Ultrasound in Neuromuscular Medicine

Introduction

Neuromuscular ultrasound (NMUS) continues emerging as an accessible effective adjunct to conventional electrodiagnostics. Use of NMUS adds helpful information to the diagnostic picture and can affect management.¹

The unique benefits of NMUS include point-of-care dynamic imaging of muscle and nerve, supplemental information including vascularity and mobility of structures, muscle and nerve measurements, superior spatial resolution, and visual guidance for procedures. The advantages of NMUS are that there is little to no discomfort, which is particularly relevant for pediatric cases, and limited expense for the patient. A multidisciplinary team including surgeons, neurologists, physiatrists, and primary care physicians may specifically request NMUS.

Frequently implemented in muscle disease and entrapment neuropathies, NMUS use is broadening because studies are creating reliable protocols for other areas of neuromuscular disease (NMD). For example, recent well-delineated NMUS protocols for evaluating scapular winging, diaphragm weakness, and brachial plexus pathology have been published.^2-4 In this article, we review current uses of NMUS for muscle disease and peripheral neuropathies and explore future directions.

Muscle Ultrasound

Muscle imaging was among the first uses of NMUS and continues to expand with applications for muscular dystrophies, myopathies, motor neuron disease, and other muscle disorders. Ultrasound of normal skeletal muscle has a heterogeneous appearance that is fairly hypoechoic (dark) interspersed with hyperechoic (bright) areas, representing the normal fibrous connective tissue within the muscle. In the transverse plane, there is a “starry-sky” appearance because these fibrous structures are viewed in cross-section against the darker background of muscle fibers (Figure 1A). In the longitudinal plane, the bright fibrous structures run lengthwise, streaking across the darker muscle fibers (Figure 1B).

Muscle disease can present a diagnostic challenge in clinical practice because of clinical confounders, patchy distribution of pathology, absence of lab abnormalities, and poor tolerance of EMG testing. Pathologic patterns on ultrasound imaging of muscle may complement a thorough history and physical examination for evaluating myopathic processes. Ultrasound can also increase diagnostic yield by identifying involved muscles. When muscle biopsy is needed, NMUS provides useful guidance when patchy involvement could otherwise lead to a suboptimal nondiagnostic muscle sample.

Muscular Dystrophies and Myopathies

Characteristic ultrasound findings of muscular dystrophies include loss of normal heterogeneous appearance as muscle is replaced by fatty fibrous tissue in affected muscles. Dystrophic muscles take on a bright, homogenous appearance.⁵ Deep tissue reflections are lost or attenuated in severely affected dystrophic muscles. Similar changes of increased echogenicity may be seen in acute inflammatory myopathies, but in contrast to muscular dystrophies, there are often preserved deep-tissue reflections (Figure 1C).⁶

Distribution of abnormal imaging findings may identify a specific NMD. For example, inclusion body myositis often shows increased echogenicity of the flexor digitorum profundus with relative sparing of the flexor carpi ulnaris.⁷ Facioscapulohumeral muscular dystrophy may show preferential involvement of the distal thigh muscles.⁸ Start by imaging muscles that are easily accessible and clinically weak in both transverse and sagittal planes. Frequently examined muscles include the tibialis anterior and vastus lateralis in the lower extremity and the biceps and deltoid in the upper extremity.

Diaphragmatic Ultrasound

Another innovative use of NMUS is evaluation of diaphragm paralysis. This is especially relevant because of safety concerns in needle EMG of the diaphragmatic musculature. Diaphragm thickness and change in thickness during the respiratory cycle can be accurately assessed and compared side to side. A practical approach to imaging the diaphragm can be efficiently implemented in the EMG lab or in the intensive care unit (ICU).³

Motor Neuron Disease

Although, by definition, motor neuron disease is not primarily a muscle pathology, downstream effects of lower motor neuron dysfunction are seen in muscle. The ability to capture and video record dynamic movements (eg, fasciculations) is more sensitive with USNM vs EMG.⁹ The person being testedcan be asked if they feel twitching in a particular area, and the ultrasound probe can be placed on that muscle to observe both fasciculations and muscle appearance. Muscle thickness measurements (using very light pressure on the probe and an anatomical landmark) may be decreased in NMD when compared with normal values or side-to-side comparison.¹⁰

Echogenicity, vascularity, and anisotropy (variability of echointensity when angle of the ultrasound probe is changed) can also be evaluated with NMUS. In end-stage amyotrophic lateral sclerosis (ALS), the affected muscle appears “moth eaten” because of increased echogenicity in denervated areas intermixed with hypoechoic patchy areas of preserved motor units. Importantly, this finding is not specific for ALS and may be seen in the muscle with other neurogenic disorders.⁶

Peripheral Nerve Ultrasound

First used in assessment of carpal tunnel syndrome (still the most common use of NMUS), NMUS is easy to use and diagnostic for many forms of nerve pathology. The sonographic appearance of a normal peripheral nerve consists of discrete “honeycomb-like” fascicles encased by a relatively hyperechoic epineurium (Figure 2). Cross-sectional area (CSA) is measured by placing the ultrasound probe perpendicular to the nerve at the site of maximal enlargement just proximal to the site of suspected entrapment. The CSA measurements are easy to make and have low interobserver variability even when made on different ultrasound devices.¹¹ Other measurements including echogenicity, vascularity, and mobility are also recorded.

Entrapment Neuropathies

The most implemented and practical use of peripheral nerve ultrasound is evaluation for entrapment neuropathies of the median, ulnar, and fibular nerves, respectively. Well-established ultrasound techniques for these entrapments can be easily studied and practiced in a short period of time.¹² A diseased nerve has changes in cross-sectional area (increased) and echogenicity (decreased) over time. There may also be changes in vascularity on power doppler ultrasound (increased) caused by local inflammation and injury, and site-specific changes in nerve mobility (decreased in median neuropathy at the wrist, increased in the case of nerve subluxation/dislocation in ulnar neuropathy at the elbow). Use the “ascending elevator” technique to evaluate the entire nerve, scanning in the axial plane distally to proximally, looking for focal changes along or outside typical entrapment locations. Assess pathologic areas in the longitudinal plane as well, taking CSA measurements at the entrapment site and sites immediately distal and proximal so comparisons can be made. Use of NMUS for less common entrapment neuropathy syndromes including pronator teres syndrome, anterior osseous nerve (AIN) syndrome, posterior interosseous nerve (PIN) syndrome, and traumatic neuropathy have also been described.^12,13

Acquired Polyneuropathies

Ultrasound findings in chronic inflammatory demyelinating polyneuropathy (CIDP) have recently been the focus of tremendous interest. Findings include multifocal nerve enlargement in noncompressible sites and regional or segmental enlargement in the proximal segments of the median nerve, ulnar nerve and brachial plexus.¹⁴ Enlargement in these areas on NMUS in addition to variability in fascicular size and echogenicity may aid in differentiating demyelinating from axonal neuropathies.^15,16 In multifocal motor neuropathy (MMN), there may be multifocal enlargements in the brachial plexus, median, ulnar or radial nerves, but these have not been shown to necessarily correlate with electrodiagnostic findings such as conduction block.¹⁷ In cases phenotypically consistent with CIDP or MMN for which electrodiagnostics have not shown evidence of demyelination, NMUS may identify nerve enlargement.¹⁸ The presence of multifocal ulnar and median nerve enlargement can help differentiate MMN from ALS, which significantly alters disease management.¹⁹

Other acquired axonal polyneuropathies (eg, idiopathic or diabetic polyneuropathy) show either normal cross-sectional area or only mild enlargement compared with healthy controls, and these abnormalities may be less apparent on an individual basis.²⁰

We recommend using an “elevator technique” as described previously, including evaluation along the entire course of the median and ulnar nerves. If significant variability in nerve size is seen, measurements should be taken at multiple areas, including those of maximal and minimal cross-sectional area, making note of changes in echogenicity, vascularity, and fascicular structure. As stated previously, the proximal segments of these nerves and brachial plexus are of particular interest.¹⁵

Hereditary Polyneuropathies

The most characteristic finding in hereditary neuropathy (HN), such as Charcot-Marie-Tooth (CMT) disease is diffuse nerve enlargement along the entire course of an affected nerve. This is in contrast to the segmental enlargement seen in CIDP or focal enlargement seen with entrapment neuropathy. The diffuse pattern of nerve enlargement seen in HN tends to be more pronounced in demyelinating forms of CMT, but both demyelinating and axonal forms have been shown to result in nerve enlargement when compared to healthy controls.^14,20 When CMT is suspected clinically or electrodiagnostically, we recommend distal-to-proximal evaluation of selected affected nerves in the upper and/or lower extremities, with evaluation of CSA at multiple sites to determine the pattern of enlargement.

Conclusion

There are numerous well-described and established roles for NMUS in neuromuscular medicine, making this imaging modality highly useful and an integrated complement to history, physical exam, and electrodiagnostic testing. In addition to the uses discussed, NMUS may also be used to guide accurate injections/localization for lumbar punctures, occipital nerve blocks, botulinum toxin treatment, and other musculoskeletal procedures.

Additional innovative and practical uses for NMUS are being described and developed at a rapid pace. Examples of budding applications include the use of ultrahigh-resolution ultrasound (See Case), elastography,²¹ automation, and the use of contrast for imaging discrete superficial nerves and anatomic areas that are difficult to visualize with conventional ultrasound. Cranial nerve ultrasound of the optic, facial, vagus, spinal accessory, and hypoglossal nerve is a burgeoning area that may inform both focal pathology and broader NMD such as intracranial hypertension, optic neuritis, Bell’s palsy, Guillain Barré syndrome, CIDP, and CMT.^{23, 24}