Muscle Denervation and Nerve Entrapment

Muscle Denervation and Nerve Entrapment Syndromes Howard R. Galloway, B.M., B.S., F.R.A.N.Z.C.R.1

ABSTRACT

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Nerve entrapment and muscle denervation syndromes are often hard to diagnose, presenting as pain or unusual weakness. In addition many of the clinically named syndromes are poorly defined and understood. An understanding of the clinical signs, the normal and variant anatomy, and the often variable relationship between the imaging findings and the clinical findings is essential in the accurate diagnosis and management of these disorders. MRI has proved sensitive to the presence of muscle denervation and can provide high resolution imaging along the course of the major nerves allowing demonstration of mass lesions or normal anatomical variations. The diagnosis of nerve entrapment and muscle denervation syndromes can be a substantial clinical challenge. Imaging, particularly MRI, can prove very useful in confirming a nerve lesion by demonstrating changes of muscle denervation. Identification of the muscles involved combined with knowledge of the normal patterns of innervation and their variations can allow localization of the site of the nerve lesion. KEYWORDS: Muscle denervation, nerve entrapment, MRI

CLINICAL PRESENTATION AND DIAGNOSTIC ISSUES Nerve entrapment and muscle denervation syndromes are often hard to diagnose, presenting as pain or unusual weakness. In addition, many of the clinically named syndromes are poorly defined and understood. An understanding of the clinical signs, the normal and variant anatomy, and the often variable relationship between the imaging findings and the clinical findings is essential in the accurate diagnosis and management of these disorders. Although the cause and site of nerve compression syndromes can be directly imaged, in several clinical syndromes imaging shows signs of muscle denervation in the distribution of the affected nerve without demonstrating a mass or other focal cause. In some circum-

stances this may be due to the etiology of the nerve lesion being traction rather than compression, especially around the shoulder in athletes.

1 Department of Human Movement, University of Queensland, Richmond Surrey, United Kingdom. Address for correspondence and reprint requests: Howard Galloway, B.M., B.S., Department of Human Movement, University of Queensland, 1/27 Petersham Road, Richmond Surrey TW106UH UK (e-mail: [email protected]). Imaging of Muscle; Guest Editor, David A. Connell,

F.R.A.C.R., F.F.S.E.M.(UK). Semin Musculoskelet Radiol 2010;14:227–235. Copyright # 2010 Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: + 1(212) 584-4662. DOI: http://dx.doi.org/10.1055/s-0030-1253162. ISSN 1089-7860.

Direct Imaging of Nerve Compression Although at first sight an attractive proposition, in practice direct imaging of nerve compression has proved to be quite difficult. It is well recognized that compression of a nerve acutely causes swelling that is thought to be due to the blockage of axonal transport. Ischemia may also play a role, and histological studies in cadavers have shown epineural and perineural fibrosis.1,2 In some common situations such as carpal tunnel syndrome, imaging of the nerve itself at the site of compression is quite feasible. As well as unusual causes of compression

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Figure 1 Short tau inversion recovery images of the ulna nerve demonstrating high signal and swelling in a case of ulna neuritis in the cubital tunnel. (Images courtesy of Dr. K. Stevens, Stanford University, CA.)

by mass lesions in the canal or abnormalities of the nerve, changes in cross sectional area of the nerve have been described on ultrasound and appear to correlate well with the clinical presentation. Just how much the imaging adds to the diagnosis of the routine cases is still a matter for evaluation.3 Sometimes the effect of compression on the nerve itself can be demonstrated by a change in signal intensity on magnetic resonance imaging (MRI), and this has been described in the sciatic nerve in piriformis syndrome4 (Fig. 1). Often mass lesions or anatomical variations are be diagnosed and thought to be the cause of the patient’s symptoms, but these may be more commonly seen in asymptomatic individuals (e.g., supraspinous notch ganglia, variations in the sciatic nerve, and piriformis).

IMAGING FINDINGS AND HISTOLOGICAL CORRELATES OF DENERVATION MRI can consistently and sensitively demonstrate signs of muscle denervation, which has been apparent since the changes were first described by Polak et al.5 In rats with sciatic nerve lesions, Bendszus et al6 demonstrated an increased signal on short tau inversion recovery (STIR) images at 24 hours and on T2-weighted

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images at 48 hours that further increased up to 2 months. Fatty atrophy was evident as early as 7 days. Wessig et al7 from the same group showed similar findings with an increase in T2 after 48 hours that peaked at 3 weeks and was associated with increased capillary dilation. They found that the T2 signal normalized at 10 weeks, at which time it was associated with regression of capillary dilation. Gadolinium uptake of denervated muscle has been described at 48 hours after denervation, presumably on the basis of increased capillary permeability.8 Chronic denervation leads to fatty atrophy with fiber atrophy, increased fat between muscle fascicles and decrease in muscle size and increased signal on T1 images. Although most studies, both experimental and clinical, have used MRI, changes of denervation are also visible on ultrasound. Ku¨llmer et al9 studied MRI ultrasound and histological changes in rabbits after section of the suprascapular nerve. Sonography, MRI, and histopathology all showed early changes at 2 to 3 weeks with subtle histological changes, a minor decrease in fascicle diameter, and an increase in echogenicity on ultrasound and increase in T2 signal intensity on MRI (STIR was not used). At 28 to 35 days, definite changes were visible on all modalities, and this continued through to day 65. This was consistent with another study by Gunreben and Bogdahn,10 which showed sonographic changes from day 10 in a patient with acute brachial plexus palsy. In clinical settings, MRI appears to be the most sensitive with early changes on STIR images easy to appreciate and appearing earlier. An appreciation of the ultrasound findings is necessary, however, because ultrasound is often used in the investigation of clinical symptoms such as pain that may be associated with denervation. When compared with other tests such as electromyography (EMG), a further study from Bendszus et al11 demonstrated the comparable accuracy of MRI in the diagnosis of foot drop. Imaging has a further advantage in areas of complex anatomy where the nerves might not be easily or specifically accessible for EMG. In clinical settings, MRI appears to be the most sensitive with changes on STIR images easy to appreciate in the acute phase. In the most common clinical settings, however, nerve compression or traction injury is subacute, and so findings of edema and/or atrophy are usually present on MRI and ultrasound, although they may be more difficult to appreciate on ultrasound without comparison with normal muscle. The recognition of the imaging patterns of denervation is useful not only in diagnosing the presence of denervation but in determining the nerve involved and the level of the lesion on the basis of the distribution of the muscles involved.


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MUSCLE DENERVATION AND NERVE ENTRAPMENT SYNDROMES/GALLOWAY

Quadrilateral Space Syndrome Quadrilateral space syndrome was first described by Cahill and Palmer12 as a syndrome caused by compression of the posterior circumflex artery and axillary nerve by fibrous bands in the quadrilateral space with the arm in abduction and external rotation presenting with local tenderness in the quadrilateral space, typically in younger patients, often overhead athletes. The diagnosis was initially made by arteriography. Surgical exploration of the four patients in McAdams and Dillingham’s series13 showed fibrous bands entrapping the nerve in three and venous dilation in the fourth. A cadaver dissection study by McCelland and Paxinos14 showed that fibrous bands are a common finding in the quadrilateral space, present in 14 of 16 shoulders. The most common site for a fibrous band was between the teres major and the long head of the triceps. Where the bands were present, both internal and external rotation of the shoulder caused a reduction in the cross-sectional area of the quadrilateral space. Imaging apart from angiography in classic cases appears to have little positive predictive value apart from demonstrating rare cases of a mass such as a ganglion in the quadrilateral space.15

Isolated Teres Minor Atrophy True quadrilateral space syndrome is uncommon, but a much more common imaging finding is isolated teres minor atrophy (Fig. 2). This came to light with the widespread use of MRI for shoulder imaging and has been shown in up to 3% of consecutive shoulder MRIs.16 Initially this was thought to be a manifestation of quadrilateral space

Figure 2 Fatty infiltration and atrophy of teres minor as an incidental finding in an overhead athlete.

syndrome, but it is more common, often asymptomatic, and occurs in an older age group. The presence of other shoulder pathology in the older age group has led to a hypothesis that this is related to humeral decentering and represents a traction injury of the nerve.17 The presence of isolated teres atrophy in a younger patient, particularly an overhead athlete, may be significant, however, because teres minor has been shown in EMG studies to be an important stabilizer of the glenohumeral joint in overhead activities.18

Supraspinous Notch Syndrome The suprascapular nerve arises from the upper trunk of the brachial plexus and carries fibers from C5 and C6. It provides the motor innervations to the supraspinatus and infraspinatus muscles. After leaving the brachial plexus, the nerve runs dorsally through the suprascapular notch running under the transverse scapular ligament into the suprascapular fossa where it supplies the supraspinatus. The nerve then travels through the spinoglenoid notch under the spinoglenoid ligament, exiting the fibro-osseous tunnel and ending by innervating the infraspinatus. The site of compromise of the nerve will determine the pattern of muscle involvement. A lesion in the supraspinous notch will affect both supra and infraspinatus, whereas a lesion in the spinoglenoid notch will only affect the infraspinatus. The role of entrapment of the suprascapular nerve as a cause of chronic shoulder pain was first described by Thompson and Kopell in 1959.1 Since then the syndrome has been reported many times, and multiple causes have been identified including acute trauma and nontraumatic causes such as ganglion cysts, inflammatory conditions, overhead athletic activities, and variations in the anatomy of the supraspinous notch and ligament. An anatomical study by Ticker et al19 demonstrated considerable variation in the shape of the suprascapular notch and the superior transverse scapular ligament. Partial and complete ossification of the ligament and multiple band were described, all of which may potentially compromise the nerve in the supraspinous or spinoglenoid notch. A ganglion in the supraspinatus fossa was seen in one case. Supraspinous notch ganglions are common and usually arise from a tear of the superior glenoid labrum. The presence of signs of denervation associated with a ganglion suggest the ganglion as the cause, but EMG is required for confirmation because the nerve lesion may be due to traction or ligament compression rather than compression by the ganglion. Although nerves may be injured as a result of acute traction (e.g., acute dislocation) (Fig. 3), signs of denervation may be common and apparently incidental


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Figure 3 Edema in the supraspinatus and infraspinatus as a result of an acute traction injury that also resulted in an acute tear of the supraspinatus tendon and an interstitial tear of the inferior glenohumeral ligament.

in overhead athletes although associated with definite functional abnormalities20 In this study of volleyball players, isolated infraspinatus lesions were common. Studies have also shown that there may be substantial elongation of the nerve with overhead motion.21 In imaging the shoulder, radiologists need to be aware that isolated denervation of the teres minor may be an incidental finding, particularly in older patients with other pathology. In overhead athletes there are often multiple lesions, and the presence of denervation, although not symptomatic in the usual sense, may be associated with functional deficits.

Piriformis Syndrome Piriformis syndrome, which proposes compression or entrapment of the sciatic nerve by the piriformis as it exits the pelvis, is a controversial entity that predates the recognition of the role of the intervertebral disc in producing symptoms. The diagnostic criteria and indeed the very existence of the syndrome remain the subject of discussion.22 There are no high-quality systematic studies linking imaging findings to the clinical syndrome. In this brief review we touch on the anatomical variants and the imaging findings that various authors have believed to play a potential role in the syndrome.

Anatomy and Variations The sciatic nerve is formed by roots from the lumbosacral plexus (L4, L5, S1, S2, and S3) and consists of 20% nerve fibers and 80% loose fibrofatty tissue. After a short course on the piriformis muscle, it exits the pelvis below the muscle. There are several reports in the literature citing variations in the exit of the sciatic nerve relative to the piriformis.22,23 The piriformis muscle

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itself originates from the anterior surface of the sacrum by way of fleshy digitations from the second, third, and fourth sacral vertebrae. After crossing the anterior surface of the sacroiliac joint, it exits the pelvis through the sciatic notch to insert into the upper border of the greater trochanter by way of a round tendon that is often a conjoint piriformis and obturator internus or gemelli conjoint tendon. Pecina24 demonstrated an intrapelvic division of the sciatic nerve into peroneal and tibial components within the pelvis in 26% and postforaminal division in 4.6%, division at the inferior border of the gluteus maximus in 11.5%, and division in the proximal thigh in the remainder. In 18% the peroneal division splits the piriformis into two bellies with the nerve passing between them. Proposed etiologies have included direct compression of the nerve, entrapment of the nerve by adhesions either posttraumatic or primary, and stretching of the nerve due to piriformis hypertrophy. MRI is capable of demonstrating the anatomical variations and also increased signal within the sciatic nerve itself. There are, however, only a few MRI studies of piriformis syndrome and even fewer with surgical and outcome correlation.4,22 Hypertrophy of the piriformis has been shown in symptomatic patients but also in asymptomatic patients and in the asymptomatic side of symptomatic patients. Anatomical variants of the nerve are common and inconsistently associated with symptoms. In the largest series,4 there were variable findings with enlargement or atrophy of the ipsilateral piriformis, enlargement of the gemelli and atrophy of more distal muscles including hamstrings and peronei. Lewis et al4 also reported increased signal in the sciatic nerve on STIR images at the level of the sciatic notch or, in one patient, the ischial tuberosity. In this and other series, patients responding to surgery have had normal imaging. Adhesions between the nerve and adjacent structures have been reported in an operative series23 but have not been visualized with MRI. The largest imaging series with surgical confirmation24 affirmed the ability of MRI to demonstrate the anatomical variations, but the relationship to symptoms remains unclear because there was no asymptomatic control, and three patients with no anatomical abnormality had resolution of their symptoms following tenotomy of the piriformis and neurolysis (Figs. 4A and B).

Role of Imaging Patients who have been assessed for sciatica that remains unexplained after assessment of the lumbar spine may have their pelvis imaged for extraspinal causes of sciatica. Although the relationship to symptoms is problematic, it


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is useful to be able to identify normal variants of the piriformis and be aware of the possible significance of increased signal in the sciatic nerve and the perineural structures.

Common Peroneal Nerve The common peroneal nerve courses anterolaterally along the biceps femoris muscle, around the fibular neck deep to the peroneus longus tendon, and enters the peroneal tunnel. As it enters the tunnel, the nerve divides into the superficial and deep peroneal nerves. Nerve compression within this area (peroneal tunnel) results in pain along the dermatome of the common peroneal nerve. The common peroneal nerve is prone to injury as it passes superficially around the neck of the fibula. The nerve may be subject to local trauma through impact or external compression, traction injury from an ankle sprain or compression, or stretching from a local

mass such as a ganglion arising from the proximal tibiofibula joint. In addition, an unusual site of compression has been described due to a variation of the distal biceps femoris tendon.25 MR imaging can depict the peroneal tunnel and the common peroneal nerve and its branches. The most clinically relevant use of MRI is in demonstrating denervated muscles and space-occupying lesions, rather than examining the nerve itself (Figs. 5A and B).

Obturator Nerve Entrapment The obturator nerve contains fibers from L2, 3, and 4 and arises from the anterior division of the lumbar plexus and then descends through the psoas running downward over the sacral ala into lesser pelvis entering the upper part of the obturator foramen and then divides into anterior and posterior branches. The anterior branch runs in front of obturator externus and adductor brevis

Figure 5 Large lobulated ganglion of the (A) proximal tibiofibular joint with (B) early changes of denervation in the peroneals as a result of stretching of the nerve over the mass. The patient complained of pain and had minor objective weakness.


Figure 4 Piriformis syndrome. (A) Asymmetry of the piriformis with the left muscle larger than the right (arrow). (B) Under computed tomography guidance, needle seen in the belly of the piriformis; the muscle may be injected to relieve symptoms and, presumably, muscle spasm. (Images courtesy Dr. D.A. Connell, The Royal National Orthopaedic Hospital, Middlesex, UK.)


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Figure 6 (A) Image demonstrating the anatomy of the heel showing the lateral plantar nerve (arrow). Images demonstrate atrophy and edema of the abductor digiti minimi on (B) coronal and (C) short tau inversion recovery. (Images courtesy of Dr. K. Stevens, Stanford University, CA.) AbD, abductor digiti; AbH, abductor hallucis; FDB, flexor digitorum brevis; QP, quadralus planti.

behind the pectineus and adductor longus muscles giving an articular branch that enters the hip joint through the acetabular notch, supplying branches to the hip adductors, and dividing into cutaneous, vascular, and communicating branches. Obturator neuropathy is a difficult clinical problem to evaluate. The most prominent symptom of obturator neuropathy is pain radiating from the groin into the medial upper aspect of the thigh. Dysesthesia and weakness of the muscles supplied by the obturator nerve can occur if the neuropathy is severe. The most common cause of pain, particularly in athletes, is due to fascial entrapment of the nerve.26,27 Surgery in patients with fascial entrapment has demonstrated entrapment of the obturator nerve by a thick fascia overlying the short adductor muscle. Classically obturator neuropathy can be caused by a pelvic fracture, hip arthroplasty, abdominal or pelvic surgery, forceps delivery, lithotomy position, pelvic tumor, obturator hernia, and, rarely, acetabular cyst. Once again the major role of MRI is in identifying signs of denervation in the adductor brevis and longus muscles. In more unusual causes the primary lesion (e.g., acetabular labral ganglion28) may be demonstrated.

from heel pain due to plantar fasciitis. Baxter’s neuropathy may account for 20% of cases of heel pain but is frequently overlooked as a potential cause of pain. Chundru et al29 found an incidence of atrophy of the abductor digiti minimi muscle atrophy (ADMA) of 5.6%, and there were significant differences between patients with ADMA and controls in advancing age, calcaneal spur, and plantar fasciitis. Entrapment of the inferior calcaneal nerve may result from altered biomechanics, reflected by posterior tibial tendon dysfunction or Achilles tendinosis, or it may result from direct mechanical compression of the nerve due to plantar fasciitis and/or plantar calcaneal enthesophytes. On MRI, the presence of ADMA reflects chronic compression of the inferior calcaneal nerve and suggests the clinical diagnosis of Baxter’s neuropathy in an appropriate clinical setting30 (Figs. 6A–C). For patients in whom heel pain persists despite conservative therapy, MRI evaluation is indicated prior to any surgical intervention. When ADMA is demonstrated prior to fasciotomy, the surgical approach may be modified to address the nerve compression as well as the fascial pathology.

Baxter’s Neuropathy (Lateral Plantar Nerve) Entrapment of the first branch of the lateral plantar nerve (inferior calcaneal nerve), or Baxter’s neuropathy, produces medial heel pain that may be indistinguishable

ENTRAPMENT NEUROPATHIES IN THE FOREARM There are several entrapment neuropathies in the forearm that may be difficult to diagnose clinically, often


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Posterior Interosseous Nerve Syndrome The radial nerve arises from the posterior cord of the brachial plexus and runs with the brachial artery around the humerus in the spiral groove. Above the elbow it crosses onto the volar aspect of the elbow through the lateral intermuscular septum. Anterior to the epicondyle the nerve divides into deep motor and superficial sensory branches. The deep branch passes through the supinator and comes to lie on the dorsal aspect of the interosseous membrane. The nerve then gives off multiple motor branches mostly to the extensor muscles of the forearm and hand. There are multiple possible sites of compression.31,32 When the lesion occurs more distally, there is weakness in the forearm with identification of the specific muscle involved allowing localization of the lesion. The clinical radial tunnel syndrome that presents as a purely sensory disturbance with lateral elbow pain is a controversial clinical entity.21 The existence of the radial tunnel and possible sites of compression remain in dispute. The clinical picture is very similar to lateral epicondylitis and imaging, and other tests cannot confirm the diagnosis. The role of imaging in this situation

is in the first instance to assess the lateral epicondyle and also to seek evidence of denervation in the more distal muscles.

Pronator Syndrome Pronator syndrome presents as chronic forearm pain as a result of entrapment of the median nerve at the level of the pronator teres. Compression is thought to result from anatomical variants of the deep and superficial origins of the pronator or of the bicipital aponeurosis or the fibrous arch origin of the flexor digitalis superficialis. The clinical presentation is dominated by pain and numbness in the volar aspect of the forearm, often bought on by an episode of excessive pronation and supination. MRI usually does not demonstrate the site of the compression but demonstrates changes of denervation (usually edema) in the pronator teres33 (Fig. 6B).

Anterior Interosseous Nerve The anterior interosseous nerve is a motor branch of the median nerve lying in the anterior compartment of the forearm. The nerve arises 2 to 8 cm distal to the medial epicondyle lying deep in the forearm on the volar surface of the interosseous membrane. The nerve usually gives branches to the flexor pollicis longus (FPL), pronator quadratus, and the flexor digitorum profundus (FDP) of the index and middle fingers. Most cases are thought to be neuritis and arise and resolve spontaneously. Patients typically present with pain in the volar aspect of the forearm with associated muscle weakness of the thumb, index, and middle fingers as determined by the innervation (Fig. 7A and B).

Figure 7 Anterior interosseous nerve syndrome. Patient with a proximal lesion of the nerve demonstrating edema in the flexor pollicis longus, (A) flexor digitorum profundus and (B) pronator. (Images courtesy of Dr. K. Stevens, Stanford University, CA.)


presenting with pain and/or sensory disturbance. Imaging can confirm the presence of a nerve lesion by demonstrating changes of denervation. Imaging is often not able to determine the cause of the entrapment but is helpful in determining the presence of denervation changes, and the pattern of changes can localize the nerve involved and the site of the lesion. In atypical cases imaging may also provide a means of following the course of the condition.

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The site and cause of the nerve lesion is usually not demonstrated by MRI, but signs of denervation, usually edema, are seen in the FPL, FDP, and the pronator quadratus. As in other syndromes MRI may also be useful in following the course of the condition if it fails to resolve as expected.33 MRI can provide highresolution imaging along the course of the major nerves, allowing demonstration of mass lesions or normal anatomical variations.

CONCLUSION The diagnosis of nerve entrapment and muscle denervation syndromes can be a substantial clinical challenge. Imaging, particularly MRI, can prove very useful in confirming a nerve lesion by demonstrating changes of muscle denervation. Identification of the muscles involved combined with knowledge of the normal patterns of innervation and their variations can allow localization of the site of the nerve lesion.

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