indications for neuromuscular ultrasound: expert opinion

Clinical Neurophysiology xxx (2018) xxx–xxx

Contents lists available at ScienceDirect

Clinical Neurophysiology

journal homepage: www.elsevier .com/locate /c l inph

Indications for neuromuscular ultrasound: Expert opinion and review ofthe literature

https://doi.org/10.1016/j.clinph.2018.09.0131388-2457/� 2018 Published by Elsevier B.V. on behalf of International Federation of Clinical Neurophysiology.

⇑ Corresponding author at: Wake Forest School of Medicine, Medical Center Blvd, Winston-Salem, NC 27157-1078, USA.E-mail addresses: [email protected] (F.O. Walker), [email protected] (M.S. Cartwright), [email protected] (K.E. Alter), [email protected] (L.H. Vis

[email protected] (L.D. Hobson-Webb), [email protected] (L. Padua), [email protected] (J.A. Strakowski), [email protected] ([email protected] (A.J. Boon), [email protected] (H. Axer), [email protected] (N. van Alfen), [email protected] ([email protected] (E. Wilder-Smith), [email protected] (J.S. Yoon), [email protected] (B.-J. Kim), [email protected] (A. Breiner), [email protected] ([email protected] (A. Grimm), [email protected] (C.M. Zaidman).

Please cite this article in press as: Walker FO et al. Indications for neuromuscular ultrasound: Expert opinion and review of the literature. Clin Neuro(2018), https://doi.org/10.1016/j.clinph.2018.09.013

Francis O. Walker a,⇑, Michael S. Cartwright a, Katharine E. Alter b, Leo H. Visser c, Lisa D. Hobson-Webb d,Luca Padua e,f, Jeffery A. Strakowski g,h,i, David C. Preston j, Andrea J. Boon k, Hubertus Axer l,Nens van Alfenm, Eman A. Tawfik n, Einar Wilder-Smith o,p,q, Joon Shik Yoon r, Byung-Jo Kim s, Ari Breiner t,Jeremy D.P. Bland u, Alexander Grimmv, Craig M. Zaidmanw

aDepartment of Neurology at Wake Forest School of Medicine, Medical Center Blvd, Winston-Salem, NC, USAbDepartment of Rehabilitation Medicine, National INeurolnstitutes of Health, Bethesda, MD 20892, USAcDepartments of Neurology and Clinical Neurophysiology, Elisabeth-Tweesteden Hospital, Tilburg, The NetherlandsdDepartment of Neurology, Neuromuscular Division, Duke University School of Medicine, Durham, NC, USAeDon Carlo Gnocchi ONLUS Foundation, Piazzale Rodolfo Morandi, 6, 20121 Milan, ItalyfDepartment of Geriatrics, Neurosciences and Orthopaedics, Universita Cattolica del Sacro Cuore, Rome, ItalygDepartment of Physical Medicine and Rehabilitation, The Ohio State University, Columbus, OH, USAhDepartment of Physical Medicine and Rehabilitation, OhioHealth Riverside Methodist Hospital, Columbus, OH, USAiOhioHealth McConnell Spine, Sport and Joint Center, Columbus, OH, USAjNeurological Institute, University Hospitals, Cleveland Medical Center, Case Western Reserve University, Cleveland, OH, USAkDepartment of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN, USAlHans Berger Department of Neurology, Jena University Hospital, Jena 07747, GermanymDepartment of Neurology and Clinical Neurophysiology, Donders Institute for Brain, Cognition, and Behaviour, Radboud University Medical Center, Nijmegen, The NetherlandsnDepartment of Physical Medicine & Rehabilitation, Faculty of Medicine, Ain Shams University, Cairo, EgyptoDepartment of Neurology, Yong Loo Lin School of Medicine, National University Singapore, SingaporepDepartment of Neurology, Kantonsspital Lucerne, SwitzerlandqDepartment of Neurology, Inselspital Berne, SwitzerlandrDepartment of Physical Medicine and Rehabilitation, Korea University Guro Hospital, Seoul, Republic of KoreasDepartment of Neurology, Korea University Anam Hospital, Korea University College of Medicine, Seoul, Republic of KoreatDivision of Neurology, Department of Medicine, The Ottawa Hospital and University of Ottawa, CanadauDeparment of Clinical Neurophysiology, East Kent Hospitals University NHS Foundation Trust, Canterbury, Kent, UKvDepartment of Neurology, University Hospital Tuebingen, Tuebingen, GermanywDivision of Neuromuscular Medicine, Department of Neurology, Washington University in St. Louis, 660 S. Euclid Ave, Box 8111, St. Louis, MO 63110, USA

a r t i c l e i n f o h i g h l i g h t s

Article history:Accepted 2 September 2018Available online xxxx

Keywords:NeuropathyMyopathyMotor neuron diseaseElectromyographyNerve conduction studiesDiaphragm

� Experts routinely use ultrasound to evaluate both common and rare disorders of nerve and muscle.� Accumulated evidence now puts diagnostic neuromuscular ultrasound on par with EMG and NCS.� Medical centers must acquire ultrasound equipment to keep electrodiagnostic laboratories current.

a b s t r a c t

Over the last two decades, dozens of applications have emerged for ultrasonography in neuromusculardisorders. We wanted to measure its impact on practice in laboratories where the technique is in fre-quent use.After identifying experts in neuromuscular ultrasound and electrodiagnosis, we assessed their use of

ultrasonography for different indications and their expectations for its future evolution. We then

ser), lisa.Preston),Tawfik),. Bland),

physiol

https://doi.org/10.1016/j.clinph.2018.09.013

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2 F.O. Walker et al. / Clinical Neurophysiology xxx (2018) xxx–xxx

Please cite this article in press as: Walker FO et a(2018), https://doi.org/10.1016/j.clinph.2018.09

identified the earliest papers to provide convincing evidence of the utility of ultrasound for particularindications and analyzed the relationship of their date of publication with expert usage.We found that experts use ultrasonography often for inflammatory, hereditary, traumatic, compressive

and neoplastic neuropathies, and somewhat less often for neuronopathies and myopathies. Usage signif-icantly correlated with the timing of key publications in the field. We review these findings and theextensive evidence supporting the value of neuromuscular ultrasound. Advancement of the field of clin-ical neurophysiology depends on widespread translation of these findings.

� 2018 Published by Elsevier B.V. on behalf of International Federation of Clinical Neurophysiology.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

2.1. Expert panel. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002.2. Questionnaire . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002.3. Survey analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002.4. Literature review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002.5. Additional analysis of index papers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

3. Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.1. Indications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 003.2. Ultrasound first . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 003.3. Usefulness of ultrasound components and future expectations for the field . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4. Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005. The rationale underlying indications for neuromuscular ultrasound: A review. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

5.1. Generalized muscle disorders: . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.1.1. Inclusion body myositis (52%/16%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.1.2. Other inflammatory myopathies: dermatomyositis (51%/11%) and polymyositis (45%/11%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.1.3. Muscular dystrophy (44%/11%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.2. Muscle disorders, localized . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.2.1. Diaphragm paresis (66%/40%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.2.2. Selective muscle atrophy (61%/30%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.2.3. Intramuscular cysticercosis (50%/0%)** (Two asterisks mean that less than half the experts have seen patients with this indication,
one asterisk means that 6–9 of the experts have not seen it). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.2.4. Ultrasound guidance of chemodenervation (41%/24%)* . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.2.5. Camptocormia (38%24%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

5.3. Nerve disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.3.1. Regional or multifocal (primarily axonal) nerve disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.1. Nerve tumor or neuroma (89%/47%) (Beggs et al., 1999—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.2. Nerve torsion (81%/26%)* (Aryanyi et al., 2015—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.3. Thoracic outlet syndrome (75%/23%) (no index paper identified) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.4. Neurolymphomatosis (73%/33%)** (Vjayan et al., 2015—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.5. Brachial plexopathy (72%/24%) (Martinoli et al., 2002a—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.6. Neurofibroma (71%/48%) (Telleman et al., 2017a; 2017b—index papers) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.7. Lepromatous neuropathy (66%/26%)** (Martinoli et al., 2000—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.8. Brachial neuritis (63%/21%) (Arányi et al., 2015—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.9. Diabetic amyotrophy (28%/4%) (An et al., 2018—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.10. Cranial neuropathy (22%/6%) (Cartwright et al., 2009—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.1.11. Cervical radiculopathy (12%/6%) (Kim et al., 2015—index paper). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.2. Focal nerve disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.2.1. Tarsal tunnel syndrome (89%/31%) (Nagaoka et al., 2005—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.2.2. Fibular neuropathy (88%/29%) (Visser 2006—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.2.3. Ulnar neuropathy at the elbow (84%/31%) (Beekman et al., 2004—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.2.4. Carpal tunnel syndrome (82%/37%) (Buchberger et al., 1991—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.2.5. Other entrapment neuropathy (81%/29%) (no index paper identifiable) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3.2.6. Traumatic neuropathy (81%/29%) (Cartwright et al., 2007—index paper) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.4. Generalized primarily demyelinating nerve disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.4.1. Charcot Marie Tooth (CMT) (76%/25%) (Martinoli et al., 2002b—index paper). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.4.2. Chronic inflammatory demyelinating polyneuropathy (CIDP) (83%/19%) and multifocal motor neuropathy (MMN) (76%/19%)
(Sugimoto et al., 2013; Zaidman et al., 2013b—index papers for CIDP; Beekman et al., 2005 index paper for MMN) . . . . . . . . . 005.4.3. Hereditary neuropathy with liability to pressure palsies (HNPP) (68%/23%) (Beekman et al., 2002—index paper) . . . . . . . . . . . . 005.4.4. Guillain Barre syndrome/acute inflammatory demyelinating polyneuropathy (AIDP) (54%/9%) (Zaidman et al., 2009—index paper) 00

5.5. Generalized primarily axon/motor neuron loss disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.5.1. Motor neuron disease and amyotrophic lateral sclerosis (ALS) (77%/23%) (Arts et al., 2008—index paper) . . . . . . . . . . . . . . . . . . 005.5.2. Non-diabetic axonal polyneuropathy (32%/4%); diabetic polyneuropathy (27%/7%); toxic neuropathy (17%/8%) (Other-non-diabetic
polyneuropathy—no index paper identifiable; diabetic polyneuropathy Severenson et al., 2007—index paper; toxic polyneuropathyBriani et al., 2013—index paper). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

5.5.3. Sensory neuronopathy (22%/6%) (Pelosi et al., 2017—index paper). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

l. Indications for neuromuscular ultrasound: Expert opinion and review of the literature. Clin Neurophysiol.013


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5.6. Situational indications: . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.6.1. Palpable masses (86%/47%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.6.2. Variant anatomy (76%/34%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.6.3. Phobic patients or patients unable to tolerate electrodiagnosis (67%/67%) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
6. The value of neuromuscular ultrasound and the likelihood of its continued evolution: . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
6.1. Validity and limitations of the expert survey . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 006.2. Is there reason to expect that MRI will supersede ultrasound as a complementary routine test for neuromuscular evaluation? . . . . . . . 006.3. Relative growth of electrodiagnostic and ultrasound imaging technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 006.4. Added value of instrumentation and ultrasound in practice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 006.5. Future expectations for neuromuscular ultrasound . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 006.6. The nature of the current evidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
7. Translational implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
7.1. Re-envisioning electrodiagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Funding. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00Declarations of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00Appendix A. Supplementary material . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
1. Introduction

For much of the last fifty years, there has been remarkable uni-formity in electrodiagnostic practice. Aside from the rare patientwho might need referral to a specialized center for a single fiberEMG study, patients have been able to receive consistent diagnos-tic evaluations with comparable results regardless of the size of thelaboratory or its geographic location. However, now a number oflaboratories provide advanced ultrasound imaging in addition tostandard electrophysiological assessment of nerve and muscle, atrend that appears to be accelerating, and this is creating anunprecedented gap between ultrasound enhanced and standardclinical neurophysiology practice.

Over 25,000 papers have now been published in PubMed ondiagnostic ultrasound of nerve and/or muscle. It accurately estab-lishes a diagnosis for a wide variety of neuromuscular disorders(Hobson-Webb et al., 2018, Pillen et al., 2016, Cartwright et al.,2012). Furthermore, the technique has also changed the way wethink and speak. In the past it was common parlance to say thatthe nerves in chronic entrapment syndromes were ‘‘pinched,” butnow we have all seen how they can be focally or diffusely enlarged,subject to dynamic compression or internally distorted (Tagliafico2016). The purpose of this study was to conduct a survey of expertsto see how neuromuscular ultrasound is changing electrodiagnosis,its scope of applications, and to determine to what extent ultra-sound should be considered optional versus necessary in a modernclinical neurophysiology practice. It also looked to see how closelythe date of publications on new indications for ultrasound corre-lated with actual use of the technique, and finally, it reviewedthe literature, to present the evidence on the use of ultrasoundfor neuromuscular indications.

2. Methods

2.1. Expert panel

Members of the expert panel were drawn from suggestions offormer journal editors and members of the governance of the Inter-national Federation of Clinical Neurophysiology. They wereselected from three specialties that routinely practice electrodiag-nostic medicine: Neurology, Clinical Neurophysiology, and Physi-cal Medicine and Rehabilitation (PMR). Invitations were sent to22 identified individual experts of whom 19 agreed to participate;2 who chose not to participate were no longer actively involvedwith neuromuscular ultrasound and the third felt that expert sta-tus had yet to be reached. There were 8 neurologists, 6 clinical neu-rophysiologists, and 5 PMR physicians. All participants met the

cite this article in press as: Walker FO et al. Indications for neuromuscula), https://doi.org/10.1016/j.clinph.2018.09.013

following criteria: (a) significant practical experience with thetechnique; (b) participation in national and international coursesteaching neuromuscular ultrasound; and (c) multiple publicationsin the fields of both electrodiagnostic medicine and neuromuscularultrasound (mean = 57 publications per expert, including 5 text-books). The panel represented 9 different countries on 4 conti-nents. Since the survey was in part designed to assess theintegration of ultrasound into electrodiagnostic practice, expertsin neuromuscular ultrasound whose primary specialty was radiol-ogy or rheumatology were not included, although their contribu-tions to the field are cited throughout.

2.2. Questionnaire

The questionnaire was designed to estimate the frequency thatexperts use ultrasound for different indications in their practiceand how often they used ultrasound prior to electrodiagnostic test-ing. Additional questions were directed at how experts saw thefuture of the technology, how they characterized its diagnosticusefulness, and what aspects of instrumentation they found mosthelpful in their current practice. All the participant experts weregiven the opportunity to provide feedback on the questions priorto completing the survey.

2.3. Survey analysis

The survey on indications was intentionally worded with termsthat assessed relative frequency of use. It focused on currentusage--not intended usage in the future. Participants were askedif they had patients referred for the indication specified and if so,had they used ultrasound always, often, sometimes, or never inevaluating such patients. Subsequently, the same indications werereviewed to evaluate the expert’s use of ultrasound as the initialdiagnostic evaluation prior to electromyography (EMG) and nerveconduction studies (NCS), again, always, often, sometimes or never.For the purposes of analysis and data display, somewhat arbitraryunits were assigned (always = 100%, often = 70%; sometimes = 30%,never = 0%). For the portions of the survey assessing instrumenta-tion impact and future expectations for the field, questions alsoused qualitative terms. The assigned percentage values for theseterms is indicated in the figure legends, to help assist in informa-tion display. For future expectations, the maximal likelihood scoreachievable was adjusted to 90%, to indicate the inherent limita-tions of prediction.

It is recognized that this approach to data display and analysis isnon-quantitative, but it was designed to provide a reasonablyaccurate way to compare the relative usage of ultrasound across

r ultrasound: Expert opinion and review of the literature. Clin Neurophysiol



multiple indications. Similarly, users of clinical rating scalessometimes assign percentages to ordinal data to express relativeseverity of a disorder or relative change with treatment for primar-ily descriptive purposes. The experts were not allowed to discusswith one another or see the results of others’ questionnaires untilafter all the data were collated and only one questionairre wascompleted per laboratory. Also, the experts, while completing thesurvey, were unaware of the intention to compare their responsesto the timing of the published literature. A few items had a fair tolarge number of experts who had not encountered that particularindication (e.g. lepromatous neuropathy), and asterisks in the fig-ures highlight these items.

2.4. Literature review

The review of the literature, for papers cited in the discussion,focused primarily on indications for neuromuscular ultrasound.These were selected based on clinical judgment of their relevanceto the field and the strength of the evidence contained. Once com-piled, the discussion and citations were circulated among theexperts and they were encouraged to provide additional or alter-nate references if they thought they provided equivalent or stron-ger evidence than those chosen, or if they addressed other uniqueaspects of the indication. When available, evidence based reviewswere included. All the expert participants reviewed a draft of themanuscript and provided input at the draft stage and all were inagreement with the final draft of the manuscript.

2.5. Additional analysis of index papers

We were curious to see if there was a relationship between thetiming of particularly informative papers published on specificindications for neuromuscular ultrasound and their application inpractice by this group of experts. For each specific indication fornerve disorders, the literature was searched for the earliest mean-ingful publication, and the frequency of neuromuscular ultrasounduse was correlated with this date. Not all indications had definitivepublications, mostly because certain categories were too non-specific (specifically: palpable masses, phobic patients, variantanatomy, ‘other’ entrapment neuropathies, thoracic outlet syn-drome, and ‘other’ axonal neuropathies.); but of the 30 nerve indi-cations, surveyed, 24 items were specific enough to haveidentifiable single, early influential publications. These were deter-mined first by searching Google Scholar (‘‘sonography” of thespecific indication) and evaluating the top papers listed. The paperthat was earliest, with the highest ranking, and that was suffi-ciently specific (e.g. mentioned the indication in the title or charac-terized findings in a series of patients on that indication) waschosen. This approach identified 18 of the 24 index papers, 12(50%) of which were ranked #1 or #2 in Google Scholar, andanother 6 (25%) of which were ranked between #3–6. This methoddid not identify index papers for the other 6 indications (multipleunrelated papers occupied the top ten citations). Those wereselected by reviewing all papers in PubMed (‘‘sonography of x”)and choosing the earliest descriptive series of patients that waspublished on the topic that was sufficiently specific. One paper isa case report in press because no earlier publications are available.Once collated, the group of experts was given a chance to see ifthere were alternative papers, particularly if from earlier years,that were superior or equivalent to the paper cited. For moredetails, see Appendix. An evaluation of indications for ultrasoundin muscle disorders was not conducted because referrals for pri-mary muscle disease make up only a small fraction of referrals inelectrodiagnostic practice.

Once this data was collected, years since publication of theidentified key indication paper and frequency of ultrasound use

Please cite this article in press as: Walker FO et al. Indications for neuromuscula(2018), https://doi.org/10.1016/j.clinph.2018.09.013

by the expert panel was analyzed to determine if a correlationwas present. We hypothesized that the indications with longerintervals since publication of the index paper would correlate withmore experts using ultrasound for the given indication.

3. Results

3.1. Indications

Experts use ultrasound for a large number of indications themajority of the time (Figs. 1–5). This ranges from about half ofthe time for inflammatory myopathies, to significantly more thanhalf the time for diaphragm paresis, motor neuron disease, chronicinflammatory and hypertrophic neuropathies, suspected masses ortumors, brachial plexopathy, entrapment and traumatic neu-ropathies, unexplainedmuscle atrophy, and those phobic or unableto tolerate electrodiagnostic studies. Of the items queried, cervicalradiculopathy had the least usage, and the technique was used lessthan half the time in common axonal neuropathies, diabetic amy-otrophy, camptocormia, cranial neuropathy, and Guillain Barresyndrome.

Of interest, the association between years since the seminalpublication on an indication and the frequency of use of ultrasoundshowed a moderate correlation with R = 0.56 and robust signifi-cance p = 0.004 (Fig. 6).

3.2. Ultrasound first

Ultrasound first is a catchphrase and approach that refers to theuse of ultrasound as an initial study to facilitate diagnosis. For neu-romuscular ultrasound this sometimes refers to use in the clinic toevaluate patients with complex and undiagnosed muscular dystro-phy to guide the choice of subsequent gene tests (Bönnemannet al., 2014). In this survey, we queried experts regarding the fre-quency with which they have used ultrasound before performingeither EMG or NCS studies for patients referred to their laboratory(Figs. 1–5). We found that at least some of the surveyed expertshave used ultrasound first for virtually all the indications listed,and the majority of experts believe that ultrasound first willbecome routine for a select group of disorders in the future.

3.3. Usefulness of ultrasound components and future expectations forthe field

One participant did not complete this portion of the survey, andseveral participants did not answer one or two of the questions init because they were unsure how to respond. Therefore, each ques-tion in Figs. 7–9 indicates the number of respondents per item andthe distribution of those responses.

The most useful aspects of neuromuscular ultrasound, accord-ing to the experts, are that it helps define anatomy, discovers unex-pected findings, and complements electrodiagnostic testing(Fig. 7). Experts also find modest to moderate added value in theability of ultrasound to assess nerve movement, image real-timeblood flow in nerve and muscle, and display fascicular anatomy.Of available ultrasound instrumentation, the experts find high-resolution transducers and color and power Doppler imaging tobe of considerable benefit in daily practice (Fig. 8). Experts findmoderate benefit from extended field of view ultrasound andquantitative gray scale analysis. Contrast agents, speckle tracking,elastography, and 3-D ultrasound are considered of limited benefitat this time, but it should be noted that these are new technologiesthat are not widely available and have yet to be thoroughly studied(Gasparotti et al., 2017; Goutman et al., 2017; Motomiya et al.,2017; Dikici et al., 2017; Kwon et al., 2014).



Fig. 1. This figure is a summary slide describing expert usage for the indications listed. Although experts graded responses as no cases seen, never, sometimes, often, andalways, the responses were assigned percentages to assist in information display: Never = 0%, Sometimes = 30%, Often = 70%, Always = 100%. The responses were designed toassess current usage, not anticipated future usage. The upper, top dark line represents how frequently they use ultrasound in evaluation of specific indications, the slightlylighter lower line, indicates the frequency with which they use ultrasound first, before other electrodiagnostic studies. NC stands for the number of experts who reportedhaving seen no cases for that indication in their laboratory.

Fig. 2. This figure uses the same display strategies as in Fig. 1 but for different indications. The double asterisk indicates an indication with many experts who have never seena case, and the single asterisk, an indication were a modest number of experts have not seen the indication in their laboratory.


The experts uniformly agree on the high likelihood that morelaboratories will adopt neuromuscular ultrasound, it will becomea key element in training residents and fellows, its role in neuro-muscular research will continue to expand, and the technology willcontinue to improve (Fig. 9). Further, the consensus was stronglypositive for every future application assessed.


4. Discussion

Experts who are already highly skilled in electrodiagnosis useneuromuscular ultrasound frequently for multiple indications.Once adopted for one indication, its usage quickly spreads acrossmultiple indications. The discussion is designed to (A) summarize



Fig. 3. This figure uses the same display strategies outlined in Fig. 1 but for another group of indications.

Fig. 4. This figure uses the same display strategies as outlined in Fig. 1, for a different group of indications.

Fig. 5. This figure uses the same display strategies as outlined in Fig. 1. These indications are labeled as situational, as they are not tied to a specific diagnosis.


Please cite this article in press as: Walker FO et al. Indications for neuromuscular ultrasound: Expert opinion and review of the literature. Clin Neurophysiol(2018), https://doi.org/10.1016/j.clinph.2018.09.013


Fig. 6. This is a scatterplot showing years since publication of the index paper on the y-axis, and the frequency of usage of ultrasound by experts for the related indication onthe x-axis.


the evidence supporting the indications for neuromuscular ultra-sound (Section 5), (B) address the likelihood of the continued evo-lution and value of neuromuscular ultrasound (Section 6) and (C)characterize the translational implications of these findings (Sec-tion 7). The first of these, Section 5, is, by necessity, the longestas it surveys the breadth of existing literature on neuromuscularultrasound (note, less than 1% of the available literature is cited.)

5. The rationale underlying indications for neuromuscularultrasound: A review

This section highlights the published evidence to date on thevariety of indications or the use of neuromuscular ultrasound.Many of the indications are related and most of the pathologicchanges described for nerve and muscle (e.g. muscle atrophy,nerve enlargement, and altered echogenicity) are common to mul-tiple disorders. The selection of citations was designed to help theinterested reader find a few representative papers for each indica-tion; an exhaustive review is beyond the scope of this paper. Thoseengaging in a more in depth search of these topics will find that thenumbers of studies on neuromuscular ultrasound, the absence ofconflicting evidence and the consistency of findings further atteststo its usefulness.

5.1. Generalized muscle disorders:

The first indication ever discovered for neuromuscular ultra-sound was for primary muscle diseases. (Heckmatt andDubowitz, 1980). The Heckmatt grading scale (Heckmatt et al.,1982), which rates echointensity of the muscle and the visibilityof the signal of the subjacent bone into 4 levels, is still used forgrading ultrasound images of muscle involvement in a variety ofmyopathic and neurogenic disorders. Quantitative assessment isalso possible (Scholten et al., 2003). The changes on ultrasound(and on MRI and CT) primarily reflect the gradual atrophy and loss


of healthy myocytes and their replacement by fat and fibrous tis-sue (Reimers et al., 1993a; Pillen et al., 2009). It was noted earlyon that ultrasound was relatively insensitive in distinguishingend stage muscle disease from end stage neurogenic disorders,and that the interpretation of muscle ultrasound often takes placein the context of broader clinical and laboratory assessments.

5.1.1. Inclusion body myositis (52%/16%)The percentages shown are the estimated use frequency from

Figs. 1–5, first showing the usage of ultrasound for the disorder(52%), and second showing the usage of ultrasound first (prior to otherelectrodiagnostic studies) (16%).

Inclusion body myositis is one of the few common muscle dis-orders with a characteristic signature on ultrasound in which theflexor digitorum profundus is significantly more echogenic andatrophic than the adjacent flexor carpi ulnaris. A single ultrasoundimage of these adjacent muscles highlights this striking disparity(Vu and Cartwright 2016, Noto et al., 2014). In the majority of casesa similar disparity has been noted in the lower limb, with increasedechogenicity in the gastrocnemius compared to the soleus muscle(Nodera et al., 2016). In ALS or polymyositis, disorders commonlyconfused with inclusion body myositis, adjacent muscles arealmost always equally involved. It is not known to what extentother less common myopathies may show a pattern similar to thatseen in inclusion body myositis, but this is a topic under activestudy. In affected patients, the distinguishing ultrasound findings,which can be acquired quickly without discomfort, help narrowthe differential diagnosis and limit the number of additional elec-trodiagnostic studies needed to establish a diagnosis.

5.1.2. Other inflammatory myopathies: dermatomyositis (51%/11%)and polymyositis (45%/11%)

In the acute phase, polymyositis and dermatomyositis are char-acterized by normal or increased muscle thickness, sometimeswith evidence of fasciitis manifest as increased fascial thickness,




increased blood flow on color Doppler or reduced echointensity.Tissue enlargement and hypoechogenicity in these disorders mayresult from increased blood flow, which can sometimes be identi-fied with increased power Doppler signal as well (Yoshida et al.,2016, Bhansing et al., 2015, Habers et al., 2015). With chronicity,the muscle becomes more echogenic and atrophy develops withdecreased blood flow (Reimers et al., 1993a; 1993b). Because theclinical examination, muscle biopsy, EMG and serum CK are typi-cally quite informative in polymyositis and dermatomyositis, therole for ultrasound is discretionary. The appearance of subcuta-neous edema (early) and calcification (late) in affected patientscan provide additional helpful information regarding the acutenessor chronicity of the disorder.

5.1.3. Muscular dystrophy (44%/11%)Although neuromuscular ultrasound findings in muscular dys-

trophy can be prominent (Heckmatt and Dubowitz, 1980,Heckmatt et al., 1982), the added value of ultrasound imaging

Fig. 7. This figure demonstrates the self-reported assessment of how much each of theparentheses is the absolute number of responses for each category by the 18 experts: Notthe highest possible score using this grading system would be 90%. Note that one participanswer one or two of the questions because they were unsure as to how to best respon

Fig. 8. This figure demonstrates the self-reported assessment by the experts of how muimaging. In parentheses is the absolute number of responses for each category: None = 0%that the highest possible score would be 90% using this grading system. (See Fig. 7 lege


in the more common muscular dystrophies is modest as diagno-sis can often be made clinically and confirmed with blood tests.Dynamic imaging of dystrophic muscle can also be of value inthat the relaxation time of percussed muscle can be used inthe assessment of myotonia (Abraham et al., 2018). For less com-mon muscular dystrophies, the distribution of imaging findingsamong different muscles can help in the selection of the mostappropriate genetic study (Bönnemann et al., 2014; Zukoskyet al., 2015; Brockman et al., 2007). For example, in Bethlemmyopathy muscle ultrasound reveals increased echointensity inthe center of the rectus femoris (the central shadow sign)(Pillen et al., 2008, Bönnemann et al., 2003). Unlike MRI or CT,which require scheduling and may involve radiation or sedation,ultrasound can be performed at the point of care, speeding upthe evaluation and reducing risk and cost. In patients with onlymild weakness, ultrasound can be used to identify muscles withhigh yield for EMG or biopsy (Heckmatt and Dubowitz, 1987;Lindequist et al., 1990).

aspects of ultrasound imaging contributes to its diagnostic impact in practice. Inat all = 0%, somewhat = 30%, A moderate amount = 70%, a great deal = 90%. Note thatant did not address the survey questions in Figs. 7–9, and a few participants did notd.

ch each of the instrumentation features added to the diagnostic value of ultrasound, very little10%, somewhat30%, a moderate amount = 70%, or a great deal = 90%. Notend for additional details).



Fig. 9. This figure displays the self-reported assessment of how the experts view the future of neuromuscular ultrasound. In parentheses are the numbers of responses foreach of the categories. Unlikely = 10%, possibly likely = 30%, Very likely = 90%. Note that the highest possible score using this grading system would be 90%.(US = neuromuscular ultrasound). (See Fig. 7 legend for additional details.)


5.2. Muscle disorders, localized

5.2.1. Diaphragm paresis (66%/40%)The experts most frequently use muscle ultrasound for the eval-

uation of diaphragm paresis. In large part this relates to the chal-lenges posed by electrodiagnostic study of this muscle. Thediaphragm does not lend itself to belly-tendon electrode place-ment for nerve conduction studies and co-stimulation artifact fromthe brachial plexus can further complicate interpretation. Further,needle electromyography (EMG) of the diaphragm poses a risk ofpneumothorax, which can be life threatening in a patient withpre-existing respiratory dysfunction. Few electrodiagnostic labora-tories routinely perform diaphragm studies.

Ultrasound is sensitive and accurate for diagnosing diaphragmparesis (Boon et al., 2014). It provides a non-invasive view of dia-phragm muscle thickness and echogenicity at rest and with maxi-mal activation, and allows for reliable side-to-side comparison. It issuperior to fluoroscopic evaluation for detecting paresis (Boonet al., 2014). Furthermore, ultrasound is helpful for EMG studiesin that it can be used to guide needle placement or to estimatethe depth and location of the diaphragm, thus substantially reduc-ing the risk of complications (Boon et al., 2008; Harper et al., 2013;Shahgholi et al., 2014). It is a technique which may be used as thefirst and/or only test for assessing diaphragm function in a clinicalneurophysiology laboratory.

Recent papers suggest a role for ultrasound in evaluatingpatients in the intensive care unit prior to extubation and forassessing the potential benefit of diaphragmatic pacing (Zambonet al., 2017; Sklasky et al., 2015). Given the vital importance of dia-phragm function, further ultrasound indications are likely toevolve (Harlaar et al., 2018).

5.2.2. Selective muscle atrophy (61%/30%)Occasionally patients present with unexplained muscle atro-

phy. Ultrasound can quantitate the degree of atrophy, and basedon the echogenicity of the muscle, it can provide informationregarding its chronicity. Ultrasound screening can provide addi-tional useful information regarding involvement of other affectedmuscles as well, often providing insight into its cause. In extremecases of profound atrophy the affected muscle may be electricallysilent, showing neither insertional activity nor motor unit poten-


tials (Walker and Macdonald, 2012). Ultrasound is often used byexperts to evaluate unexplained focal muscle atrophy because ithelps the design of subsequent electrodiagnostic studies and mayfacilitate pattern analysis of additional affected and unaffectedmuscles before performing extensive electromyography. Ultra-sound can also help guide needle placement in an atrophic muscleto ensure that the needle is not inserted into an uninvolved deepermuscle or other vital structure (Boon et al., 2014).

5.2.3. Intramuscular cysticercosis (50%/0%)** (Two asterisks mean thatless than half the experts have seen patients with this indication, oneasterisk means that 6–9 of the experts have not seen it)

This is a rare disorder, and few of the experts have seen caseswhere this disorder was suspected. Ultrasound reveals a cysticstructure in muscle, sometimes also demonstrating a calcified sco-lex (Nagaraju et al., 2015, Kanhere et al., 2015, Chaudhary, 2014),which in the proper clinical setting is highly suggestive of the diag-nosis. Because electrodiagnosis is uninformative in this disorder,neuromuscular ultrasound is of particular value.

5.2.4. Ultrasound guidance of chemodenervation (41%/24%)*

Ultrasound is a proven tool for guiding local anesthetic injec-tions and soft tissue biopsies, so it is not surprising that ultrasoundis also effective for guiding botulinum toxin injections (Alter et al.,2013; Alter and Karp 2017). The impact of ultrasound has beendocumented to result in better outcomes in spasticity and dystoniafor botulinum toxin injections (Picelli et al., 2012, Walter et al.,2018) and when combined with e-stimulation, for phenol injec-tions as well (Matsumoto et al., 2017). Of interest, subspecialistsin PMR, familiar with ultrasound guidance for joint injections,tended to be more likely users of this technique than clinical neu-rophysiologists or neurologists in this survey. Ultrasound guidanceof botulinum toxin also proves helpful in patients who have com-plications from misplaced EMG needle guided injections (Honget al., 2012). Ultrasound can assist in identifying the cricothyroidmembrane or muscle in patients requiring botulinum toxin forvoice disorders and spastic dysphonia (Siddiqui et al., 2015, Yanget al., 2015). For subjects in whom muscle localization is challeng-ing, ultrasound is attractive for injection guidance because it can beused along with EMG needle guidance and electrical stimulation.




5.2.5. Camptocormia (38%24%)Camptocormia refers to a syndrome in which patients have an

unusual bent-spine posture when upright which remits on becom-ing supine. Although rare, it can be seen in association with Parkin-son’s disease or neuromuscular disorders (Ghosh and Milone,2015), its causes are disparate, either resulting from dystonic con-traction of trunk flexors or from a myopathy affecting spine exten-sors (Sakai et al., 2017, Bertram and Colosimo, 2016, Bertram et al.,2015). Ultrasound is helpful in distinguishing these causes as it canidentify hypertrophy of flexor muscles if they are dystonic andatrophy and increased echogencity of extensor muscles if theyare myopathic. Since the myopathy that causes camptocormia isoften atypical, using multiple modes of diagnostic evaluation (i.e.imaging and EMG) is often helpful in confirming its presence andassisting with proper biopsy guidance. Correct diagnosis of dys-tonic camptocormia can help determine if a trial of DBS or botuli-num toxin might be appropriate, treatments that would beunhelpful or pose risks if the disorder is caused by myopathy.

5.3. Nerve disorders

5.3.1. Regional or multifocal (primarily axonal) nerve disorders5.3.1.1. Nerve tumor or neuroma (89%/47%) (Beggs et al., 1999—indexpaper). Although electrodiagnosis can localize pathology to a seg-ment of nerve, it is insensitive for characterizing pathology withinthis segment. Neuromuscular ultrasound is capable of identifyingtumors or neuromas, which may even occur at common entrap-ment sites (Telleman et al., 2017a, 2017b, Zhang et al., 2016,Tahiri et al., 2013, Gruber et al., 2007 Hobson Webb and Walker2004, Beggs et al., 1999). Although not explored in this survey,recent studies have demonstrated the potential usefulness ofintra-operative ultrasound in guiding surgical management ofnerve tumors as well (Simon et al., 2014; Jose et al., 2014). Ultra-sound can help distinguish affected from unaffected fascicles insuch cases, and can also be useful for screening multiloculartumors as seen in neurofibromatosis (Winter et al., 2017;Telleman et al., 2018b, 2017a, 2017b).

5.3.1.2. Nerve torsion (81%/26%)* (Aryanyi et al., 2015—index paper).Of recent interest, has been the reported association of brachialneuritis with nerve torsion, particularly in the radial nerve, whichmay develop acutely or chronically in association with brachialneuritis (Pan et al., 2014; Arányi et al., 2017, 2015; Shi et al.,2018; Samarawickrama et al., 2016a). Ultrasound reveals focalacute constrictions or fascicular entwinement within a nervewhich appear as beading. Although electrodiagnostic studies canidentify severe axonal injury, only imaging studies such as ultra-sound can identify the signature features of this disorder whichmay prompt urgent surgical evaluation.

5.3.1.3. Thoracic outlet syndrome (75%/23%) (no index paper identi-fied). The challenge of establishing a diagnosis and identifyingpatients likely to respond to surgery for thoracic outlet syndromeis well known (Ferrante and Ferrante, 2017; Strakowski, 2013;Simmons, 2013). Ultrasound offers several clues to its presence,including the ability to identify cervical ribs or fibrous bands thatmay impinge on the brachial plexus, and the ability to identifyfocal swelling of nerve trunks or roots (Arányi et al., 2016,Mangrulkar et al., 2008). It also has a unique value for dynamicassessment of potentially compressing muscles, such as the scale-nes and pectoralis minor with provocative clinical maneuvers(Sucher 2012). Although well studied in other disorders of the bra-chial plexus, neuromuscular ultrasound in neurogenic thoracicoutlet syndrome has yet to be systematically studied, in part dueto the lack of a gold standard for its diagnosis.


5.3.1.4. Neurolymphomatosis (73%/33%)** (Vjayan et al., 2015—indexpaper). Cases of neurolymphomatosis have been seen by only afew of the surveyed experts. It may present as either polyneuropa-thy or mononeuropathy with either diffuse of focal enlargement ofnerves (Vijayan et al., 2015). A significant increase in intraneuralblood flow may be seen on power Doppler imaging which facili-tates diagnosis of this rare disorder (Walker and Cartwright 2015).

5.3.1.5. Brachial plexopathy (72%/24%) (Martinoli et al., 2002a—indexpaper). Electrodiagnostic evaluation of plexus lesions is limited inthat short segment motor or sensory nerve conduction studiesare difficult and distal nerve conduction studies and needle EMGare suboptimal for precise localization. In contrast, ultrasoundcan provide exquisite detail of the brachial plexus and its manybranches as well as related structures in the neck that can con-tribute to nerve compression (Martinoli et al., 2002a, Baute et al.,2018). However, the brachial plexus is a challenging area in whichto develop expertise in neuromuscular ultrasound (Somashekar,2016, Smith et al., 2016). MR imaging is an alternative, albeit onewith possibly lower sensitivity and specificity (Zaidman et al.,2013a).

5.3.1.6. Neurofibroma (71%/48%) (Telleman et al., 2017a; 2017b—indexpapers). Recent reports have suggested a potentially promisingrole for identifying and following neurofibromas in patients withneurofibromatosis, tumors which may undergo malignant trans-formation (Telleman et al., 2018b, 2017a, 2017b; Winter et al.,2017). The low cost and ease of use of ultrasound make it idealas a screening tool, but further studies are needed to determinehow it can best be used in managing patients.

5.3.1.7. Lepromatous neuropathy (66%/26%)** (Martinoli et al., 2000—index paper). Few of the experts have seen cases of lepromatousneuropathy as it is rare in their geographic areas of practice. How-ever, ultrasound can be quite helpful in diagnosis with nerveenlargement sometimes most prominent in the ulnar nerve justproximal to the medial epicondyle, often with increased vascular-ity. (Bathala et al., 2017, 2012; Jain et al., 2016; Martinoli. 2000).From a public health perspective, the portability of ultrasounddevices, which can be battery or solar powered, makes them par-ticularly attractive for screening individuals in areas withoutaccess to modern infrastructure who may be at increased risk forleprosy or cysticercosis.

5.3.1.8. Brachial neuritis (63%/21%) (Arányi et al., 2015—indexpaper). Imaging in brachial neuritis has been quite informative.Both by MR and ultrasound, this disorder can cause torsion or mul-tifocal abnormalities in peripheral nerves at multiple levelsthroughout the upper limb (Arányi et al., 2017, 2015; Gruberet al., 2017; Abraham et al., 2016; Lieba-Samal et al., 2016; VanAlfen 2017). In addition, the identification of focal enlargementof limb nerves or individual proximal nerve fascicles by ultrasoundprovides evidence of this disorder. Such findings, in patients withsigns of anterior interosseous (or other focal) neuropathy but witha history suggestive of brachial neuritis, can help avoid the need forsurgical exploration for suspected entrapment. Ultrasound can alsoidentify patients for surgical intervention should they show evi-dence of nerve torsion with distal loss of function.

5.3.1.9. Diabetic amyotrophy (28%/4%) (An et al., 2018—indexpaper). Clinical evaluation and electrodiagnostic testing are usu-ally definitive in diabetic amyotrophy. However, ultrasound canbe of value in evaluating muscle involvement and chronicity. Arecent case suggests that proximal lower limb motor and sensorynerves may show focal changes on ultrasound extending beyondthe expected radiculoplexus distribution, but more studies are




needed (An et al., 2018). The deep location of the lumbosacralplexus makes it inaccessible to routine ultrasound imaging; hereMRI is the preferred technique.

5.3.1.10. Cranial neuropathy (22%/6%) (Cartwright et al., 2009—indexpaper). Cranial neuropathies are an emerging area of investigationby ultrasound in part because of the recent improvements in ultra-sound resolution and in part because of the challenge of evaluatingcranial nerves with electrophysiology (Smith, 2018, Stino andSmith, 2018). Cranial nerves 1, 3, 4, 5, 6, 8, 9 are difficult to visual-ize on ultrasound (Tawfik et al., 2015). The optic nerve is readilyimaged, but caution should be taken to ensure that power settingson the instrument (and use of color flow imaging) are limited toavoid inadvertent injury to the eye. As it is often considered partof the CNS, it is not discussed further in this review (Tawfiket al., 2015). The vagus, if enlarged in AIDP, may be associated withan increased risk of autonomic instability (Grimm et al., 2014a;Knappertz et al., 1998). It also can be enlarged in patients withCMT 1B, and decreased in size in patients with diabetes mellitus(Tawfik et al., 2017, Cartwright et al., 2009). The facial andhypoglossal nerves are visible with ultrasound to some extent(Meng et al., 2016; Tawfik et al., 2015). The spinal accessory nerve,which is vulnerable to minor procedures in the neck, is amenableto imaging, and a recent study suggests that ultrasound is sensitivefor the detection of transection of this nerve (Cesmebasi et al.,2015a; Cesmebasi and Spinner, 2015). At this time expert use ofultrasound for evaluating cranial neuropathies is limited, but withincreasing experience with the technique new indications mayevolve.

5.3.1.11. Cervical radiculopathy (12%/6%) (Kim et al., 2015—indexpaper). A few publications have suggested that ultrasound canidentify nerve enlargement in cervical spinal nerves just as theyexit the neural foramen in radiculopathy (Takeuchi et al., 2017;Metin Ökmen et al., 2018; Kim et al., 2015), but further studiesare needed. Expert use of ultrasound is limited in this area, butexpertise in imaging the spinal nerves in a common disorder suchas cervical radiculopathy could have additional value in helpingelectrodiagnosticians acquire skill in brachial plexus imaging.

5.3.2. Focal nerve disordersUltrasound is helpful in entrapment neuropathies in a variety of

ways. It provides anatomic confirmation of focal neuropathy whichis particularly useful when electrophysiological studies are border-line or non-localizing. It also can identify unexpected anatomiclesions that can cause nerve compression, such as cysts, foreignbodies or tumors, which may be electrodiagnostically indistin-guishable from common entrapment. Ultrasound also providesadditional physiologic information, such as nerve vascularity andmobility that may be of help in evaluating pathophysiologicalmechanisms (Park et al., 2018; Dejaco et al., 2013).

5.3.2.1. Tarsal tunnel syndrome (89%/31%) (Nagaoka et al., 2005—index paper). Some studies suggest electrodiagnostic techniqueshave relatively poor accuracy for identifying tibial neuropathy atthe tarsal tunnel (Doneddu et al., 2017). Ultrasound can be usedto identify anatomic structures in the tarsal tunnel that could pre-dispose to neuropathy such as lipomas, varicosities, ganglion cystsor tenosynovitis. In addition, it provides a direct evaluation of thesize and fascicular anatomy of the tibial nerve (Nagaoka et al.,2005, Tawfik et al., 2016). A recent review concludes that imagingmay be more informative than electrodiagnosis in this disorderlikely accounting for expert interest in the technique (Donedduet al., 2017; Iborra et al., 2018). In one recently reported series,ultrasound was abnormal in all cases of electrophysiologically ver-ified tarsal tunnel syndrome (Samarawickrama et al., 2016b).


5.3.2.2. Fibular neuropathy (88%/29%) (Visser 2006—indexpaper). Fibular neuropathy at the knee provides a compellingrationale for the use of ultrasound for diagnosis because ultra-sound sometimes demonstrates a surgically correctible intraneuralganglion cyst (Spinner et al., 2008). This finding is more common inpatients lacking another cause for the disorder such as leg crossing,squatting or weight loss (Visser 2006, Cartwright andWalker 2013,Visser et al., 2013). Electrophysiological findings alone cannotexclude the presence of such a cyst, and given the higher resolutionof ultrasound than MRI, ultrasound appears more sensitive fortheir detection (Wilson et al., 2017). The common fibular nervecan also be severely injured from knee dislocations and othertrauma in that region. The anatomic correlation provided by ultra-sound in these types of injuries includes nerve stretch, compres-sion from hematoma, transection, projectile penetration ormuscle tear and can assist with proper diagnosis and management(Zywiel et al., 2011, Marciniak 2013, Grant et al., 2015). Ultrasoundcan also help identify variant fibular nerve anatomy that may com-plicate interpretation of nerve conduction studies (Luchetta et al.,2011).

5.3.2.3. Ulnar neuropathy at the elbow (84%/31%) (Beekman et al.,2004—index paper). Ultrasound also provides a particularly usefulassessment of the ulnar nerve at the elbow (Yoon et al., 2010;Yoon et al., 2008; Beekman et al., 2004a). Nerve conduction studiesare less sensitive for diagnosing this disorder than carpal tunnelsyndrome. One complicating factor is subluxation or dislocationof the ulnar nerve over the medial epicondyle with elbow flexionin some individuals. In such cases, the measurement of theexpected course of the ulnar nerve around the elbow over-estimates the true length of the nerve, which leads to a nerve con-duction velocity calculation that may miss true slowing (Childress,1975; Kim et al., 2005, 2008). Recent papers have suggested thatdislocation, in which the nerve completely pivots around the med-ial epicondyle may be protective, whereas, subluxation, where itrises up on the medial epicondyle, but does not dislocate, mayplace the nerve just deep to the skin adjacent to the medial epi-condyle where it is vulnerable to pressure at the elbow (Leiset al., 2017). However, the extent to which subluxation actuallyputs the nerve at risk is debated. (Van Den Berg et al., 2013). Ultra-sound imaging, with a bit of practice, provides a more preciseassessment of this type of nerve movement than palpation, partic-ularly in obese patients or in those who have had previous ulnarnerve surgery. It also can be used to assess the influence of themedial triceps brachii muscles on subluxation and compressionof the nerve (Jacobson et al., 2001).

Reference values for the ulnar nerve show consistency acrossmultiple studies (Fink et al., 2017; Terayama et al., 2018). Of addi-tional interest, ultrasound can help pinpoint the lesion to theretroepicondylar groove (sulcus olecrani), most often seen in deskworkers, or the humeroulnar arcade (cubital tunnel proper) belowthe attachment of the flexor carpi ulnaris muscle just distal to theelbow, more commonly seen in manual workers (Omejec andPodnar, 2016). Ultrasound is effective for detection of anatomicvariations such as an anconeus epitrochlearis muscle that can pre-dispose to nerve compression, particularly in younger individuals(Lee et al., 2016; De Maeseneer et al., 2015). Further, ultrasoundis helpful in identifying ulnar nerve pathology in symptomaticpatients in whom electrodiagnosis is normal (Yoon et al., 2010)and, in conjunction with nerve conduction studies, may also helppredict the results of surgical intervention (Beekman et al.,2004b). Ultrasound also is useful for assessing post-surgical prob-lems, as it can identify undesired positioning of the nerve, exces-sive mobility or subluxation, kinking, persistent focal notchingand post-surgical scarring (Gruber et al., 2015, Duetzmann et al.,




2016). Further investigation of how ultrasound can enhance man-agement and outcomes is needed (Cartwright et al., 2015).

5.3.2.4. Carpal tunnel syndrome (82%/37%) (Buchberger et al., 1991—index paper). Neuromuscular ultrasound is supported by level Arecommendation for the diagnosis of carpal tunnel syndrome(Cartwright et al., 2012). Further, neither NCS nor ultrasound havebeen shown convincingly to be diagnostically superior to oneanother; rather they are essentially of equivalent value. Of interest,up to 25% of false negative ultrasound studies in CTS may resultfrom isolated enlargement of the median nerve in the distal carpaltunnel or palm instead of the wrist, and this should be taken intoaccount in any future studies comparing the two approaches(Paliwal et al., 2014; Csillik et al., 2016). Ultrasound evaluation ofthe median nerve in suspected carpal tunnel syndrome shouldinclude, at a minimum, distal and proximal portions of the nervein the hand; blood flow imaging may also be of benefit (Karahanet al., 2018).

Ultrasound imaging of the median nerve in CTS adds value toNCS in several ways. First, it provides anatomic evidence of focalenlargement that is independent of electrophysiological findings.Second, it provides a structural baseline for subsequent studies,complemting the physiological baseline provided by NCS shouldpatients need to be restudied for treatment failure. For example,ultrasound can identify focal pathology in the recurrent branchof the median nerve a structure sometimes injured during surgery(Smith et al., 2017; Riegler et al., 2017). Third, it sometimes iden-tifies unexpected causes or contributing factors not evident byelectrodiagnosis including tumor, accessory muscles, or thrombo-sis of a persistent median artery (DeFranco et al., 2014; Walkeret al., 2012; Rzpecka-Wejs et al., 2012; Padua et al., 2006). Fourth,it can identify variants, such as Martin-Gruber anastomosis, whichcan complicate interpretation of nerve conduction studies (Gansand van Alfen, 2017); Fifth, ultrasound of carpal tunnel syndrome,the best understood, easiest to image, and most frequently encoun-tered focal neuropathy, helps practitioners hone and maintainultrasound imaging skills in identifying neuromuscular pathology.These include changes in echogenicity and nerve shape thataccompany entrapment, atypical nerve branching, persistent med-ian arteries, anomalous tendon, nerve and muscle anatomy, loss ofnormal nerve sliding and movement relative to the tendons withwrist/finger flexion and extension, increased nerve vascularity,and neurogenic atrophy and hyperechogenicity in muscles inner-vated by the median nerve.

5.3.2.5. Other entrapment neuropathy (81%/29%) (no index paperidentifiable). When relatively uncommon entrapments are sus-pected, most of the experts find ultrasound of benefit in partbecause unexpected anatomic pathology is likely to be more oftenfound in such disorders. Furthermore, in many less common neu-ropathies, short segment nerve conduction studies are not alwayspossible. In such cases, ultrasound could be used to enhance nearnerve studies, should they be desired (Deimel et al., 2013). Patientsanxious to find the cause of their symptoms, particularly if electro-diagnostic studies are negative, are often reassured by ultrasound,even if it too yields negative results. Of note, this survey did notspecifically address the use of ultrasound in meralgia paresthetica,posterior interosseous neuropathy, or other disorders of smallernerves, specific indications for which there is increasing evidenceof its value. (Walker, 2017; Kim et al., 2017; Hung et al., 2016;Moritz et al., 2013; Diemel et al., 2013; Aravindakannan andWilder-Smith, 2012; Kim et al., 2012). Of particular interest is‘‘double crush” syndromes in which ultrasound can rapidly screenfor a second focal neuropathy in a patient with compression at adistal or proximal site of the same nerve (Dietz et al., 2016; Erraet al., 2016; Lee et al., 2016). Also not addressed in this report,


are uses of ultrasound for evaluating bowel and bladder dysfunc-tion an area of active ongoing research (Tagliafico et al., 2014).

5.3.2.6. Traumatic neuropathy (81%/29%) (Cartwright et al., 2007—index paper). Perhaps the most persuasive outcomes evidence forthe use of neuromuscular ultrasound is in suspected traumaticneuropathy (Renna et al., 2012; Chin et al., 2017; Burks et al.,2017; Lauretti et al., 2015). In these cases, ultrasound modifiesthe diagnosis and treatment plan in up to 58% of studies (Paduaet al., 2013, 2012). Discoverable pathology ranges from transection,to scar tissue formation, to bony entrapment of nerves in fracturesor callous. Transection is of particular importance, as electrodiag-nostic studies alone cannot distinguish between transection andacute complete neurapraxia or chronic complete axonotmesis(Bianchi et al., 2014; Walker, 2017; Cartwright et al., 2007). Delay-ing surgery, even by a few weeks, to repair transection results inworse outcomes so the ability to detect transection early is of prog-nostic significance. Furthermore, ultrasound can help identifynerve lesions distant from the trauma site, for example posteriorinterosseous neuropathy may develop in patients with radial nervecompression from humeral fractures (Erra et al., 2016). Finally,ultrasound may help in management and prognostication aftertraumatic neuroma (Coraci et al., 2015). Distinguishing lesionedfrom unlesioned fascicles and extraneural from intraneural scar-ring, fibrosis or hematoma can help guide surgical intervention.Not surprisingly, a majority of the experts frequently use ultra-sound in suspected nerve trauma.

5.4. Generalized primarily demyelinating nerve disorders

5.4.1. Charcot Marie Tooth (CMT) (76%/25%) (Martinoli et al., 2002b—index paper)

Ultrasound demonstrates striking, diffuse, nerve enlargement inCMT type 1, the most common form of hereditary hypertrophicneuropathy. The abnormality is present from a very young age, ismore prominent proximally, and is associated with significantenlargement of individual nerve fascicles (Telleman et al., 2018a;Yiu et al., 2015; Martinoli et al., 2002b). A quick ultrasound scan,even of one or two nerves is highly informative, and can be usedto screen family members of affected patients. Given the harm thatchemotherapy can cause in such patients, a quick and painlessscreening tool for patients suspected of having the disorder is ofvalue. Of note, the absence of profound nerve enlargement doesnot exclude axonal forms of CMT, but nerves may be moderatelyenlarged in these disorders as well (Padua et al., 2018; Schreiberet al., 2013). A recent report also suggests that nerve enlargementmay be seen in children with Dejerine-Sottas disease (Hobbelinket al., 2018), and is prominent in CMT1B (Cartwright et al., 2009).

5.4.2. Chronic inflammatory demyelinating polyneuropathy (CIDP)(83%/19%) and multifocal motor neuropathy (MMN) (76%/19%)(Sugimoto et al., 2013; Zaidman et al., 2013b—index papers for CIDP;Beekman et al., 2005 index paper for MMN)

These two disorders are discussed together because a numberof recent neuromuscular ultrasound papers include both disorders.In both, ultrasound typically demonstrates significant, multifocalnerve enlargement particularly in the proximal median and ulnarnerves and brachial plexus, not always associated with clinical dys-function in the same distribution. Several grading scales and proto-cols for determining abnormality have been proposed (Grimmet al., 2016a; Kerasnoudis et al., 2016; Padua et al., 2014; Janget al., 2014) and perhaps the simplest of these is most attractive(Goedee et al., 2017). Given the risk and expense of treating CIDPand MMNwith steroids, IVIG, or chemotherapeutic agents it makessense to use both imaging and electrophysiology to establish adiagnosis. Furthermore, ultrasound may help differentiate suba-




cute CIDP from persistent acute inflammatory demyelinatingpolyneuropathy (AIDP) (Kerasnoudis et al., 2014). Serial studieswith ultrasound also show some promise for following theresponse of these disorders to treatment (Hartig et al., 2018;Decard et al., 2017; Rattay et al., 2017; Zaidman et al., 2014b,2013b). A majority of experts now routinely use ultrasound inevaluating these complex, problematic and uncommon disorders(Telleman 2018a).

5.4.3. Hereditary neuropathy with liability to pressure palsies (HNPP)(68%/23%) (Beekman et al., 2002—index paper)

Hereditary neuropathy with liability to pressure palsies (HNPP)also demonstrates striking multifocal nerve enlargement by ultra-sound, but unlike CIDP or MMN, the distribution of findings inHNPP is selective to sites of enhanced anatomic vulnerability(Padua et al., 2018).

5.4.4. Guillain Barre syndrome/acute inflammatory demyelinatingpolyneuropathy (AIDP) (54%/9%) (Zaidman et al., 2009—index paper)

Electrophysiologic testing early in GBS shows a number ofspecific and informative findings for diagnosis (Alberti et al.,2011). Of interest, ultrasound may also show changes, even earlyin the disease course or in variant forms, with enlargement inproximal spinal nerves (Berciano et al., 2017, 2014; Mori et al.,2016, Razalli et al., 2016, Grimm et al., 2016b, 2014a, Gallardoet al., 2015). This is of interest, since delayed motor root conduc-tion latencies are also an early finding in this disorder (Temucinand Nurlu 2011). In the future, experts may choose to use ultra-sound more frequently in the evaluation of Guillain Barre Syn-drome if studies show it can inform prognosis.

5.5. Generalized primarily axon/motor neuron loss disorders

5.5.1. Motor neuron disease and amyotrophic lateral sclerosis (ALS)(77%/23%) (Arts et al., 2008—index paper)

Ultrasound is a particularly sensitive tool for detecting fascicu-lations in muscle (Walker et al., 1990). Now that the Awaji criteriainclude fasciculations as part of the diagnostic criteria for amy-otrophic lateral sclerosis (ALS), adding ultrasound to the clinicalexam has proven to be useful for establishing this diagnosis inpatients (Grimm et al., 2015, Boekestein et al., 2012, Misawaet al., 2011, O’gorman et al., 2017). Ultrasound can also be usedto assess the split hand index, using echointensity ratios of the the-nar and hypothenar muscles (Seok et al 2018). For those seekingelectrodiagnostic confirmation of ALS, ultrasound, by identifyingpromising muscles for EMG sampling, can reduce the number ofmuscles that need to be tested for diagnosis (Caress 2017). Of note,recent studies have suggested that fasciculations may be the earli-est manifestation of amyotrophic lateral sclerosis, and, that as thisdisease spreads to uninvolved limbs, fasciculations may be theheralding feature. It is possible therefore, that fasciculations couldalso serve as a biomarker of the disorder (de Carvahalo et al., 2017;Eisen and Vucic, 2013).

Nerve ultrasound in ALS may also be of diagnostic benefitbecause motor nerves tend to be slightly smaller than normal. Thisis likely due to gradual motor axonal loss (Schreiber et al., 2016;Cartwright et al., 2011). Multifocal motor neuropathy (MMN),which can be confused clinically with motor neuron disease, oftenshows enlargement of nerves, and as such, the presence of nerveenlargement may be a useful additional discriminating factor indistinguishing between MMN and ALS (Jongbloed et al., 2016).

Spinal muscular atrophy, a now treatable disorder, also showscharacteristic changes on ultrasound, with hyperechoic, atrophicmuscles and a correspondingly hypertrophic layer of subcutaneousfat. The striking contrast between the hypoechoic fat and hypere-choic muscle provides a useful yardstick for assessing its presence


(Wu et al., 2010). Given that this is a disorder primarily of infantsand children, the availability of a non-invasive tool for its diagno-sis, makes it of particular value. A recent study has suggested thatultrasound detected atrophy and echogenicity may be usefulbiomarkers of SMA progression (Ng et al., 2015).

Ultrasound is also informative in patients who have old orremote polio, in that it shows a striking increase in echogenicity,and often fasciculations, in muscles that were once affected bythe disorder (Walker et al., 1990).

5.5.2. Non-diabetic axonal polyneuropathy (32%/4%); diabeticpolyneuropathy (27%/7%); toxic neuropathy (17%/8%) (Other-non-diabetic polyneuropathy—no index paper identifiable; diabeticpolyneuropathy Severenson et al., 2007—index paper; toxic polyneu-ropathy Briani et al., 2013—index paper).

Experts find relatively limited usefulness for ultrasound in dia-betic and axonal neuropathies (Telleman et al., 2018a). Recent pub-lications have shown mild generalized enlargement of nerves indiabetic neuropathy, and occasional enlargement of nerves in sometoxic neuropathies (Breiner et al., 2017; Stone et al., 2014; Brianiet al., 2013). The few reports on neuromuscular ultrasound in zos-ter neuropathy, vasculitic neuropathy, and trans-thyretin amyloi-dosis suggest it may have a helpful role (Podner et al., 2017;Nodera et al., 2006; Zubair et al., 2017; Salvalaggio et al., 2017).For example, in suspected vasculitic neuropathy, ultrasound mayhelp in selection of affected nerve segments for biopsy (Grimmet al., 2014b). Further investigation of these and other predomi-nantly axonal neuropathies (e.g. HIV neuropathy, for which ultra-sound findings have not been reported) may identify specificpatterns of nerve changes apparent by ultrasound.

5.5.3. Sensory neuronopathy (22%/6%) (Pelosi et al., 2017—indexpaper)

While nerves typically enlarge and become hypoechoic in mostneuropathies (Walker 2017), recent studies have shown that insome sensory neuronopathies, particularly cerebellar ataxia, neu-ropathy, vestibular areflexia syndrome (CANVAS), nerve thinningcan be seen (Pelosi et al., 2018, 2017). Ultrasound in Friedereich’sataxia, another, somewhat more complicated and possibly mixedform of sensory neuronopathy, shows that some nerves may showenlargement in this disorder, so additional work is needed (Mulroyet al., 2017). In Wartenberg’s migrant sensory neuritis, an idio-pathic, patchy, pure sensory neuropathy ultrasound reveals diffusemultifocal nerve enlargement which includes pure sensory andmixed nerves (Herraets et al., 2017). At this time, most expertsare not routinely using ultrasound to evaluate pure sensory disor-ders, but further investigation seems promising.

5.6. Situational indications:

5.6.1. Palpable masses (86%/47%)It is not uncommon for patients to describe palpable lumps or

bumps during an electrodiagnostic evaluation. Ultrasound is quitehelpful in these cases. It can demonstrate to the patient that noth-ing is apparent by ultrasound which can be quite reassuring; alter-natively, it can identify lesions which sometimes are not apparentby clinical examination. Common palpable findings include benignenlarged lymph nodes, lipomas and ganglion cysts. However ultra-sound can identify a wide variety of other pathologic changesincluding scar tissue, neuromas, tumors, calcifications, aneurysms,arteritis, aberrant muscles or tendons, musculoskeletal disordersand bony malformations. The sonoacoustic properties of unex-pected peripheral masses may also be useful in discriminatingbetween various peripheral nerve associated tumors and changeson color Doppler may even help in the diagnosis temporal arteritis(Ryu et al., 2015, Nescher et al., 2002). The neuromuscular sonog-




rapher, even if not sure about the exact nature of the change, canoften determine if it is causing focal compression of nerve or mus-cle and describe it in a manner that helps the referring physiciandecide if further imaging (e.g. MR) is warranted (DiDomenicoet al., 2014). A recent report suggests that extra-neural findingsare not uncommon in routine neuromuscular ultrasound examina-tions (Bignotti et al., 2018).

5.6.2. Variant anatomy (76%/34%)Variant anatomy can sometimes be anticipated, for example, in

patientswith congenitalmalformations, severe trauma, orwhohaveundergone reconstructive surgery or nerve transposition. In others,anatomic variation is discovered during their laboratory evaluation.In either case, ultrasound can be of value in helping to guide EMGand NCS studies for nerves or muscles in unusual locations and forevaluating pathology secondary to the variant anatomy (Zhu et al.,2011; Erra et al., 2013; Enhesari et al., 2014; Cesmebasi et al.,2015b; Gans et al., 2017; Grigoriu et al., 2015). For example, persis-tent median arteries can thrombose causing acute symptoms sug-gestive of carpal tunnel syndrome or nerves can be entrapped ininstrumentation used to secure displaced fractures (Walker et al.,2013; Peer et al., 2001). Identifying variant anatomy also may helpguide interventions around vital structures. Ultrasound can also beused to identify anatomic variants suggested by unusual NCS find-ings such asMartin-Gruber anastomoses or accessory fibular nerves(Gans and van Alfen, 2017; Luchetta et al., 2011).

5.6.3. Phobic patients or patients unable to tolerate electrodiagnosis(67%/67%)

A small percentage of patients referred for electrodiagnostic test-ing are unable to tolerate the procedure. Small children and infantspresent special challenges in this regard and an unknown numberare never referred for testing even when it might be appropriate.At the request of the parents, sedation is sometimes used whichhas other risks and drawbacks. As a third component of the neurodi-agnostic evaluation, ultrasound offers an intermediate step in theevaluation of such individuals. It assesses nerves and muscles in apatient friendly manner, which in itself, may be sufficient for diag-nosis in some disorders or suitably informative to obviate the needfor EMG or nerve conduction studies. For example, there is evidencethat ultrasound, by assessing the echointensity ratio of differentiallyinnervated muscles, may be helpful in quantitating the extent ofaxonal loss in distal hand muscles without the discomfort of EMG(Kim et al., 2016). Sometimes, after performing an ultrasound,enough trust is built with the examiner to allow for limited addi-tional electrodiagnostic studies. Ultrasound may also help in deter-mining if there is a need for other types of testing.

6. The value of neuromuscular ultrasound and the likelihood ofits continued evolution:

6.1. Validity and limitations of the expert survey

This study has several limitations. It should be reiterated thatthe self-reporting component regarding expert usage is non-quantitative and the translation of terms such as ‘sometimes, oftenand frequent’ can vary across different individuals. It is further pos-sible that participant enthusiasm for ultrasound may have biasedthe results. Hidden bias in a survey of this type cannot be com-pletely excluded, although a number of steps were taken to avoidor minimize it. The geographic and specialty representation amongthe experts is well balanced and there was, reassuringly, a consen-sus among the experts on the selection of representative publica-tions cited in this report. The survey involves self-reporting andrecall instead of a monitored retrospective analysis of all studies


performed, and it is possible that inaccuracies resulted from thisapproach; however, given the variation in responses from partici-pant to participant, and significant variations in practice suggestthat there was no universal trend in over or underreporting ultra-sound usage. It should be noted, however, that the overall relation-ship between the publication date of evidence and the actual usageof ultrasound (Fig. 6) suggests that expert practice is responsive tothe published literature and thus, less likely to be reflective ofinternal or systematic bias.

Another limitation of the manuscript is that it does not addressthe skill level required to perform neuromuscular ultrasound, northe requisite sophistication of ultrasound equipment to address cer-tain conditions. Similarly, appropriate requirements for instrumen-tation for each indication have yet to be defined, but this reflects theevolving nature and standardization of ultrasound devices. The timerequired for physicians in electrodiagnostic practice to acquireexpert ultrasound imaging and interpretation skills is unknownbecause many of the experts learned ultrasound through the ineffi-cient process of trial and error. However, the degree to whichthoughtful instruction can speed up learning is significant in thatreliable large muscle ultrasound measurement skills can beacquired with less than one hour’s training, and reliable upperextremitynerve imaging skills can be acquired in twomonths of res-idency training in an electrodiagnostic laboratory with ultrasoundequipment (Zaidman et al., 2014a, Garcia-Santibanez et al., 2018).

Other possible limitations of neuromuscular ultrasound unad-dressed in this manuscript include the overlap in presentation ofmusculoskeletal (MSK) disorders with neuromuscular disorders.Not all physicians skilled in neuromuscular ultrasound can evalu-ate for MSK disorders. It is also possible that ultrasound could con-tribute to the costs of neurodiagnostic evaluations. However, onceexpertise in neuromuscular ultrasound and an instrument areacquired, the marginal cost of ultrasound is quite modest. An anal-ysis of the cost of ultrasound in practice is beyond the scope of thisreview, but preliminary work suggests ultrasound is cost-effective(Cartwright et al., 2015).

6.2. Is there reason to expect that MRI will supersede ultrasound as acomplementary routine test for neuromuscular evaluation?

The experts were not specifically asked this question, but theinvestment in ultrasound and optimism for its future clearly indi-cates that this is not felt to be likely. To date, for the few publishedcomparisons of MRI with neuromuscular ultrasound, ultrasoundhas proven to be an equal or somewhat superior diagnostic tech-nique (Bignotti et al., 2017; Smith et al., 2016; Jannsen et al.,2014; Zaidman et al., 2013a; Gabmarota et al., 2007). This is notsurprising as ultrasound has significantly better resolution thanMRI (Cartwright et al., 2017, Gambarota et al., 2007), and the com-puter driven technology that has contributed to improved MR res-olution over the last few decades is similar to the technology thatcontinues to improve ultrasound resolution. The lower cost, porta-bility, and availability without scheduling of ultrasound are fixedadvantages of the technique. Nonetheless, MRI offers specificadvantages including contrast enhancement, tractography andaccess to nerves throughout the body—information unavailablethrough ultrasound making MRI a valuable tool for research, vali-dation of ultrasound findings and direct evaluation of patients. Ofnote, ultrasound and MRI measurements of nerve size correlatequite well (Pitarokoili et al., 2018).

6.3. Relative growth of electrodiagnostic and ultrasound imagingtechnology

Although ultrasound and electrodiagnosis both evolved fromoscilloscope technology (Walker, 2007), electrodiagnostic technol-




ogy is in an evolutionary plateau at this time and is relativelyunchanged in the last few decades. Motor unit quantitation hasimproved with newer programs, but the impact of computerizedEMG analysis has been, at best, modest. In contrast, ultrasoundhas evolved considerably and this survey shows a unanimousexpert consensus as to continued improvements in ultrasoundtechnology. Furthermore, instrumentation is becoming moreadaptable, with remarkable miniaturization of some ultrasounddevices, some now the size of a cellular telephone. Image resolu-tion continues to improve with modifications in transducers andsignal analysis, and over the last few decades, the entry level costof an effective instrument has dropped considerably. Currently, atleast two companies have developed combined ultrasound/EMGinstruments that can simultaneously display ultrasound and EMGdata. Standard options on ultrasound instruments have alsoincreased, with extended field of view, 3-D and 4-D imaging, elas-tography, and other advanced programs becoming more availableon smaller instruments. Ultra-high frequency transducers havebeen developed that offer unprecedented visualization of superifi-cal peripheral nerves and surrounding structures (Cartwright et al.,2017). Training in neuromuscular ultrasound is now much morewidespread than a decade ago. The evolution of ultrasound isaccelerating and recognition of this trend has led to training med-ical students and residents in clinical applications of ultrasound,and in a few countries, neuromuscular ultrasound certification pro-grams are active or in development. There is also rapidly growinginterest in the use of ultrasound guidance for enhancing existingtechniques such as steroid injections, diagnostic anesthetic blocksand pre-operative localization of nerves, as well as in the develop-ment of new techniques such as needle fenestration for carpal tun-nel syndrome, hydrodissection of entrapped nerves andregenerative procedures (Hanna et al., 2017, Tudose et al., 2017,Cass, 2016, Strakowski, 2016, Tagliafico et al., 2016, McShaneet al., 2012). Expertise with ultrasound is a prerequisite forwould-be innovators in these areas and for those testing the clini-cal value of new approaches.

6.4. Added value of instrumentation and ultrasound in practice

The majority of the focus of neuromuscular ultrasound over thelast few decades has been on resolving the anatomy of nerves,muscles, blood vessels and the surrounding tissues (Figs. 7 and8). Experts have thus placed the highest value, in their currentequipment, on the high resolution transducers and color flowimaging—the features most helpful for assessing anatomy, comple-menting electrodiagnostic findings, and in identifying unexpectedpathology. Quantitative gray scale analysis and extended field ofview, techniques which can further assist in anatomic resolutionare rated next most helpful. Contrast agents, speckle tracking, elas-tography and 3D ultrasound are more recent innovations in ultra-sound technology that have been the subject of relatively fewpublications, and not all experts have access to these innovations.Understandably, they are rated less important at this time, as thepotential usefulness of these technologies has not been fullyexplored. Given the added time required to use these techniquesand the greater complexity involved in assessing physiology com-pared to anatomy (e.g. changes in anatomy over time), it can beassumed that their integration into routine practice will takelonger than the immediate benefits of high-resolution transducersand blood flow assessment.

6.5. Future expectations for neuromuscular ultrasound

The most compelling results of the survey relate to the unanim-ity of opinion by experts on the continued expansion for indica-tions and use of neuromuscular ultrasound in the future. None of


the experts foresee curtailment of their use of the technologyand all foresee a high likelihood for more indications, better qualityinstruments, more research, and better diagnosis. All see it as apart of routine clinical neurophysiology training and practice inthe future. Also, given the increasing use of ultrasound in medicalschools, it seems likely that prospective residents and fellows willexpect training programs to be able to instruct them in neuromus-cular ultrasound. Point of care ultrasound is becoming an integralpart of many medical specialties as well. The experts are optimisticabout increasing pediatric indications for neuromuscular ultra-sound and the use of ultrasound first for certain indications. Theonly area where there is significantly less agreement by expertsis the likelihood of lower cost- ultrasound instruments.

6.6. The nature of the current evidence

The rate of discovery of new indications for neuromuscular ultra-sound, the endurance of previously discovered indications, the con-tinued evolution of instrumentation, its non-invasiveness, and thegrowing use of ultrasound for different neuromuscular disordersby experts in electrodiagnostic medicine makes a compelling casefor imaging in clinical neurophysiology laboratories. We encouragerigorous attention to design in future studies of neuromuscularultrasound to help facilitate its acceptance by those outside the fieldof electrodiagnosis. Similarly, readers interested in formal levels ofevidence are encouraged to explore the literature and report theirfindings. However, for those readers who practice electrodiagnosisand who wish to form an independent opinion on the usefulnessof neuromuscular ultrasound, we suggest that they borrow aninstrument and simply look for themselves.

7. Translational implications

For decades, electrodiagnostic medicine has been based on afairly equal assignment of importance to EMG and NCS in the eval-uation of patients referred for a neuromuscular evaluation. This isbecause the need for one or both procedures cannot be determineduntil an expert in the laboratory sees the patient and initial testresults are available. A laboratory that only performed one of thesetests would be of limited value.

Neuromuscular ultrasound has now become, in addition to EMGand NCS, a third component of a neurodiagnostic evaluation. This isbecause the need for any combination of EMG, NCS or ultrasoundcannot be determined until an expert sees the patient and somepreliminary test results are available (Tables 1 and 2). What makesthe interplay of the three studies of interest is that some informa-tion provided by EMG and NCS cannot be replicated by ultrasoundincluding selective motor versus sensory impairment in the samenerve, sensory localization with respect to the dorsal root ganglion,and some aspects of prognosis and severity. On the other hand,ultrasound diagnoses common entrapment neuropathies with anaccuracy comparable to that of electrodiagnosis, localizes othernerve problems when NCS alone cannot (e.g. when responses areabsent, when inching is not possible, or when nerve dysfunctionis not severe enough to be detected electrically). Furthermore,ultrasound provides information beyond localization unavailableby EMG or NCS regarding the presence or absence of intrinsic orextrinsic nerve pathology (e.g. tumors, cysts etc.) or chronic muscledisease and it provides this information quickly, safely, and with-out discomfort.

7.1. Re-envisioning electrodiagnosis

Fifty year ago, the approach in an electrodiagnostic laboratorywas to perform all possibly helpful diagnostic studies at the initial



Table 1Added value of ultrasound in focal neuropathy.

(A) Suspected focal neuropathy already localized by electrodiagnosis (EDX)1. Confirms or further refines localization (e.g. in long segments, such as median nerve in the forearm).2. Excludes unexpected intrinsic or extrinsic anatomic pathology (e.g. ganglion cyst in fibular neuropathy at the knee, or focal nerve tumor/neuroma).3. May be used to exclude a second entrapment of the nerve at a distal or proximal site (e.g. double crush).4. Identification of nerve torsion (brachial neuritis).5. Establishment of anatomic baseline for future comparison in anticipation of medical or surgical treatment.6. Muscle ultrasound, by using echointensity ratios, may provide insight into relative axonal loss in distal muscles.7. Helps identify variant nerve anatomy that complicates interpretation of nerve conduction studies (Martin-Gruber or accessory fibular nerve).

(B) Suspected focal neuropathy unable to be further localized by EDX (absent motor/sensory responses)1. Localizes the lesion to a specific site along the nerve.2. In the presence of trauma, confirms nerve continuity or identifies transection and assesses for hematoma, bone injury, or other contributing factors.

(C) Suspected focal neuropathy with borderline EDX1. Can help support or refute the presence of focal nerve pathology.

(D) Suspected focal neuropathy with normal EDX1. May identify focal nerve pathology not apparent by EDX, or present in nerve branches not suitable for EDX testing.2. May identify dislocation of the ulnar nerve with elbow flexion, which may account for false negative NCS findings.3. May identify a proximal fascicular lesion masquerading as a distal entrapment as in brachial neuritis.

Table 2Added value in other neuromuscular disorders.

(A) Suspected polyneuropathy (before or after EDX)1. Helps support or refute the presence of hypertrophic polyneuropathies (CMT, MMN, CIDP, HNPP, and AIDP).2. Distinguishes CMT and HNPP from CIDP and MMN.3. Increased power Doppler signal may identify lepromatous neuropathy or neurolymphomatosis.4. Evaluates distal muscle atrophy/increased echogenicity indicative of a chronic neurogenic process.5. Demonstrates nerve thinning in CANVAS or enlargement in Wartenberg’s migrant sensory neuritis.

(B) Suspected motor neuron disease: prior to EMG1. Identification of fasciculations to help diagnose ALS using modified Awaji criteria, or to enhance muscle selection for EMG examination.2. Distinction, based on location, size and frequency, of benign from pathological fasciculations.3. May provide evidence, using relative muscle echointensity and thickness, of split-hand syndrome which may be seen in ALS.4. The absence of enlarged nerves (and the presence of slightly smaller nerves) may help distinguish motor neuron disease from MMN.

(C) Suspected muscle disorder prior to EMG1. Provide a rapid screen for inclusion body myositis.2. Identifies muscles involved in unexplained myopathy or camptocormia, aiding clinical diagnosis.3. Identifies calcification and/or cysts indicative of prior inflammation, hemorrhage or infection.4. Identifies muscles most suitable for EMG or biopsy, particularly in mild or severe myopathies.5. Evaluates diaphragm function and provides guidance, if needed, for EMG needle insertion.6. Quantitative muscle ultrasound may help distinguish central and peripheral etiologies in infants and small children, and helps guide choice of further testing.

(D) Other1. Evaluates nerve and muscle in those unable to tolerate EDX.2. Assesses variant anatomy from surgery, trauma, or congenital anomalies.3. May be used to guide chemodenervation, steroid injections, near nerve needle placement, or phenol injections, or nerve biopsy.4. May be used to map the course of nerves (e.g. spinal accessory) prior to surgical intervention to prevent injury.

Abbreviations, CMT = Charcot Marie Tooth, MMN (Multifocal motor neuropathy), CIDP = chronic inflammatory demyelinating polyneuropathy, HNPP = Hereditary neu-ropathy with liability to pressure palsy, AIDP = acute inflammatory demyelinating polyneuropathy. CANVAS = cerebellar ataxia, neuropathy, vestibular areflexia syndrome).EMG = electromyography.


encounter because patients were often reluctant to return andbecause, at that time, alternative studies of the peripheral nervoussystem were typically invasive and not always informative. Sincethen, testing alternatives have evolved. Instead of spinal myelogra-phy to rule out radiculopathy, patients may now undergo an MRI,instead of nerve biopsy to evaluate small fiber pathology, patientsmay now undergo a skin biopsy, instead of muscle biopsy to fur-ther evaluate a myopathy, patients may now undergo a wide vari-ety of genetic and antibody tests. Over this time period, theapproach to diagnosis in a patient with suspected neuromusculardisorders has thus shifted away from conducting all possibly help-ful studies to conducting those that are least invasive and mostuseful for guiding patient care. As discussed above and as shownin Tables 1 and 2, neuromuscular ultrasound is instrumental in thisregard, painlessly adding information that is otherwise unobtain-able. The inclusion of neuromuscular ultrasound with EMG andNCS across testing centers will eventually lead practitioners todevelop protocols for sequencing these three types of studies to


optimize clinical helpfulness and diagnostic yield (Te Riele et al.2017).

Those interested in staying current in clinical neurophysiologyneed to first acquire a high-resolution ultrasound device and thendevelop skill in its use. At this time, many laboratories do not haveaccess to ultrasound; for example, in Canada at this time there arefewer than 10 centers in the country with ultrasound access. This isno longer tenable and it is the responsibility of hospitals and aca-demic medical centers to promptly address this issue. The secondstep does not require immediate mastery of all potential applica-tions, but rather, it need only begin with one individual masteringone indication along with one nerve segment and relevant mus-cles. Once this is done, the technique can gradually spread to morenerve segments, muscles, indications and members in a laboratory.For each of the experts surveyed, the technique was mastered onenerve, one muscle, and one indication at a time, and now, there areample courses and literature to guide newcomers to acquire exper-tise relatively quickly. The gap in best practices between experts




and most practitioners in the field of peripheral clinical neurophys-iology hinders optimal care and the advancement of the field.Acquiring an ultrasound instrument and the skills needed to useit must be a top priority for all electrodiagnostic laboratories.

Funding

This research did not receive any specific grant from fundingagencies in the public, commercial, or not for profit sectors.

Declarations of interest

None.

Appendix A. Supplementary material

Supplementary data to this article can be found online athttps://doi.org/10.1016/j.clinph.2018.09.013.

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