

8.6–12.0 7.7–10.7 9.6–13.3

6.9–9.6

7.6–10.6

4.4–6.2

30–39

11.1–14.9 9.0–12.1 10.2–13.7 10.0–13.4 11.6–15.6 10.1–13.5 9.0–12.1 11.2–15.1

8.1–10.9

8.9–12.0

5.2–7.1

40–49

11.8–15.7 9.6–12.8 10.9–14.5 10.7–14.2 12.4–16.5 10.7–14.3 9.6–12.8 11.9–15.9

8.6–11.5

9.5–12.7

5.6–7.4

50–59

12.8–16.7 10.4–13.6 11.8–15.4 11.5–15.1 13.4–17.5 11.6–15.2 10.4–13.6 12.9–16.9

9.4–12.2

10.3–13.5 6.0–7.9

60–69

13.3–17.3 10.8–14.1 12.2–15.9 12.0–15.7 13.9–18.2 12.1–15.8 10.8–14.1 13.4–17.5

9.7–12.7

10.7–14.0 6.3–8.2

70–79

13.7–17.7 11.1–14.4 12.5–16.3 12.3–16.0 14.3–18.6 12.4–16.1 11.1–14.4 13.8–17.9 10.0–13.0 11.0–14.3 6.5–8.3

ADM, Abductor digiti minimi; BF, biceps femoris; EDB, extensor digitorum brevis; Gastroc, gastrocnemius; Per long, peroneus longus; Quad, quadriceps; Tib ant, tibialis anterior. Reprinted with permission from Buchthal F, Rosenfalck P. Action potential parameters in different human muscles. Acta Psych. Neurol. Scand. 1955. Munsgaard International Publishers Ltd, Copenhagen, Denmark. 

Appendix

768

ULTRASOUND CROSS-­SECTIONAL AREA REFERENCE RANGES Adult Normals Nerve

Site

Upper Limit of Normal (mm2)

Side-­to-­Side Upper Limit Difference (mm2)

Median

Wrist Forearm Pronator teres Antecubital fossa Mid-­arm Axilla

13.0 10.7 11.0 13.2 13.1 9.7

3.4 2.6 2.8 4.3 3.0 3.5

Ulnar

Wrist Forearm Distal elbow Elbow Proximal below Mid-­arm Axilla

8.1 8.3 8.6 8.8 9.3 8.3 8.6

2.6 2.0 2.0 2.2 1.8 1.6 1.8

Radial

Antecubital fossa Spiral groove

14.1 13.3

5.0 4.5

Musculocutaneous

Axilla

11.9

4.2

Vagus

Carotid bifurcation

9.0

3.1

Brachial plexus

Trunk

11.1

4.5

Sciatic

Distal thigh

80.6

18.9

Peroneal

Popliteal fossa Fibular head

20.9 17.8

9.5 4.9

Tibial

Popliteal fossa Proximal calf Ankle

55.9 39.9 22.3

15.7 10.8 5.7

Sural

Distal calf

8.9

2.6

Notes: Reference values are based on mean + 2 standard deviations. Nerve area may increase with increased BMI. Sources: 1. Cartwright MS, Shin HW, Passmore LV, Walker FO. Ultrasonographic reference values for assessing the normal median nerve in adults. J Neuroimaging. 2009;19(1):47–51. 2. Cartwright MS, Shin HW, Passmore LV, Walker FO. Ultrasonographic findings of the normal ulnar nerve in adults. Arch Phys Med Rehabil. 2007;88(3):394–396. 3. Cartwright MS, Passmore LV, Yoon JS, Brown ME, Caress JB, Walker FO. Cross-­sectional area reference values for nerve ultrasonography. Muscle Nerve. 2008;37(5):566-­571 

Pediatric Normalsa Age 0–3 y

Age 4–6 y

Age 7–11 y

Age 12–16 y

N

Mean (SD)

N

Mean (SD)

N

Mean (SD)

N

Mean (SD)

Median wrist

7

3.9 (1.1)

7

4.7 (1.0)

6

5.1 (0.2)

3

6.7 (0.6)

Median forearm

7

4.0 (0.9)

6

5.6 (1.9)

7

6.2 (1.5)

4

9.1 (2.3)

Ulnar wrist

2

2.5 (0.7)

2

4.5 (0.7)

2

3.5 (0.7)

6

5.8 (1.5)

Ulnar elbow

2

3.5 (0.7)

1

4.0 ( )

3

5.0 (2.0)

5

7.2 (1.3)

Radial groove

2

4.0 (0.0)

3

3.7 (1.5)

5

5.0 (0.7)

3

8.7 (1.5)

Sciatic leg

2

19.0 (2.8)

2

30.5 (7.8)

3

30.7 (7.5)

1

23.0 ( )

Peroneal knee

2

7.0 (1.4)

1

6.0 ( )

4

10.0 (2.9)

3

6.7 (3.1)

Tibial knee

2

11.5 (2.1)

1

18.0 ( )

4

19.5 (6.6)

3

19.7 (9.0)

Tibial ankle

2

7.5 (0.7)

3

9.0 (1.7)

4

7.5 (2.5)

5

12.6 (2.1)

Adapted from Cartwright MS, Mayans DR, Gillson NA, Griffin LP, Walker FO. Nerve cross-­sectional area in extremes of age. Muscle Nerve. 2013;47(6):890–893. aPlease note: the authors emphasized that there were few data points at each site for a given age. Therefore, this data should not be used to generate cutoff values for abnormal enlargement, but rather to provide a starting point for each laboratory to generate its own reference values.