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Diagnostic ultrasound in neuromuscular disease

Diagnostic ultrasound in neuromuscular disease
Literature review current through: Jan 2024.
This topic last updated: Jun 20, 2022.

INTRODUCTION — Neuromuscular ultrasound is a diagnostic tool for nerve and muscle diseases that provides real-time anatomic and physiologic information. It is typically used in conjunction with standard diagnostic tests such as electromyography, nerve conduction studies, and tissue biopsy. It is a point-of-care technology that allows for the study of muscle contraction, fasciculations, and nerve and tendon movement.

This topic will review the use of ultrasound for the evaluation of neuromuscular disease. Electrodiagnostic methods for neuromuscular disease are discussed separately. (See "Overview of electromyography" and "Overview of nerve conduction studies".)

PHYSICS OF NEUROMUSCULAR SONOGRAPHY — The physics of ultrasound as pertinent to the study of muscle and nerve is discussed here, but the topic is covered in greater detail separately. A glossary of terms used in neuromuscular ultrasound is available [1]. (See "Echocardiography essentials: Physics and instrumentation".)

The fundamental technique of ultrasound involves the insonation of tissue and analysis of the echoes reflected back to the insonating transducer. Reflected ultrasound occurs at interfaces within or between tissues of different acoustic impedance, a measure directly proportional to the speed at which sound travels through them. Bone conducts sound much faster than soft tissue; soft tissue conducts sound slightly faster than water but much faster than air. As such, the brightest echoes in the body are seen between bone and soft tissue. The use of coupling gel between skin and transducer minimizes the reflection that would otherwise occur between skin and air.

The frequency of insonated sound determines resolution and depth of penetration. Higher frequencies provide better resolution of superficial structures because of their shorter wavelengths, but lower frequencies provide better images of deep structures, albeit at somewhat lower resolution, because they penetrate deeper. This is the same principle that explains why the low-pitched rumble of thunder is audible for miles, but the sharp, high-pitched sound of a thunderclap is only heard with nearby lightning strikes. Intraluminal and intraoperative ultrasound probes offer additional means of obtaining high resolution in certain types of deep structures. (See "Intravascular ultrasound, optical coherence tomography, and angioscopy of coronary circulation".)

In addition to acoustic impedance, another property known as anisotropy is relevant to sonographic differentiation. Anisotropy is the tendency of tissues to reflect sound in a directionally dependent manner, as opposed to diffusely scattering the reflection. Different tissues exhibit variable degrees of anisotropy, and higher degrees of anisotropy result in differences in echogenicity when the ultrasound probe angle is changed. Using frequent, subtle adjustments in probe alignment, the skilled sonographer differentiates structures by observing the extent of this property in insonated tissues. As an example, tendons appear highly echogenic when the ultrasound probe is angled perpendicular to the tendon, but look almost anechoic when the probe is angled obliquely [2]. Holding the probe perpendicular to a desired target minimizes the impact of anisotropy and is an approach often used to obtain standard images (image 1).

Almost any imaging probe can be used to study muscle, although small muscles, such as extensor digitorum brevis, are best evaluated using high-resolution transducers. Much of the literature on muscle ultrasound (often referred to as musculoskeletal ultrasound) deals with the study of structural disorders of muscle such as strains, tears, hernias, hematomas, tumors, and other mass lesions [3,4]. In these conditions, the patient often can point to where the problem is. This review focuses on uses of ultrasound in the study of primary neurologic disorders of muscle and nerve in which the anatomic relationship of symptoms to pathology is more complex.

Unlike magnetic resonance and computed tomography (CT), ultrasound only provides a keyhole aperture for investigating pathology. As such, the technique involves serial evaluation of nerves and muscles at different locations best informed by a clinical evaluation and differential diagnosis.

ULTRASOUND OF MUSCLE TISSUE

Findings in normal muscle — Healthy muscle tissue has a distinctive appearance by ultrasound [3-5].

Anatomic features – In axial images, muscle consists of primarily echolucent (dark) areas interspersed with small, bright, curved echoes of seemingly random orientations. In the sagittal plane, however, these bright echoes are seen to be the fibrous tissue that surrounds muscle fibers and fascicles and are recognizable as striations (image 2). In bipennate or multipennate muscles, a central aponeurosis can often be identified as an area of thickened fibrous tissue. If followed distally, this structure becomes the tendon.

Ultrasound of muscle motion – With the exception of visible arterial pulsations, healthy muscle is static at rest. However, with slow contraction, the central portion of muscle can be seen to bulge with thinning of its more distal ends. In the area of bulging, thickening muscle fascicles can be seen to jostle for space in the increasingly pressurized environment (movie 1) [6]. In the sagittal view, the angle of pennation can be seen to change as the muscle moves through its range of motion [7]. The bulk of muscle thickening occurs with low levels of muscle contraction and effort, which explains why body builders can demonstrate their physique while retaining a relaxed expression [8].

Ultrasound can also be used to investigate kinesiology. As an example, with isometric dorsiflexion of the foot, the interosseous membrane separating the tibialis anterior from the tibialis posterior bulges posteriorly; with isometric foot inversion, it bulges anteriorly, reflecting the different activation of these two muscles (image 3).

Findings in diseased muscle — Ultrasound is capable of detecting the presence of chronic pathologic changes in muscle and measuring its dimensions. With special quantitative adaptations, the technique may provide additional information about more subtle or acute abnormalities.

There are four main findings that distinguish diseased muscle from healthy muscle [9]:

Increased echogenicity

Atrophy

Increased homogeneity

Loss of the bone shadow

Of these, increased echogenicity is the easiest to recognize. This results from replacement of normal muscle architecture with fat, fibrosis, loss of healthy muscle, and inflammation, all of which increase tissue reflections of sound. The highly organized nature of the myofibrillar structure of healthy muscle is conducive to sound transmission, whereas fat, inflammation, and fibrosis generate multiple microscopic reflectors of sound. The next most useful finding is atrophy, or loss of normal muscle bulk. This can be evaluated by comparison with an unaffected contralateral extremity or with published reference values adjusted for age and sex [10].

Healthy muscle is dark surrounded by bright tissue reflections from fibrous supportive tissue [9]. As the muscle becomes more echogenic with progressive disease, the distinction between normal fibrous tissue and muscle blurs, making the image more homogeneous. Loss of the bone shadow results from increased attenuation of the ultrasound signal as sound is either reflected or absorbed by the increased fat, fibrosis, and other changes.

Unlike needle electromyography (EMG) of muscle, which shows characteristic differences between myopathic and neurogenic findings, often a single ultrasound image does not easily distinguish between myopathic and neurogenic conditions (image 4 and image 5). However, the distribution of affected muscles is often different [5,11]. Generalized myopathies tend to affect proximal muscles, and generalized polyneuropathies tend to affect distal muscles. Certain distribution patterns are particularly informative. For example, inclusion body myositis can be recognized by marked atrophy and increased echo intensity in the flexor digitorum profundus with sparing of the adjacent flexor carpi ulnaris [12,13]. Changes restricted to a single root or nerve distribution are highly suggestive of neurogenic lesions. In some disorders, such as Duchenne muscular dystrophy, muscle enlargement occurs, which also is identifiable by ultrasound [14]. (See "Duchenne and Becker muscular dystrophy: Clinical features and diagnosis".)

Acute denervation of muscle leads to increased water content and swelling that cause measurable changes in echogenicity with sophisticated imaging analysis software [15,16]. However, to simple inspection of ultrasound images, such changes may be difficult to appreciate unlike the more striking changes on magnetic resonance imaging (MRI) [17-19].

The utility of muscle ultrasound for the diagnosis of neuromuscular disorders is evolving, particularly in specialized ultrasound centers [20]. In a 2008 review of prospective case-control studies, the sensitivities of visual evaluation of muscle echo intensity for the detection of a neuromuscular disorder in children ranged from 67 to 81 percent, and corresponding specificities ranged from 84 to 92 percent [21]. Among studies using methods that quantified muscle echo intensity (eg, by computerized image analysis), the sensitivities were higher and ranged from 87 to 92 percent. Thus, quantitative techniques may yield further improvements in the diagnostic utility of ultrasound [22]. A number of studies suggest that ultrasound is sensitive and specific in the diagnosis of myopathy and muscular dystrophy in children and adults [23-27]. The degree of ultrasound changes in these disorders has also been shown to correlate with findings from other imaging studies and with histopathology. The ratio of muscle echo intensity in the thenar and hypothenar eminence has utility in the diagnosis of amyotrophic lateral sclerosis, and similar strategies investigating the size and echo intensity of smaller muscles in the hand and feet may provide a noninvasive way to evaluate functional consequences of polyneuropathy and mononeuropathy [28-31].

A few other findings and limitations are of interest. Calcium deposition within muscle, a finding seen following trauma or in chronic dermatomyositis, is easily identified by ultrasound (image 6). Subcutaneous vascular calcifications are also readily apparent with this technique and may be seen in some inflammatory myopathies. Metabolic disorders of muscle, if they are not associated with significant histopathologic changes, typically show little change on ultrasound. Similarly, injection of botulinum toxin does little to alter muscle architecture and causes no change in echotexture. However, a single botulinum toxin injection causes measurable loss of muscle thickness at six weeks. This finding suggests that ultrasound might be a responsive biomarker for assessing progression or therapeutic intervention in neuromuscular disease [32].

Dynamic changes in diseased muscle — Fasciculations caused by spontaneously discharging motor neurons are probably the most studied dynamic change in diseased muscle [6,33]. Fasciculations cause contraction of a single motor unit (the motor axon and all the muscle fibers it innervates) in muscle. Clinically, a fasciculation appears as a focal twitch in a muscle, and most patients with fasciculations have multiple different motor units that discharge erratically.

Ultrasound is more sensitive than EMG at detecting fasciculations, probably because it samples a larger muscle region than needle EMG [6,21,34]. Fasciculations may be one of the first detectable manifestations of amyotrophic lateral sclerosis (ALS) and may have a role for screening asymptomatic relatives of those with familial forms of ALS [35]. In addition, ultrasound can increase diagnostic sensitivity of ALS using a modification of the Awaji criteria [36-39]. Ultrasound also allows specific aspects of fasciculations to be studied, such as twitch contraction time, contraction and relaxation durations, cross-sectional area involved by the twitch, and recurrence, but these features are largely of research significance (movie 2).

A variety of other aspects of altered dynamic function of muscle are amenable to study by ultrasound, such as changes in angles of pennation in disorders of muscle shortening, loss of contractile thickening in myopathy or neurogenic weakness, and slowed or increased relaxation times in thyroid disease, but such studies have largely gone unperformed. Of interest, ultrasound is capable of identifying the subtle movements of fibrillations in muscle (which correspond to fibrillation potentials on EMG), but special instruments and settings are required along with muscle warming and complete subject relaxation [40,41].

Ultrasound of the diaphragm is increasingly being used to evaluate suspected phrenic nerve palsy and other disorders affecting ventilatory function. Ultrasound is more sensitive to diaphragm movement than fluoroscopy, can assess diaphragm atrophy and thickening with inspiration, can help in decision-making regarding extubation of patients on mechanical ventilation or diaphragm pacing, and, if needed, can help guide needle EMG of the diaphragm [42-47]. As the technology of ultrasound evolves, other promising applications for neuromuscular diseases are being studied [48].

ULTRASOUND OF NERVE TISSUE

Findings in normal nerves — With currently available high-end instrumentation and high-resolution probes, major upper extremity nerves and their distal branches can be followed from the axilla into the digits. In the lower extremity, nerves can be followed from the gluteal region to the feet, but given the large diameter of the legs and the thickness of the feet and sole, it is more difficult to resolve proximal portions of the nerve and terminal branches. Large and small nerves of the brachial plexus are readily visible by ultrasound [49], but the lumbosacral plexus, because of its deep location, is not easily imaged in adults. Some cranial nerves can also be imaged [50].

Anatomic features – Nerves have a distinct appearance on ultrasound, but there is some variation in relation to nerve thickness and surrounding structures. A typical nerve has a honeycomb appearance with a somewhat echogenic external perineurium punctuated by hypoechoic rounded fascicles (movie 3) [5,51-53]. The number of apparent fascicles increases with the resolution of the ultrasound instrument. By contrast, nerve fascicles are never seen with CT and only become reliably apparent with 7 Tesla MRI scans [54].

At the wrist, when surrounded by hyperechoic tendons, the median nerve appears relatively hypoechoic, and, with lower-resolution probes, the nerve has a speckled appearance [5,51]. Similarly, the ulnar nerve at the elbow, perhaps because of its approximation to the bony medial epicondyle, may seem somewhat hypoechoic. In general, nerves are round to oval, but their shape varies as they course through the different tissues in an extremity. For example, the median nerve is often somewhat triangular in the forearm and flattens as it enters the carpal tunnel.

The fascicular anatomy of nerve is somewhat complex. Major nerve branches may appear on ultrasound as distinct fascicles within the same nerve sheath proximal to branch points, as seen with the peroneal and tibial branches of the sciatic nerve and motor and sensory branches of the radial nerve (movie 4). With higher-resolution transducers, the internal fascicular architecture of nerve is often apparent in greater detail. With ultra-high-frequency transducers, multiple fascicles can be seen; for example, up to 20 or more fascicles can be imaged in the median nerve at the wrist [53].

The brachial plexus has distinct anatomy (figure 1) [49]. The cervical nerve roots, although not visible within the spine, are visible after exiting from the spinal foramina, and they can be seen descending in grouped bundles of fascicles. Although gross dissection reveals discrete trunks and cords, it is difficult to define their boundaries with ultrasound particularly as they surround the subclavian artery, where they are compacted together. In the subclavicular region, the plexus can be difficult to image, but the nerves are more superficial and readily apparent in the axilla.

In general, nerves are readily distinguished from tendons, in that they are not freely movable, have different anatomic paths, and show less anisotropy. They are readily distinguished from arteries and veins because they do not pulsate and do not compress. In rare cases where there is a noncompressible venous thrombosis, the unique fascicular structure of the nerve, as well as its course and branching, are distinctive [5].

The distal portions of cranial nerves can also be imaged with ultrasound. The optic nerve is visible within the orbit, but heat generated by the ultrasound probe can cause cataracts in animals. Therefore, optic nerve evaluations should be done with special settings and safety-checked equipment [55]. Studies of the optic nerve show promise as a measure of increased intracranial pressure. (See "Elevated intracranial pressure (ICP) in children: Clinical manifestations and diagnosis" and "Evaluation and management of elevated intracranial pressure in adults".)

Branches of the facial nerve can be imaged as they course through the parotid gland, and both the spinal accessory and vagus nerves can be imaged in the cervical region [50,56,57].

Normal nerve movement – Nerves need to be able to move as extremities flex and extend, and as such are capable of movement in different directions. For example, with fisting and extreme flexion of the wrist, the median nerve, which is normally situated on the palmar surface of the carpal tunnel, rotates 90 degrees and dives below the other flexor tendons, an observation only apparent with real-time ultrasound (movie 5 and movie 6) [5]. In addition, the nerve can be seen to move proximally and distally with flexion and extension of the digits, although much less than the tendons move [58].

Similarly, the ulnar nerve in the ulnar groove and the sciatic nerve proximal to the popliteal fossa can be seen to move relative to nearby structures with flexion of the extremity, and dislocation of the ulnar nerve out of the ulnar groove is readily apparent with dynamic imaging (movie 7). The presence of such dislocation can significantly affect estimates of nerve conduction velocity and may lead to false-negative nerve conduction study results in patients with ulnar neuropathy at the elbow [59].

Findings in neuropathy — Ultrasound may aid in the electrodiagnostic evaluation of neuropathy. Nerve location may be better identified with ultrasound than with standard anatomic landmarks, and ultrasound can be used to better define suspected anatomic variants [60]. Additionally, structural changes such as nerve enlargement and loss of echogenicity may be seen with ultrasound [51,61,62].

In entrapment neuropathies, these changes are focal, just distal and proximal to sites of compression [63]. In demyelinating polyneuropathy, nerve enlargement occurs diffusely in inherited neuropathies and more irregularly in acquired inflammatory neuropathies [64]. Other findings include focal enlargement, entwinement or rotation of individual fascicles, increased nerve echogenicity, increased intraneural vascularity, or thinning (loss of volume), which may occur in different clinical contexts [65,66]. The pathologic basis of these changes is incompletely understood but probably reflects a variety of vascular, inflammatory, or reactive changes.

Visualization of these neuropathic changes and adjacent sources of nerve entrapment may be useful in the evaluation of patients with neuropathy [67]. In one study of 385 patients undergoing electrodiagnostic evaluations for suspected mononeuropathies, ultrasound provided additional diagnostic or therapeutic value to standard electrodiagnostic studies in more than one-third of cases [68].

Carpal tunnel syndrome — Ultrasound can be used in the diagnosis and evaluation of patients with carpal tunnel syndrome (CTS). Increased cross-sectional area of the median nerve on ultrasound can be a useful test to support the diagnosis of median neuropathy at the wrist (CTS) [69]. Ultrasound may also be helpful to identify alternative structural causes to CTS symptoms such as tenosynovitis [70]. In addition, ultrasound measures of CTS improve with successful symptomatic treatments. For example, median nerve cross-sectional area and intraneural vascularity reduce synchronously with both clinical and electrodiagnostic measures of improvement following glucocorticoid injections at the wrist [71]. Similar ultrasound improvements in the median nerve follow surgical decompression [72,73]. (See "Carpal tunnel syndrome: Pathophysiology and risk factors" and "Carpal tunnel syndrome: Clinical manifestations and diagnosis".)

Multiple studies have shown that the median nerve is enlarged and often hypoechoic in CTS [74-77], a finding that confirms a fundamental observation of surgeons who had noted that the median nerve frequently appeared swollen in patients with this disorder. The ultrasound finding in acute CTS is somewhat counterintuitive in that it is often said to be "pinched," and it might be expected that a reduction of myelin/axonal girth or inflammation might cause it to be hyperechoic. However, detailed studies confirm that overall, the median nerve is increased in size in CTS through all areas of compression [78]. There is some debate as to where to optimally measure median nerve enlargement in CTS, in part because of distal-proximal sliding of the nerve with wrist flexion. Regardless, it should always be assessed at both the wrist and palm in patients suspected of CTS, as enlargement may occur in only one of these locations [79].

The mechanism of nerve swelling with focal compression is hypothesized to be from damming of axoplasmic flow and increased small vessel blood flow, findings that would also explain reduced nerve echogenicity as seen on ultrasound. Studies in animals show nerve enlargement distal and proximal to chronic mechanical nerve compression [80-85].

Additional abnormalities that are associated with CTS include flattening of the median nerve and, on occasion, diminished dimensions of the carpal tunnel itself [86]. Other evidence has shown that nerves are less mobile in CTS [87,88]. Other findings, such as a bifid median nerve or a persistent median artery, may be relevant with regard to choosing a surgical approach to the disorder (movie 8). Thickening of the flexor retinaculum may also contribute to the disorder, and elastography may be informative [89,90].

Other entrapment neuropathies — Multiple studies of entrapped nerves at other locations show similar changes to the median nerve in CTS, with prominent nerve enlargement with loss of echogenicity, often with increased intraneural vascularity (image 7) [64,91-95].

Ultrasound can be used to identify ulnar neuropathy at the elbow [96]. Furthermore, ultrasound may distinguish ulnar nerve subluxation from complete dislocation out of the ulnar groove. This finding can help improve the accuracy of ulnar nerve conduction studies and can help in objective verification of ulnar nerve mobility, which influences the choice of operative procedure for surgical correction [59,97].

For patients with fibular neuropathy at the knee, ultrasound is also useful for detecting ganglion cysts, which are amenable to surgical treatment [98].

Ultrasound also has been shown to be cost effective in the management of focal mononeuropathies [99].

Other forms of focal nerve pathology — A growing body of literature supports the usefulness of ultrasound in identifying other types of nerve lesions. Perhaps most instructive are case reports demonstrating the ability of ultrasound to distinguish transected from crushed nerves, findings that have unequivocal surgical implications [100-102]. Large series have confirmed the value of ultrasound in evaluating suspected traumatic neuropathy.

Other types of gross nerve lesions are readily identified by ultrasound as well, including granulomas, neuromas (movie 9), ganglion cysts, extrinsic masses, neurofibromas, and other nerve tumors [103-107]. An unexpected presence of increased vascularity may be a sign of lepromatous neuropathy or neurolymphomatosis [108-110].

Polyneuropathy — Ultrasound is useful for detecting the nerve enlargement that characterizes hypertrophic hereditary and acquired demyelinating polyneuropathies [34,111,112].

The earliest reports of ultrasound of nerve disease were in hypertrophic neuropathies, such as Charcot-Marie-Tooth disease, in which palpably enlarged nerves were confirmed to be of increased size with ultrasound [113]. The extent and degree of enlargement, which are greatest in Charcot-Marie-Tooth type 1, occur at an early age and are somewhat more prominent proximally [114]. (See "Charcot-Marie-Tooth disease: Genetics, clinical features, and diagnosis".)

Significant enlargement of nerves in the brachial plexus and in the limbs is common with inflammatory neuropathies such as chronic inflammatory demyelinating polyneuropathy (CIDP) and multifocal motor neuropathy (MMN), and the absence of enlargement is fairly convincing evidence of the absence of CIDP or MMN [61,111,115-119]. (See "Chronic inflammatory demyelinating polyneuropathy: Etiology, clinical features, and diagnosis".)

In a report that used ultrasound to measure the cross-sectional areas of median and ulnar nerves, the results from 100 adult and pediatric subjects who had various neuropathies were compared with those from 90 healthy control subjects [61]. Nerve enlargement was found in the following proportions of subjects with neuropathy:

For patients with Charcot-Marie-Tooth type 1A, all 11 (100 percent)

For patients with CIDP, 31 of 36 (86 percent)

For patients with Guillain-Barré syndrome, 8 of 17 (47 percent)

For patients with axonal neuropathy, 7 of 36 (19 percent)

In patients with CIDP, nerve enlargement increased with longer time from disease onset [61]. In those with Guillain-Barré syndrome, nerve enlargement was found as early as 5 days and as late as 15 years after onset of symptoms. (See "Guillain-Barré syndrome in children: Epidemiology, clinical features, and diagnosis" and "Guillain-Barré syndrome in adults: Pathogenesis, clinical features, and diagnosis".)

Ultrasound has not shown consistent changes in axonal neuropathies. Cross-sectional area may be smaller in some cases, such as amyotrophic lateral sclerosis (particularly the ulnar nerve), and some sensory neuronopathies, such as CANVAS (cerebellar ataxia, neuropathy, and vestibular areflexia syndrome), presumably as a result of axonal loss [120,121]. By contrast, mild diffuse enlargement may be seen in diabetic polyneuropathy [122].

SUMMARY

Role of ultrasound in neuromuscular disease – Neuromuscular ultrasound is a diagnostic tool for nerve and muscle diseases that provides real-time anatomic and physiologic information. It is typically used in conjunction with standard diagnostic tests such as electromyography, nerve conduction studies, and tissue biopsy. (See 'Introduction' above.)

Findings in normal muscle tissue – Healthy muscle tissue has a distinctive appearance on ultrasound that readily distinguishes it from other tissues. In the axial image, muscle consists of primarily echolucent (dark) areas interspersed with small linear or curvilinear bright echoes. In the sagittal plane, these bright echoes are seen to be the fibrous tissue that surrounds both muscle fibers and fascicles and that gives rise to visible striations (image 2). (See 'Findings in normal muscle' above.)

Findings in diseased muscle – On ultrasound of muscle, both neurogenic and primary muscle diseases are associated with increased echogenicity, atrophy, increased homogeneity, and loss of the bone shadow. In some disorders, such as Duchenne muscular dystrophy, muscle enlargement occurs, and ultrasound effectively identifies hypertrophy. The most striking dynamic change in diseased muscle is the occurrence of fasciculations, which can be readily identified by ultrasound. (See 'Findings in diseased muscle' above.)

Findings in normal nerves – Nerves have a distinct but variable appearance on ultrasound. A typical nerve has a honeycomb appearance with a somewhat echogenic external perineurium punctuated by hypoechoic rounded fascicles (movie 3). (See 'Findings in normal nerves' above.)

Findings in neuropathy – Nerve location may be better identified with ultrasound than with standard anatomic landmarks, and ultrasound can be used to better define suspected anatomic variants. Additionally, structural changes such as nerve enlargement and loss of echogenicity may be seen with ultrasound. (See 'Findings in neuropathy' above.)

Neuropathic conditions – Ultrasound may aid in the electrodiagnostic evaluation of several forms of neuropathy. These include:

Carpal tunnel syndrome (see 'Carpal tunnel syndrome' above)

Entrapment neuropathies (see 'Other entrapment neuropathies' above)

Traumatic neuropathies (see 'Other forms of focal nerve pathology' above)

Hypertrophic hereditary and acquired polyneuropathies (see 'Polyneuropathy' above)

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Topic 14145 Version 23.0

References

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