Nerve Ultrasound in Peripheral Neuropathies: A Review Antonios Kerasnoudis, Georgios Tsivgoulis From the Department of Neurology, St. Luke Hospital, Thessaloniki, Greece (AK); Second Department of Neurology, University of Athens, School of Medicine, “Attikon” University Hospital, Athens, Greece (GT); and International Clinical Research Center, St. Anne’s University Hospital in Brno, Brno, Czech Republic (GT).

ABSTRACT Peripheral neuropathies are one of the most common reasons for seeking neurological care in everyday practice. Electrophysiological studies remain fundamental for the diagnosis and etiological classification of peripheral nerve impairment. The recent technological development though of high resolution ultrasound has allowed the clinician to obtain detailed structural images of peripheral nerves. Nerve ultrasound mainly focuses on the evaluation of the cross sectional area, cross sectional area variability along the anatomical course, echogenity, vascularity and mobility of the peripheral nerves. An increase of the cross sectional area, hypervascularity, disturbed fascicular echostructure and reduced nerve mobility are some of the most common findings of entrapments neuropathies, such as the carpal or cubital tunnel syndrome. Both the cross-sectional area increase and the hypervascularity detected with the Doppler technique seem to correlate significantly with the clinical and electrophysiological severity of the later mononeuropathies. Significantly greater cross sectional area values of the clinically affected cervical nerve root are often detected in cases of cervical radiculopathy. In such cases, the ultrasound findings seem also to correlate significantly with disease duration. On the other hand, multifocal cross sectional area enlargement of cervical roots and/or peripheral nerves is often documented in cases of immune-mediated neuropathies. None of the later pathological ultrasound findings seem to correlate significantly with the electrophysiological parameters or the functional disability. The aim of this review is to provide a timely update on the role of neuromuscular ultrasound in the diagnostic of the most common entrapment and immune-mediated peripheral neuropathies in clinical practice. Keywords: Nerve ultrasound, carpal tunnel syndrome, cubital tunnel syndrome, immune mediated neuropathies. Acceptance: Received March 2, 2015. Accepted for publication April 6, 2015. Correspondence: Address correspondence to Georgios Tsivgoulis, MD, Second Department of Neurology, University of Athens, School of Medicine, Athens, Greece, Iras 39, Gerakas Attikis, Athens, Greece, 15344. E-mail: [email protected]. J Neuroimaging 2015;25:528-538. DOI: 10.1111/jon.12261

Introduction Peripheral neuropathies remain one of the most common reasons for seeking neurological care in the general population.1 They occur as a component of several common and many rare diseases and are heterogenous in etiology, diverse in pathology, and varied in severity. The term peripheral neuropathies includes symmetric polyneuropathy, single and multiple mononeuropathy, and radiculopathy. While nerveconduction studies remain fundamental for the confirmation of the diagnosis, assessment of severity, and etiological classification of peripheral neuropathies, new challenges arose in the last years on how to acquire the best static and dynamic imaging of the relevant nerve structures, aiming to a holistic approach to peripheral nerve impairment. The first report of ultrasound waves was done in 1790 from Lazzaro Spallanzani, who noticed that bats use echolocation during their movement. While Pierre Curie was the first to discover and describe the piezoelectric phenomenon, one of his doctoral students Paul Langevin was first involved in the ultrasonic submarine detection. The use of ultrasound as a new diagnostic method began with the ultrasound evaluation of fetus and heart in the 1940s from Elder and Donald. The first descriptions of pathological ultrasound findings of the peripheral nerve system have been published by Solbiati et al, that reported the pathological changes of recurrent laryngeal nerve lesions in cadavers.2 Fornage et al3 were the first to describe the normal echoanatomy of the peripheral nerves. Over time, the clinical experience gained with ultrasound, 528

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combined with the technological improvement (enhanced software and emergence of>15 MHz frequency transducers) made the detailed imaging even of small sensory nerves (f.e palmar cutaneous branch of the median nerve) possible. Moreover, improvements in Doppler sensitivity and power Doppler allowed the objective assessment of vascular changes within nerve segments. The aim of this review is to provide a timely update on the role of neuromuscular ultrasound in the diagnostic of the most common entrapment and immune-mediated peripheral neuropathies in clinical practice.

Normal Findings in Peripheral Nerves Fornage et al published for the first time the normal findings of the most significant peripheral nerves, such as the median, ulnar, sciatic and fibular nerve,3 while Silvestri et al4 described in detail the fascicular echostructure of the later nerves. According to the literature, normal peripheral nerves have a tubular form, with alternating hypoechogenic and hyperchogenic zones, corresponding to nerve fibers and perineurium, given the impression of a "honeycomb" pattern when scanning transversely (Fig 1). Their size can be measured accurately in both the longitudinal and transverse scans, and depends mainly on their function (motor, sensory, mixed),5 while temperature, body mass index, age and gender may also influence nerve calibre.6 Although this is the most commonly found echopattern in peripheral nerves, occasionally an homogen, hypoechoic

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Fig 1. Axial scan of the median nerve proximal to the carpal tunnel, showing the typical “honeycomb” pattern of echogenity.

pattern may be documented in healthy peripheral nerves, such as the ulnar nerve in cubital tunnel, brachial plexus or even cervical roots.7 This finding may be mainly explained through the reduced volume of connective tissue expected in proximal anatomical segments of the peripheral nerves.7 The sonographic differentiation between nerves and tendons is based on the fact that tendons, in contrast to nerves, appear to have numerous parallel hyperechoic lines, seperated by hypoechoic lines (fibrillar pattern). In view of the anisotropy, decreasing the insonating angle on a normal tendon will cause it to change from brightly hyperechoic to darkly hypoechoic, while if the angle is then increased, the tendon will again appear hyperechoic.8 When scanning longitudinally, the reduced slippage of the nerves during the active or passive bending/extension of a limb is a further good point in differentiating them from tendons.8

Quantification of Pathological Ultrasound Findings The ultrasound examination of a peripheral nerve mainly focuses on the assessment of its 1) cross sectional area (CSA) at certain sites of clinical interest, 2) variability of the CSA along its anatomical course, 3) echogenity, 4) vascularity, and 5) nerve mobility. The CSA can be measured on transverse images, while the transducer is kept perpendicular to the nerve, applying minimal pressure. Variability within a measurement can be reduced by using an average of multiple measures (at least 3). Measuring just inside the echogenic rim of the nerve is the preferred technique (Fig 1). Cross sectional area (CSA) reference values for peripheral nerves and brachial plexus have been reported in various studies in the literature.6,9–11 The difficulty to differentiate though a normal from a pathological heterogeneity of CSA changes remained for years an important limitation of neuromuscular ultrasound. In order to deal with this limitation, four novel ultrasound measures, aiming to quantify pathologic ultrasound changes of peripheral nerves, have been recently introduced in the literature:9,12,13 1) the intranerve CSA variability (for each nerve), defined as maximal CSA/minimal CSA, 2) the internerve CSA variability (for each patient), defined as nerve with maximal intranerve CSA variability/nerve with minimal intranerve CSA variability, 3) the side-to-side difference ratio of the intranerve CSA variability (SSDIVA) (for each nerve), defined as side with maximal intranerve CSA variability/side with minimal intran-

erve CSA variability, and 4) the intraplexus CSA variability defined as: maximal CSA of the brachial plexus/minimal CSA of the brachial plexus. Intranerve CSA variability seems to be in the literature a useful marker to differentiate focal (higher values) from diffuse (lower values) nerve enlargements, while the internerve CSA variability may help to reveal a possible distribution pattern of peripheral nerve impairment.12,13 On the other hand, the “sideto-side difference ratio of the intranerve CSA variability” may be useful in detecting any lateralization of pathologic changes and the intraplexus CSA variability may help to differentiate focal (higher values) from diffuse (lower values) brachial plexus enlargement.9,13 In view of the vascularity of the nerve, this can be evaluated with the use of the Doppler technique. While normal peripheral nerves show no color Doppler signal, often increased intraneural blood flow is seen in various neuropathies, mainly as a result of compression or inflammatory response. Considering the graduation of hypervascularity, a recent study has introduced a new quantitative image-processing technique, documenting a significant correlation between the severity of carpal tunnel syndrome and hypervascularisation.14 Potential limitations of this technique may be external influencing factors (such as temperature and sympathetic limb tone), which have an effect on nerve blood flow. Therefore, skin temperature over the median nerve should be kept always above 32°C, while sympathetic afferences should be kept at stable and low levels. On the other hand, nerve echogenicity is usually assessed subjectively and based on the examiners experience. Recent studies have introduced some new techniques, aiming to help examiners quantify the echogenity in a reproducible manner.15,16 Among the pathological changes of echogenity, the ones most commonly seen are the reduced echogenicity with loss of the fascicular echostructure or the selective hypertrophy of individual nerve fascicles. Nerve mobility is usually evaluated in cases of entrapment neuropathies (such as carpal or cubital tunnel syndrome). During examination, patients are asked to flex their fingers (in CTS) or elbow (in CUTS), while the mobility of the median or ulnar nerve is evaluated. Although, the nerve mobility is usually evaluated subjectively and based on the examiners experience, techniques to quantify pathological findings may be applied.17,18 Among the most common pathological findings, are the reduced slippage of the median nerve during finger and wrist flexion in patients with CTS and the luxation/subluxation of the ulnar nerve to the medial epicondyle in patients with cubital tunnel syndrome.17–20

Pathological Findings in Entrapment Neuropathies Carpal Tunnel Syndrome Fornage et al3 described for the first time the pathological ultrasound findings of CTS, opening the way for an innovative diagnostic approach to peripheral nerve disease. The most common pathological findings seen in symptomatic CTS patients are: 1) enlarged CSA of the median nerve proximal to the edge of the flexor retinaculum, 2) increased wrist to forearm swelling ratio, 3) hypoechogenity and disturbed fascicular echostructure, 4) reduced slippage of the nerve, and 5) increased vascularity (Table 1) (Fig 2).

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Table 1. Overview of the Most Common Ultrasound Findings in Entrapment Neuropathies Syndrome

CTS

CUTS

Radial Fibular

Cervical radiculopathy

Findings

CSA > 0.11 cm2 100 wrist to forearm ratio > 1.4100 reduced echogenity increased vascularity reduced mobility CSA > 0.09 cm2 101 elbow to upper arm ratio > 1.4101 reduced echogenity increased echogenity of epineurium luxation/subluxation CSA > 0.06 cm2 9 reduced echogenity CSA > 0.12 cm2 54 reduced echogenity popliteal fossa-to-fibular head ratio > 1.454 side to side difference ratio > 1.560

CSA = cross sectional area; CTS = carpal tunnel syndrome; CUTS = cubital tunnel syndrome.

Nerve conduction studies are traditionally used as the confirmatory test for the diagnosis of CTS; however, ultrasound has increasingly gained interest as an alternative diagnostic test for CTS. The diagnostic sensitivity and specificity of nerve ultrasound in the diagnosis of CTS varies among literature reports (sensitivity 77.6%–91%, specificity 86.8%–93%),21–23 mainly depending on the reference standard used for the diagnosis. The cross-sectional area of the median nerve at the inlet of rpal tunnel (at the level of the pisiform) is the most sensitive and specific ultrasound finding in patients with CTS.24 While ultrasound will not replace electrodiagnostic testing in the diagnosis of CTS, especially in complicated or unclear cases, ultrasonography seems to provide significant improvement in the diagnostic accuracy according to a recently published evidence based guideline.24–26 On the other hand, both the CSA enlargement and the hypervascularity detected with the Doppler technique seem to correlate with the clinical and electrophysiological severity of CTS.14,27,28 One of the latest applications of neuromuscular ultrasound is the preoperative detection of anatomical variants or structural abnormalities that may lead to the development of CTS symptoms. Among them, the thrombosis or the presence of persistent

Fig 2. Ultrasound findings in a patient with carpal tunnel syndrome. (A) Axial scan of the median nerve just proximal to the carpal tunnel, showing a pathological cross sectional area enlargement (CSA = 0.20 cm2 , normal values ࣘ0.11 cm2 ) with relatively preserved fascicular echostructure, (B) axial scan of the median nerve in the middle forearm (between the flexor digitorum superficialus and profundus), showing the pathological wrist to forearm ratio = 0.20/0.09 = 2.22 (normal values 50% difference of the CSA, when compared to the unaffected left side (B).

of the peripheral nerves. This finding seems to highlight according to literature reports the immune-mediated patchy multifocal demyelination occurring along the nerve fibers in CIDP.63 In addition, Padua et al reported increased values of the intranerve CSA variability in several peripheral nerves, possibly highlighting the focal pattern of CSA enlargement occurring in CIDP.12 The above findings were confirmed in two later studies.13,63 The reports on the correlation of pathological CSA changes with electrophysiological findings in CIDP are controversial in the literature.61,66–69 Although some studies report, that motor nerve conduction seems to be significantly lower in nerve segments with increased CSA, while conduction blocks were often associated with increased CSA,66,67,69 the same findings were not confirmed in other studies.63,71 Furthermore, both nerve ultrasound and electrophysiology findings do not seem to correlate with functional disability.63 The use of nerve ultrasound scores in order to distinguish CIDP of sub-acute or progressive onset from GBS has been recently introduced in the literature. A sum score of ࣙ2 points in the “Bochum Ultrasound score” seems to allow with a sensitivity of 80% and specificity of 100% the distinction of subacute CIDP from acute inflammatory demyelinating polyneuropathy (AIDP).70 In a later preliminary study, the same score achieved better sensitivity and specificity, than classical electrophysiological (sural sparing pattern, sensory ratio) or clinical parameters (sensory symptoms or signs, autonomic nerve dysfunction, need for mechanical ventilation) in diagnosing CIDP of early onset.71 The authors concluded that the 4 anatomic sites summarized in the Bochum Ultrasound Score may highlight a specific distribution pattern of pathological findings for CIDP.71 In addition, a distinction of CIDP from multifocal motor neuropathy (MMN) or multifocal acquired demyelinating sensory and motor neuropathy (MADSAM) has been also reported with the use of the later score.72 In the same study, the authors concluded, that these ultrasound findings may reflect the clinical similarities of either MMN or MADSAM (predominantly asymmetrical, motor nerve impairment), when compared with the symmetrical, sensorimotor pattern of clinical affection usually occurring in CIDP.72 On the other hand, Grimm et al recently reported an “Ultrasound pattern sum score,” allowing the diagnosis of acute

and subacute onset CIDP and its variants with high sensitivity, specificity.73 According to this study, structural CSA changes were much more common in sensorimotor nerves and sural nerves in the case of CIDP, than in other neuropathies and controls.

Guillain-Barr´e-Syndrome (GBS) Zaidman et al published for the first time in the literature the findings of 17 patients with GBS, within 4 weeks from symptom onset.74 The median and ulnar nerves were found to be a 1.4fold enlarged compared to controls, but no correlation was identified between ultrasound and electrophysiological findings.74 The confirmation of both peripheral nerve and cervical root pathology during the early stage of the AIDP came later with the study from Grimm et al.75 The authors documented, higher CSA values almost in all peripheral nerves (with the exception of the ulnar nerve), while the CSA enlargement of the vagal nerve was most pronounced in patients with autonomic nerve dysfunction, compared to patients without.75 A possible explanation for the documented CSA enlargement could derive from the primary inflammatory demyelinating process of the proximal nerve trunks occurring in AIDP that may lead to inflammatory edema and increased endoneurial pressure. This orchestrated response seems to provoke the CSA enlargement of the peripheral nerves.76 On the other hand, according to a later study, nerve ultrasound parameters seem to show no significant correlation to electrophysiological findings or functional disability in postGBS patients.76 The authors of this study concluded, that both these diagnostic examinations seem to highlight different features of peripheral nerve impairment in AIDP. Both the functional outcome and the development of pathological nerve ultrasound changes could be eventually predicted through the increased cerebrospinal fluid (CSF) protein and reduced compound muscle action potential (cMAP) in motor conduction studies at disease onset.77

Multifocal Motor Neuropathy (MMN) Beekman et al published the first systematic study on the ultrasound findings of MMN.78 The authors reported in the majority of the 21 patients examined, a multifocal pattern of nerve

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Fig 7. Ultrasound findings in a patient with chronic inflammatory demyelinating polyneuropathy. (A) Axial and (B) longitudinal scan of the edematous median nerve in the upper arm, showing the complete loss of the fasciscular echostructure and the pathological cross sectional area enlargement (CSA = 0.62 cm2 ). Axial (C) and longitudinal scan (D) of the same nerve in the upper arm after immune therapy with immunoglobulines showing the restructure of the fascicular echostructure and the remaining hypertrophy of the nerve (hypertrophic remodelling) (CSA = 0.13 cm2 ).

enlargement, which was present at sites with and without clinical or electrophysiological abnormalities (Fig 8). The multifocal type of CSA enlargement was confirmed in a later study of 11 MMN patients.79 The authors based their pathophysiological explanation for these findings on pathological studies at sites of conduction blocks. According to these studies, perivascular areas, containing scattered demyelinated axons, surrounded by small onion bulb formations, are found often at sites of conduction blocks.79 On the other hand, nerve ultrasound findings do not seem to correlate with electrophysiological parameters or functional disability in patients with MMN.79,80 The use of ultrasound to differentiate MMN from other nosological entities, such as the amyotrophic lateral sclerosis (ALS) or the asymmetrical CIDP has been recently reported in the literature.81 According to a study from Grimm et al, CSA increase in various peripheral nerves was found significantly more frequently in MMN, than in ALS patients allowing a differentiation of these two diseases with a sensitivity of 87.5% and a specificity of 94.1%.81 The authors concluded that systematic ultrasound evaluation of different nerves and cervical roots could serve as an additional diagnostic marker to electrodiagnostic studies. In addition, using a recently introduced nerve ultrasound score (Bochum Ultrasound Score) a sonographic 534

differentiation of MMN from asymmetrical CIDP may be allowed with a sensitivity of 83.3% and specificity 57.1%.72

Multifocal Acquired Demyelinating Sensory and motor Neuropathy (MADSAM) Multifocal acquired demyelinating sensory and motor (MADSAM) neuropathy is characterized by an asymmetric multifocal pattern of motor and sensory loss, and conduction block and other features of demyelination in nerve conduction studies. There are only small case series in the literature on the ultrasound findings of MADSAM neuropathy. In the first case report,82 multiple focal nerve enlargements could be detected by ultrasound at sites of previous conduction blocks, well after complete clinical and electrophysiological resolution. In the second case report,82 existing proximal conduction blocks could be localized by ultrasound. These observations highlighted the importance of nerve ultrasound in identifying conduction blocks and demonstrated that sonographically detected morphological changes may outlast functional recovery in demyelinating neuropathies, such as MADSAM. In a similar MADSAM case with a disease course over 2 years, a hypertrophy of the median and ulnar nerve in the

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Fig 8. Ultrasound findings in a patient with multifocal motor neuropathy (MMN) and multifocal acquired demyelinating sensory and motor neuropathy (MADSAM) chronic inflammatory demyelinating polyneuropathy. Axial scan of the median (A) and ulnar nerve (B) in the upper arm in a patient with MMN, showing the cross sectional area enlargement (CSAA = 0.16 cm2 , CSAB = 0.19 cm2 ) with partial loss of the fascicular echostructure. Axial (C) and longitudinal (D) scan of the ulnar nerve 2 cm distal to the medial epicondyle in a patient with MADSAM showing the complete loss of the fasciscular echostructure without cross sectional area enlargement (CSA = 0.06 cm2 ). forearm on both sides, but no pathological findings in the lower extremities could be detected. The site where the hypertrophy was detected in ultrasound correlated with the site of conduction block in the nerve conduction studies (Fig 8).83 As previously noted, MADSAM and MMN seem to show according to a recent study much more sonographical similarities witheachother, than with CIDP.72

Vasculitic Neuropathy Peripheral nerve involvement is a common complication of systemic vasculitis, occurring in up to 30% of cases in different series.84 On classical cases, the manifestation can be rapid onset of painful sensory and motor loss affecting the lower extremities or a mononeuritis multiplex. Nodera et al85 observed for the first time a reduction of the echogenicity and diffuse CSA increase of the ulnar, tibial nerve and the cervical roots in vasculitic neuropathies. In this study ultrasonographic evaluation was repeated after 2 weeks of therapy with corticosteroids and showed significant reduction in the size of the ulnar nerve. On the other hand, Ito et al86 were able to demonstrate a statistically significant enlargement of the tibial nerve in patients with vasculitis, when compared to the control group. The lower limb pattern of structural nerve

involvement in vasculitic lesions was also confirmed in two later studies.87,88 A later study from Grimm et al89 in patients with vasculitic neuropathies highlighted for the first time, that CSA enlargement is most often seen in clinically and electrophysiologically affected nerves (22 out of 31), even during axonal involvement. The authors concluded that the detection of focal CSA enlargement in one or more axonal affected nerves could be a hint for vasculitic neuropathy and thus facilitate diagnostic and therapeutic procedures.

Paraproteinemic Polyneuropathy Abnormal ultrasound findings have been reported in patients with paraproteinemia by various, independent investigators. The first report of such findings was from Luccheta et al90 in patients with Polyneuropathy, organomegaly, endocrinopathy, M protein, skin changes (POEMS), showing CSA abnormalities mostly at entrapment sites, while no correlation was found between muscle weakness and CSA findings. A multifocal peripheral nerve involvement was also reported in a case of multiple myeloma.91 Interestingly, Padua et al92 reported pathological values both of the CSA and the intranerve CSA in various peripheral nerves in the majority of the

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28 patients with anti-myelin-associated glycoprotein antibodies (MAG) polyneuropathy.92 In addition, the enlarged nerves sum score in anti-MAG neuropathy patients was greater than in MAG-negative paraproteinaemic neuropathies and lower than in CIDP. In this stidy, no correlation was found between ultrasound findings and Inflammatory Neuropathy Cause and Treatment Group (INCAT) disability score or disease duration.92

Future Directions of Neuromuscular Ultrasound The technological development of neuromuscular ultrasound devices has provided the clinician with a tool for evaluating patients with symptoms and signs of peripheral nerve impairment. Furthermore, neuromuscular ultrasound appears to continuously win its place next to the electromyography (EMG) devices in neurophysiological laboratories, improving the accuracy of the needle placing and EMG examination and providing easily, quickly, and non-invasively reliable information on the structure of the relevant nerves and muscles. Although nerve ultrasound is an already established method for detecting underlying pathologies of entrapment neuropathies, the wide variety of distribution patterns observed in immune-mediated neuropathies has made it difficult until today to define sufficient ultrasound criteria for their diagnosis. The recently introduced ultrasound measurements have provided the sonographer with a tool to quantify pathological changes in peripheral nerve disorders.15,16 The additional use of new ultrasound scores, seems to be very promising aspect in differentiating several immune-mediated neuropathies and should be a significant goal of future research in order to study the external validity as well as the inter- and intra-rater reliability of these novel criteria.70–73 Furthermore, the development of certain ultrasound biomarkers, that may be applied in the therapy monitoring of these patients would significantly improve the diagnostic and therapeutic efficacy. On the other hand, sonoelastrography increasingly gains its role in the diagnostic of entrapment neuropathies. The combination of cross sectional area and acoustic coupler/nerve strain ratio seems to increase the diagnostic sensitivity in certain entrapment neuropathies, such as CTS.93–95 The use of the same method for evaluating structural changes in immune-mediated neuropathies and differentiating acute edema from chronic hypertrophy would be a challenging future aspect of research. Futhermore, the use of contrast agents seems to improve significantly the ability to reliably capture and measure low-flow microvascularity in entrapment neuropathies.96–98 The establishment of new diagnostic protocols both for common entrapment neuropathies, such as CTS or CUTS and polyneuropathies would help the clinician differentiate acute edema from chronic structural changes. Recent advances in ultrasound technology have resulted in the development of three-dimensional (3D) US, which has been particularly useful in the field of obstetrics. The first 3D ultrasound studies of the upper-extremity nerves were feasible for both qualitative evaluations (f.e. image quality, anatomical variations) and quantitative (CSA measurements) evaluations of the median, ulnar, and radial nerves in healthy volunteers.99 The application of this method in entrapment neuropathies may add useful information in the detection of the underlying cause.

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Journal of Neuroimaging Vol 25 No 4 July/August 2015

Nerve Ultrasound in Peripheral Neuropathies: A Review.

Peripheral neuropathies are one of the most common reasons for seeking neurological care in everyday practice. Electrophysiological studies remain fun...
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