PROXIMAL NEUROPATHIES OF THE UPPER EXTREMITY

ENTRAPMENT AND OTHER FOCAL NEUROPATHIES

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PROXIMAL NEUROPATHIES OF THE UPPER EXTREMITY Kimberly L. Goslin, MD, PhD, and Lisa S. Krivickas, MD

LONG THORACIC NERVE

Anatomy

The long thoracic nerve is a pure motor nerve, providing innervation exclusively to the serratus anterior muscle (Fig. 1). It arises before formation of the brachial plexus from the ventral rami of the C5-C7 spinal nerves, with the largest component coming from C6. Immediately on exiting the intervertebral foramen, branches from the C5 and the C6 roots combine to form a common nerve trunk proximal to the middle scalene muscle and are usually joined by a branch from C7 after traversing this muscle. The nerve passes behind the clavicle and is angulated as it enters the axilla and runs posterior to the brachial plexus. It then passes over the first and the second ribs before descending superficially along the thoracic wall on the surface of the serratus anterior. Clinical Presentation

The serratus anterior muscle primarily functions to anchor and stabilize the scapula and thus the shoulder girdle during movement. With assistance from the pectoralis major and minor muscles, it also protracts the scapula (pulls the scapula anteriorly). Injury to the long thoracic nerve

From the Department of Neurology, Oregon Health Sciences University, Portland, Oregon (KLG); and the Department of Physical Medicine and Rehabilitation, Harvard Medical School, and Electrodiagnostic Services, Spaulding Rehabilitation Hospital, Boston, Massachussetts (LSK)

NEUROLOGIC CLINICS

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VOLUME 17 NUMBER 3 * AUGUST 1999

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Figure 1. Long thoracic nerve originates from the C5-C7 nerve roots, proximal to the brachial plexus. It runs inferiorly behind the clavicle, and descends along the thoracic wall to innervate the serratus anterior muscle. (From Fisher M:Other rnononeuropathies of the upperextrernity. ln Brown WF, Bolton CF (eds): Clinical Electrornyography, 2nd ed. Boston, Butteworth, 1993, 271 ; with permission.)

produces scapular winging. Because of the central role played by the serratus anterior in anchoring the scapula, active abduction of the affected arm is often limited to 90". With the arm at rest by the side of the body, the scapula as a whole translates medially with the inferior angle also rotating medially. The involved shoulder appears somewhat lower because of the scapular rotation. These abnormalities are accentuated by having the patient flex the arm anteriorly (by pushing against a wall or performing push ups). Long thoracic neuropathy is often painless, and patients may not be aware of its presence until they note scapular winging in a mirror or experience shoulder dysfunction. Because of muscle imbalance around the shoulder girdle, many patients develop a dull ache around the shoulder; they may even develop rotator cuff pathology because of altered bio-

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mechanics. A more severe, burning pain occurs when serratus anterior weakness is caused by neuralgic amyotrophy. With injuries caused by excessive nerve stretching during physical activity, a sharp pain in the shoulder may radiate to the neck and the upper arm.52 Differential Diagnosis

With long thoracic mononeuropathy, shoulder muscles other than the serratus anterior may appear weak (deltoid, supraspinatus, infraspinatus), suggesting the possibility of injury to the axillary or suprascapular nerves. However, if these muscles are tested with the examiner’s hand stabilizing the scapula, much of the apparent weakness disappears. Weakness of trapezius or rhomboid muscles also produces scapular winging. In contrast to serratus anterior weakness, which produces medial translation of the scapula and medial rotation of the inferior angle, trapezius dysfunction produces lateral translation of the scapula accompanied by medial rotation of the inferior angle, producing a true shoulder droop. Damage to the dorsal scapular nerve with rhomboid weakness produces scapular winging with prominence of the inferior angle and lateral translation of the scapula, accentuated by arm abduction. C6 or C7 radiculopathies may also produce weakness of the serratus but involvement of other muscles is also expected. Several muscular dystrophies may be associated with scapular winging relatively early in their course. However, bilateral involvement, slow progression and a specific pattern of involvement of other muscles distinguish these disorders from long thoracic neuropathy. Avulsion of the serratus anterior from the scapula also may produce winging and simulate a nerve injury. Electrodiagnostic Evaluation

Electrodiagnosis of long thoracic nerve palsy relies primarily on the needle electrode examination (NEE) portion of the electrodiagnostic evaluation (EDX). There is no reliable way to study this nerve with nerveconduction (NCS), although several techniques have been de~ ~ r i b e d .Most ~ , ~of~ the , ~ techniques ~ , ~ ~ use a needle electrode to record the compound motor action potential (CMAP) from the serratus anterior, so no useful information is obtained from the amplitude of the response. When recording with needle electrodes, minimal movement of the needle drastically alters the amplitude. Latency information is of questionable significancebecause lesions of this nerve are unlikely to be demyelinating in pathophysiology. To exclude the possibility of a more widespread brachial plexus lesion, sensory nerve conductions should be performed, studying especially those nerve fibers that travel through the upper and the middle trunks of the brachial plexus (the lateral antebrachial cutaneous, median, and radial sensory nerves) and thus have the same root innervation as the long thoracic nerve.

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In long thoracic neuropathy, NEE abnormalities are restricted to the serratus anterior muscle. This is a difficult muscle to study. It can be approached below the inferior angle of the scapula or along the midaxillary line. Caution must be taken to insert the needle directly over a rib. If the needle is inserted too deeply between ribs, a pneumothorax may result. Intercostal muscle activity may be mistaken for residual serratus anterior activity. This can be assessed by comparison of the level of electromyographic activity when the patient takes a deep breath with that obtained during attempted contraction of the serratus muscle. Other C5-C6-C7innervated muscles and cervical paraspinal muscles should be sampled to exclude a radiculopathy or brachial p l e ~ o p a t h y . ~ ~ General Diagnostic Tests Electrodiagnosis is the main tool for evaluating long thoracic neuropathy. Cervical spine and brachial plexus MRI studies may be also indicated when a radiculopathy or plexopathy is being considered in the differential diagnosis. Origin The three major causes of isolated long thoracic nerve injuries are neuralgic amyotrophy, trauma, and repetitive activities producing excessive stretch or traction of the nerve.4l Neuralgic amyotrophy typically presents with the acute onset of severe, burning shoulder pain without a known history of trauma. Within a few days, the pain begins to dissipate, and weakness develops. Multiple portions of the brachial plexus may be involved in a patchy pattern. Parsonage and Turner73found that 30 of 136 patients who have neuralgic amyotrophy had abnormalities limited to the long thoracic nerve. other^^^^^^^^^^^^,^^^ have also reported a high frequency of isolated long thoracic neuropathy with neuralgic amyotrophy. The supraspinatus, infraspinatus, deltoid, serratus anterior, or muscles innervated by the anterior interosseous nerve are also commonly involved. There have been several reports of postoperative long thoracic neuropathy65that may be a form of neuralgic amyotrophy or a stretch injury caused by positioning during surgery. The long thoracic nerve lies superficially in the supraclavicular region, where it is subject to trauma.50Kauppila and K e ~ n a h a nreviewed ~~ 197 cases of long thoracic neuropathy and found that 32 were iatrogenic related to local invasive procedures along the course of the nerve: first rib resection^,^^ mastectomies with axillary node scalenectomies, chest tube insertion, and infraclavicular plexus anesthesia. The incidence of long thoracic nerve palsy after radical mastectomy is approximately 10% and is 1.1%after simple mastectomy.22,26 No cases have been reported after lumpectomy with axillary node dissection, but a long thoracic mononeuropathy has been reported as a result of radiation therapy given in conjunction with l~rnpectomy.~~

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It is thought that the straight course of the long thoracic nerve from origin to insertion, its fixation at the scalenus medius and serratus anterior muscles, as well as the angulation of the nerve as it enters the axilla make it vulnerable to stretch injuries. Such injuries may occur from trauma or repetitive stressful movement of the s h o ~ l d e r .The ~ ~ ,stretch ~~ theory of long thoracic nerve injury is supported by a cadaver study in which a proximal segment of the long thoracic nerve was stretched to twice its normal resting length by raising the ipsilateral arm overhead and turning the head to the opposite side.41Elongation of any nerve by greater than 10% of its resting length may result in neurapraxia.12Sports- or workrelated injuries of the long thoracic nerve occur when the ipsilateral arm is in an outstretched, overhead position7I as in weight training, ballet warm-up stretches,Io3chopping wood, playing golf and tennis, gymnastics, wrestling, batting a baseball,4l operating industrial machinery, and using a Long thoracic nerve injury has also occurred from chiropractic manipulation of the cervical spine.72Overhead arm positioning may be a factor in some of the isolated long thoracic neuropathies occurring during surgery with general a n e s t h e ~ i a .Traction ~ ~ , ~ ~ or compression of the neurovascular structures may occur during anesthesia when the upper arm is passively moved while the serratus anterior is paralyzed and thus not fixing the scapula to the chest wall. In addition to the stretch theory of long thoracic neuropathy, Horowitz and to cant in^^^ proposed several potential mechanisms of entrapment based on nerve dissections in 100 cadavers: (1) scalenus spasm or injury compressing intramuscular fibers of the nerve, (2) angulation of the nerve trunk as it crosses the second rib and its overlying heavy musculature, (3) trapping of the nerve between the coracoid process and the second rib when the scapula is forced medially, and (4) inflammation of the bursae with which the nerve is associated, causing nerve compression. These mechanisms have not been ~ o n f i r m e d . ~ ~ If one receives a direct blow to the shoulder or the lateral thoracic wall while playing football or during a fall, the nerve may be compressed, producing injury.91Another form of compressive neuropathy has been reported in soldiers and hikers who carry heavy backpacks and has been termed rucksack p a l ~ y . ~ ~ , ~ ~ Practical Management

Treatment depends on the mechanism of nerve injury. If caused by overuse, initial management consists of rest and avoidance of the offending precipitating movement. Physical therapy is essential to maintain shoulder range of motion and to increase strength of the trapezius and rhomboids to maximize scapular stability. Active exercises should be performed in the supine position during the early phases of recovery, allowing the weight of the body to fix the scapula against the thorax, hereby preventing further winging and overstretching of the nerve. Special attention should also be given to stretching the latissimus dorsi, levator

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scapulae, pectoralis minor, and rhomboid muscles, which have a tendency to become contracted and painful. Numerous orthotic devices have been advocated for maintaining the scapula against the thorax9*and in an attempt to correct scapular dysfunction, but most are ineffective86or poorly tolerated. A variety of surgical procedures have been proposed to replace serratus anterior muscle function. Because of the long course of the nerve, these procedures should only be performed after 2 years have passed without apparent recove r ~ .The ~ ~most , ~ commonly ~ performed procedures are transposition of the pectoralis major, pectoralis minor, rhomboids, or teres major musc l e ~ .Another ~ ~ ~ surgical ~ ~ , ~approach ~ ~ is scapulothoracic fusion, which eliminates the scapular winging but at the expense of reduced scapulothoracic motion. Prognosis

Most injuries caused by carrying, lifting, or stretch are incomplete, and good functional recovery occurs. Fardin30studied electromyography (EMG) abnormalities in 10 patients up to 45 months after such injuries to the long thoracic nerve, with good functional outcome in 9 of the 10 patients. Gregg et a14' described 10 cases of isolated complete paralysis of the serratus anterior muscle in young athletes. Full recovery occurred in an average of 9 months, with a maximum of 2 years. Recovery of long thoracic neuropathy from neuralgic amyotrophy has a similar prognosis and time c o ~ r s e Even . ~ ~ ,in~patients ~ who regain full functional use of the arm, mild scapular winging may persist. Patients who have long thoracic nerve palsy caused by trauma have a poorer prognosis with only partial or no recovery because they usually have a more severe lesion.40Needle EMG can be used to help evaluate recovery. Because the reinnervation distance is a long one, it may take as long as 6 months before nascent motor unit potentials appear after axonotmetisis of the long thoracic nerve. If there is no electromyographic evidence of nerve function at 2 years, the prognosis for spontaneous recovery is poor and consideration should be given to one of the surgical procedures described above. SUPRASCAPULARNERVE Anatomy

The suprascapular nerve is the only peripheral nerve originating from the upper trunk of the brachial plexus (Fig. 2). Fibers are primarily from C5 with some contributions from C6 and C4. The suprascapular nerve crosses the posterior cervical triangle and runs under the trapezius and the omohyoid muscles and then through the suprascapular notch to innervate the supraspinatus muscle. The suprascapular notch is a fibrosseous foramen bridged by the transverse scapular ligament. Within the

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Figure 2. Suprascapular nerve originates directly from the upper trunk of the brachial plexus. It runs through the suprascapular notch (A) to innervate the supraspinatus muscle, then wraps around the spinoglenoid notch (B) to supply the infraspinatus muscle. (From Haymaker W, Woodhall B: Peripheral Nerve Injuries. Philadelphia, WB Saunders, 1953; with permission.)

supraspinatus fossa, the nerve provides sensory branches to the glenohumeral and acromioclavicular joints. The nerve then traverses the spinoglenoid notch at the lateral end of the scapular spine to innervate the infraspinatus muscle. The spinoglenoid notch is frequently covered by the spinoglenoid (or inferior transverse scapular) ligament. Although the suprascapular nerve is generally considered a pure motor nerve, it also provides joint sensation and occasionally a cutaneous sensory branch overlapping in distribution with the axillary nerve.4a Clinical Presentation

The suprascapular nerve can be entrapped at the level of the suprascapular notch or spinoglenoid notch. With entrapment at the suprascapular notch, the primary symptoms are shoulder pain and weakness. The pain is deep and throbbing, located along the superior border of the scap-

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ula with extension toward the shoulder joint, occasionally radiates down the arm.20,77 Maneuvers that adduct the scapula or rotate the head away from the involved shoulder, such as flexing the shoulder while reaching across the chest, exacerbate the pain. Tenderness over the scapular notch is sometimes present. Weakness of the supraspinatus, a shoulder abductor, and of the infraspinatus, a shoulder external rotator, can usually be demonstrated. Occasionally, deltoid muscle atrophy accompanies suprascapular nerve injury because of disuse. In contrast, isolated suprascapular nerve injury at the spinoglenoid notch most often presents with painless atrophy of the infraspinatus and weakness of shoulder external rotation.32 Differential Diagnosis

Because shoulder pain is one of the chief complaints of patients who have suprascapular neuropathy, various musculoskeletal conditions must be considered in the differential diagnosis. These include subacromial bursitis, bicipital tendonitis, rotator cuff tendonitis, rotator cuff tears, impingement syndrome, acromioclavicular joint arthritis, and adhesive capsulitis (frozen shoulder syndrome). Both rotator cuff tears and suprascapular nerve lesions cause weakness of shoulder abduction despite a strong deltoid muscle. Mild atrophy of the supraspinatus or infraspinatus may occur with a rotator cuff tear as a result of disuse rather than nerve injury. A second consideration in the differential diagnosis is a cervical radiculopathy affecting the C5 and the C6 roots in which there is pain felt along the medial border of the scapula, frequently radiating into the arm. Atrophy and weakness of the deltoid and biceps muscles may occur but are usually mild in radiculopathies produced by degenerative joint or disk disease of the cervical spine. Atrophy and weakness are much more pronounced in traumatic injuries to the nerve roots, such as in root avulsion. Neuralgic amyotrophy must also be considered in the differential diagnosis of a suprascapular neuropathy. The supraspinatus and infraspinatus are two of the most commonly involved muscles, and occasionally Some previously reported paare the only muscles affected.28,73,88,99,100 t i e n t ~ ~ " ,who ~ ~ had , ~ ~spontaneous , ~ ~ , ~ ~ suprascapular entrapment neuropathy may actually have had neuralgic amyotrophy. Finally, an axillary neuropathy may present with weakness of arm abduction (deltoid) and lateral rotation (teres minor) similar to that seen with a suprascapular neuropathy. Atrophy of the deltoid muscle and sensory loss over the lateral aspect of the shoulder, however, typically accompany an axillary neuropathy. Electrodiagnostic Evaluation

Demonstration of denervation, by needle EMG, confined to the supraspinatus or i n f r a s p i n a t u ~ is ~ ~the , ~best ~ , ~objective ~ evidence of supra-

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scapular neuropathy." If either of these muscles is denervated, it is essential to sample other C5- and C6-innervated muscles as well as the cervical paraspinal muscles, to exclude a cervical radiculopathy or more widespread brachial plexus lesion.78A motor latency may be measured from Erb's point, recording from the supraspinatus or the infraspinatus muscle with a monopolar needle. For the supraspinatus muscle, the upper limit of normal is 3.7 ms for distances of 7 to 12 For the infraspinatus muscle, the upper limit of normal is 4.3 ms for distances of 10 to 15 Prolonged latencies to affected muscles have been reported in suprascapular n e ~ r o p a t h y . ' ,In ~ ~one , ~ ~case' the significant prolongation of latency was confined to the infraspinatus muscle, pinpointing a distal entrapment site. On the other hand, a normal NCS does not rule out suprascapular nerve entrapment.82,83 Patients who have muscle atrophy because of rotator cuff injuries have normal EDXs. General Diagnostic Tests

The suprascapular notch is seen on anterior-posterior radiographs if the radiograph beam is tilted caudally 15"to 30". Visualization of the notch allows one to look for osteophytes or other bony abnormalities that may entrap the suprascapular nerve. MRI of the shoulder is the imaging study of choice when looking for a ganglion cyst causing suprascapular nerve compression at the spinoglenoid notch. In addition, the MRI allows assessment of rotator cuff integrity and exclusion of a rotator cuff tear from the differential diagnosis. Ganglion cysts are often associated with tears of the superior glenoid labrum (the SLAP lesion), which are sometimes visualized on MRI but may also be associated with false-negative MRI studies. An uncommon diagnostic test is to inject a local anesthetic into the scapular notch, blocking the suprascapular nerve. Pain alleviation after the injection suggests suprascapular nerve entrapment.I7Since the differential diagnosis of suprascapular neuropathies also includes C5-C6 radiculopathies and brachial plexopathies, cervical or brachial plexus MRIs may also assist in making the correct diagnosis. Origin

Of the two potential sites of suprascapular nerve entrapment, the suprascapular and the spinoglenoid notches, the most common is compression or stretching of the nerve in its passage through the suprascapular notch, where it is tethered by its branch to the supraspinatus. Trauma to the shoulder region is a common cause of suprascapular neuropathy.43,55,82,s3,104 Any acute forcible depression of the shoulder, such as that produced by a football tackle or that which occurs with a fall on the point of the shoulder, or repetitive minor depressions may injure the nerve. Fractures at the suprascapular notch, which are unc0mmon,2~or excessive callus formation after a scapular fracture may also compress the

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nerve. Various review^"^^^^^^^ report an incidence of 2% to 35% for suprascapular nerve injury with acute dislocation of the shoulder. But with dislocations, almost all suprascapular neuropathies are associated with additional axillary, radial, or musculocutaneous neuropathies. A 10% incidence of suprascapular nerve injury has been reported after primary repair of massive rotator cuff tears.Io6 In patients who lack a history of direct trauma, the suprascapular nerve may be injured by repetitive motions involving the scapulothoracic and shoulder joints. Persistent or repetitive forced cross-body adduction of the arm may eventually produce suprascapular nerve injury.y2Anatomic observations have confirmed this sling e f f e ~ t , sbecause ~ , ~ ~ movements of the shoulder joint apply traction to the nerve and cause compression against the rigid inferior border of the superior transverse ligament. This mechanism of injury has been reported in a woman vigorously polishing her car for two hourss1and in a postoperative patient reaching across his body to grab an overhead trapeze.y3This mechanism may also be responsible for suprascapular neuropathies in gymnasts, football swimmers, weight lifters, pitchers, and tennis player^.^^,'^^ There have been at least 70 reports of suprascapular nerve entrapment at the spinoglenoid notch by ganglionic c ~ s ~ s . Ganglion ~ ~ , ~ cysts ~ , ~ ~ , ~ typically form after tears of the glenoid labrum, much as Baker's cysts in the popliteal fossa form after meniscal tears. Injury at the spinoglenoid notch may also be caused by repetitive movements that stretch the nerve across the lateral edge of the spine of the scapula. An implicated position is maximum external rotation of the arm with approximately 90" of abduction and 20" of hyperextension. Activities requiring this arm position are the volleyball s e r ~ e ?weight ~ , ~ ~ lifting, and baseball pitchings4Elite level volleyball players have developed asymptomatic atrophy of the infraspinatus, and it is believed that the eccentric contraction of the infraspinatus during the volleyball serve contributes to compression of the nerve near the spinoglenoid Practical Management

In the repetitive microtrauma often seen in athletes, avoiding the offending movement or altering technique generally corrects the problem. Nonoperative therapy consists of range-of-motion exercises for the shoulder, strengthening of the muscles that stabilize the scapula (serratus anterior, rhomboids, trapezius, and levator scapulae), and strengthening of the rotator cuff muscles themselves. Rehabilitation of virtually any shoulder problem should begin with strengthening of the scapular stabilizers so that the rotator cuff muscles have a strong base of support against which they may function. In the setting of a severe suprascapular nerve injury, the shoulder may be unstable because of muscle paralysis; if this is the case, movements such as shoulder depression while lifting weight (as in carrying a heavy suitcase), throwing with the affected arm, and

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reaching far across the body should be avoided as they place the shoulder at risk for subluxation or dislocation. For persistent symptoms unresponsive to nonoperative treatment, surgical exploration may be indicated, with release of the transverse scapular ligament.17,83 In cases of blunt trauma with or without scapular fracture, a period of observation is recommended prior to any surgical intervention, generally 6 months; however, a severe comminuted fracture of the scapula with obvious involvement of the scapular notch may be an indication for earlier surgical exploration with resection of the transverse scapular ligament and neurolysis. When there is clear underlying pathology such as a tumor, early surgical management is important. When a ganglion cyst is present at the spinoglenoid notch, surgical excision has produced excellent results in many cases.40,69,94,10' If rotator cuff pathology is also suspected and shoulder arthroscopy is performed, arthroscopic debridement of the cyst is p ~ s s i b l e .A~ less ~ , ~invasive, ~ yet successful, approach is CT-guided needle aspiration.'O Prognosis

The prognosis for recovery of suprascapular neuropathies caused by blunt trauma, repetitive movements, and neuralgic amyotrophy is excellent with conservative treatment. Martin et aF6 reviewed the results of nonoperative management of 15 cases. Good outcome was observed in 12 of the 15, and the remaining three responded to surgery. This suggests that surgery should only be undertaken when there is a clear pathologic lesion or when conservative therapy fails. Antoniadis et a16 summarized long-term follow-up in 25 cases from various causes treated with surgery after failure of conservative methods: 84%of patients were pain free after surgery, and motor function improved significantly in 86.7% of patients. Similar results are cited by 0 t h e r ~ . ~ ~ , ~ ~ , ~ ~ , ~ 0 ~ AXILLARY NEUROPATHY Anatomy

The axillary nerve is a mixed motor and sensory nerve providing innervation to the deltoid and teres minor muscles and cutaneous sensory fibers to a small area over the lateral aspect of the shoulder (Fig. 3). It is a terminal branch of the posterior cord of the brachial plexus formed from C5 and C6 fibers, running through the upper trunk and posterior cord. At its origin, the nerve travels along the anterior surface of the subscapularis muscle to its lower border where it joins the posterior circumflex humeral artery. Together the nerve and artery turn posteriorly to leave the axilla through the quadrilateral space, which is bounded superiorly by the inferior edge of the teres minor muscle, laterally by the surgical

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Sensory branch'-'

Radial

I

Figure 3. Axillary nerve originates from the posterior cord of the brachial plexus. The nerve innervates the teres minor and deltoid muscles and supplies sensation to the lateral shoulder. (From Haymaker W, Woodhall B: Peripheral Nerve Injuries. Philadelphia, WB Saunders, 1953; with permission.)

neck of the humerus, medially by the long head of the triceps, and inferiorly by the teres major. Distal to the quadrilateral space, a branch is supplied to the teres minor. The axillary nerve then separates into three branches: an anterior branch to the middle and anterior aspects of the deltoid, a posterior branch to the posterior deltoid, and the upper lateral brachial cutaneous nerve, which supplies the skin over the deltoid.

Clinical Presentation

Axillary neuropathies result in a well-defined patch of sensory loss over the lateral shoulder. Weakness and atrophy of the deltoid limit shoulder abduction. Involvement of the teres minor causes mild weakness of shoulder external rotation. The weakness is only partial, because the infraspinatus is a stronger external rotator.

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Differential Diagnosis

The differential diagnosis of a suspected axillary neuropathy includes a lesion of the posterior cord of the brachial plexus, suprascapular neuropathy, a C5 or C6 radiculopathy, and neuralgic amyotrophy. Testing muscles innervated by other branches of the posterior cord, such as the radial nerve, allows a distinction to be made between a posterior cord lesion and an axillary neuropathy. A suprascapular neuropathy may produce a similar pattern of weak arm abduction and external rotation but without any sensory loss. Deltoid weakness may be detected in a C5 or C6 radiculopathy, but involvement of other muscles, radicular pain, or sensory symptoms in the forearm or hand should also be present. Axillary neuralgic amyotrophy and musculoskeletal causes of shoulder pain, including rotator cuff tears, also should be considered in the differential diagnosis.

Electrodiagnostic Evaluation

Axillary motor NCSs can be performed by stimulating at Erb’s point and recording with a monopolar needle or surface electrode over the deltoid. For stimulation at Erbs point with a distance of 15 to 21 cm, the Since axillary neuropupper limit of normal for distal latency is 4.9 athies are usually axon-loss lesions, motor conduction studies do not generally provide more information than may be obtained from EMG. In the setting of an acute nerve injury, however, the amplitude of the CMAP recorded with a surface electrode may give an estimation of the degree of axon loss. Needle EMG is used to demonstrate denervation or reinnervation in the deltoid and the teres minor muscles. If abnormalities are found in these muscles, the electromyographer should test other muscles innervated by the upper trunk and the posterior cord to ensure that the abnormalities found in the axillary-innervated muscles are not part of a more widespread brachial plexus lesion. C5 and C6 muscles not innervated by the axillary nerve and the cervical paraspinal muscles should also be tested to exclude the possibility of a cervical radiculopathy. The sensory branch of the axillary nerve is not routinely studied in the electrophysiology laboratory.

General Diagnostic Tests

When symptoms are caused by trauma, radiographs of the shoulder and humerus should be obtained to exclude the possibility of a fracture or shoulder dislocation. When a cervical radiculopathy is being considered in the differential diagnosis, a cervical spine MRI may be indicated. Vascular quadrilateral space syndrome is diagnosed by arteriography re-

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vealing occlusion of the posterior circumflex humeral artery when the arm is abducted and externally rotated.

Origin

The most common cause of axillary neuropathy is trauma, especially dislocation of the s h o ~ l d e r ~ or ~ rhumeral ~ l , ~ ~ fracture. Axillary nerve injury is a well-known complication of anterior shoulder dislocation because the short course of the nerve around the humeral neck puts the nerve at risk for a traction injury with forward humeral displacement. Toolanen et a196 examined early complications after anterior dislocation of the shoulder and found 35 of the 55 patients had deltoid muscle denervation. The axillary nerve is thought to be the nerve most vulnerable to traction injury of the brachial plexus because it is closely tethered to the deltoid muscle.34 Other traumatic causes of axillary neuropathy include crutch palsy (which also often involves radial nerve injury), intramuscular injection in the posterior shoulder,S1and direct blows to the shoulder girdle or quadrilateral space in athletes who wrestle or play football, rugby, and Axillary neuropathy occasionally follows general anesthesia or sleeping in a prone position with the arms raised above the head.2 Rare cases of entrapment in the quadrilateral space have been reported.'6,21Quadrilateral space syndrome is caused by compression of the posterior humeral circumflex artery or the axillary nerve by associated vessels or hypertrophied muscles and is most common in young athletic individual^.^^ Symptoms develop gradually with intermittent paresthesias in the upper extremity during forward flexion, abduction, or both. External rotation of the arm aggravates the symptoms. The pain is poorly localized to the anterior aspect of the shoulder, and usually there is no weakness. Axillary nerve involvement is common in neuralgic amyotrophy. Deltoid weakness can be demonstrated in 50% of cases. Usually the suprascapular nerve is also affected, but in approximately 10% of patients who have neuralgic amyotrophy, only the deltoid is involved.99

Practical Management

The importance of physical therapy in the management of patients who have nerve injury about the shoulder cannot be overemphasized. Range of motion must be maintained to avoid joint contractures. Conservative treatment is recommended when an incomplete nerve injury is present. If the lesion seems to be complete, the patient should be reexamined with needle EMG in approximately 3 months. The distance from the site of injury to the deltoid muscle is relatively short, so some recovery should be expected within 3 to 4 months. Reinnervation usually occurs first in the posterior portion of the deltoid, so this area should always be

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tested. If there is no evidence of reinnervation, surgical exploration and nerve grafting should be considered. As in other cases of peripheral nerve injury, it is preferable to perform nerve grafting less than 6 months after the onset of the Prognosis A partial nerve injury sustained in association with fracture or dislocation of the head of the humerus usually recovers f ~ l l y . " ,Axillary ~~,~~ nerve injury associated with traction to the brachial plexus, has a less favorable p r o g n ~ s i s . Leffert ~ , ~ ~ and S e d d ~ n noted ~ ~ that six of the nine patients with isolated axillary nerve injury failed to regain full deltoid muscle strength. Berry and Bri19 reported that only two of their eight patients who presented with complete deltoid paralysis regained useful deltoid muscle function. Injury to the nerve by blunt trauma to the shoulder has a variable prognosis. Perlmutter et a174performed long-term followup in athletes who had isolated axillary nerve injury caused by a direct blow to the anterior lateral deltoid. Of seven athletes, three had significant recovery of function with conservative treatment, three had good recovery after surgery, and one had no recovery. Because the axillary nerve is composed primarily of motor fibers and travels only a short distance from its origin to its muscle insertion, it has a good prognosis for functional recovery after surgical Petrucci et a176reported that in 21 patients who underwent nerve grafting, recovery of deltoid strength was extremely rapid and complete in all. MUSCULOCUTANEOUSNERVE Anatomy

The musculocutaneous nerve is a mixed motor and sensory nerve. It innervates three of the elbow flexor muscles (the biceps, brachialis, and coracobrachialis) and provides cutaneous sensory branches to the lateral forearm (Fig. 4). It arises directly from the lateral cord of the brachial plexus, in the upper arm near the inferior border of the pectoralis major muscle. It receives contributions from C5-C7 cervical roots via the upper and middle trunks of the brachial plexus. Contribution from C7 is minimal. The nerve innervates the coracobrachialis at the level of the axilla and pierces this muscle to run in the fascia1 plane between the biceps and brachialis muscles. In the region of the elbow, this nerve runs deep to the brachial fascia, over the brachialis muscle. Distal to the elbow, the terminal extension of the musculocutaneous nerve continues as the lateral antebrachial cutaneous sensory nerve. In the forearm, this nerve becomes subcutaneous and separates into two terminal divisions, anterior and posterior, to supply sensation to the lateral half of the forearm to the level of

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Musculocutaneous n. Coracobrachialis

I M.

.::- Biceps

brachii

Figure 4. Musculocutaneous nerve originates from the lateral cord of the brachial plexus. The nerve innervates the biceps, brachialis, and coracobrachialis muscles. It continues distal to the elbow as a pure sensory nerve, providing sensation to the lateral forearm. (From Haymaker W, Woodhall B: Peripheral Nerve Injuries. Philadelphia, WB Saunders, 1953; with permission.)

the wrist. The musculocutaneous nerve is relatively fixed where it pierces the coracobrachialis muscle and at the point where it exits through the deep fascia at the elbow. It is vulnerable to traction at these sites. Clinical Presentation

The signs and symptoms of a musculocutaneous neuropathy depend on the location of the nerve injury. The coracobrachialis muscle flexes and adducts the shoulder and stabilizes the head of the humerus in the glenoid fossa. The brachialis and biceps are flexors of the elbow. The biceps brachii also supinates the forearm and flexes the arm at the shoulder. Proximal

PROXIMAL NEUROPATHIES OF THE UPPER EXTREMITY

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involvement of the nerve causes weakness of elbow flexion, an absent biceps reflex, and sensory loss in the lateral forearm. But some supination and elbow flexion may still be possible because the supinator and brachioradialis muscles contribute to supination; the brachioradialis, extensor carpi radialis longus, and pronator teres muscles contribute to elbow flexion. Because of extensive overlap in cutaneous sensory nerve territories, lesions of musculocutaneous nerve may only result in a narrow band of sensory loss along the lateral aspect of the volar forearm. The lateral antebrachial cutaneous nerve may become entrapped at the elbow, between the biceps tendon or fascia and the brachialis muscle. Pain in the cubital fossa is the presenting complaint and is exacerbated by arm pronation and elbow extension. The nerve may be tender to palpation at the elbow. Acutely, the patient may note a burning dysesthesia along the radial aspect of the volar forearmxand mild limitation of elbow extension when the elbow is in complete pronation. The fully pronated position places maximal tension on the nerve, thus exacerbating pain. Differential Diagnosis

A ruptured biceps tendonI3 presents with weakness of forearm flexion, but the biceps muscle can be seen contracted into a small hard ball. C5 or C6 radiculopathies may produce biceps weakness, but denervation or weakness of other muscles (infraspinatus, brachioradialis, deltoid, paraspinal muscles) should be present as well as radicular pain and sensory symptoms in the hand. With a musculocutaneous nerve injury, sensory deficits are not present distal to the wrist. Brachial plexus injuries involving the lateral cord have involvement of median sensory fibers in the hand in addition to a musculocutaneous neuropathy. Occasionally, patients who have compression of the lateral antebrachial cutaneous nerve are misdiagnosed as having refractory lateral epicondylitis (tennis elbow) or median-nerve compression.xMuscles innervated by the musculocutaneous nerve are frequently involved in neuralgic amyotrophy, but weakness is rarely limited solely to the distribution of the musculocutaneous nerve. Electrodiagnostic Evaluation

The goal of the EDX study is to demonstrate isolated involvement of the musculocutaneous nerve and to exclude a brachial plexopathy or cervical radiculopathy. The most important NCS is the lateral antebrachial cutaneous sensory study. This sensory potential can be elicited by stimulating just lateral to the biceps tendon at the elbow and recording over the nerve approximately 12 cm distally along a line connecting the stimulation point to the radial pulse.x9With this technique, the onset latency was 1.8 ? 0.1 ms (range 1.6 to 2.1 ms) and the conduction velocity was 57 to 75 m/s. The mean amplitude was 24 +- 7.2 pV with a range of 12

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to 50 pV. This sensory response may be technically difficult to obtain in older or obese individuals. Therefore, if the response is absent or has a low amplitude, it should be compared with that from the uninvolved arm. Both distal and proximal nerve involvement result in an abnormal lateral antebrachial cutaneous NCS. When abnormalities are present, it is important to perform other sensory NCS, especially those in which fibers that pass through the lateral cord or upper trunk (median to the thumb, radial) are tested. Abnormalities in these sensory potentials suggest more widespread brachial plexus involvement or neuropathy. Proximal motor NCSs can be performed by one's stimulating at the axilla and Erb's point and recording with either a monopolar needle or surface electrodes over the biceps m u s ~ l e When . ~ ~ , surface ~~ electrodes are used to record the CMAP, the amplitude may be compared side to side to assess the degree of axon loss, and between Erbs point and the axilla, to look for conduction block. Needle EMG is normal in musculocutaneous neuropathies at the elbow. In proximal lesions, there is denervation, reinnervation, or both in the biceps. The brachialis and coracobrachialis can also be examined but are more difficult to localize and offer little additional information, except in suspected entrapment of the nerve in the coracobrachialis muscle, in which case, denervation would be expected in the brachialis and biceps muscles but not in the coracobrachialis. If abnormalities are found in the biceps, other upper-trunk-innervated muscles should be examined to ensure that the abnormalities are not part of a more widespread lesion. Examination of the cervical paraspinal muscles helps exclude the possibility of a C5-C6 radiculopathy. General Diagnostic Tests

Radiographs of the elbow may be indicated to look for other causes of antecubital fossa pain such as bone spurs or degenerative joint disease. MR imaging of the cervical spine may also occasionally be helpful. Origin

Proximal isolated musculocutaneous neuropathies are r a ~ e . 'More ~,~~ commonly, they occur with widespread traumatic lesions of the shoulder or upper arm, especially fractures of the proximal humerus. Livesodl described five cases of isolated musculocutaneous nerve injury from shoulder dislocation. One case was reported after midclavicular f r a c t ~ r e . ~ Postoperative musculocutaneous nerve injury was observed in 3 of 54 cases of fracture of the lateral clavicle that were treated by transposition of the coracoid process onto the cla~icle.'~ The transposition of the coracoid process with its attached muscles probably caused a stretch injury of the musculocutaneous nerve at the site of its passage through the coracobrachialis muscle.

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It has been suggested that musculocutaneous nerve injuries occur where the nerve pierces the coracobrachialismuscle. It is relatively fixedIo7 at this site and can be injured, either from nerve stretch distal to where it is tightly anchored or as a result of pressure produced by vigorous, intermittent coracobrachialis muscle contractions or chronic muscle hypertrophy. This mechanism is suspected in musculocutaneous neuropathies occurring after heavy weight liftingI3 or after violent extension of the forearm such as occurs when falling on an outstretched hand with elbow hypere~tended.~ Entrapment , ~ ~ , ~ ~ of the nerve at the coracobrachialismuscle may also be the mechanism of musculocutaneous nerve injury after surgical procedures requiring abduction and external rotation of the arm.29 Alternatively, EwingZ9proposed that, based on cadaver studies, the actual mechanism of injury during surgery was stretching of the brachial plexus, with the musculocutaneous nerve particularly susceptible to injury. Injury to the musculocutaneous nerve more commonly occurs with entrapment of the distal sensory branch at the elbow between the biceps tendon or fascia and the brachialis muscle. The lateral free margin of the biceps aponeurosis compresses the musculocutaneous nerve. The compression force is accentuated when the forearm is fully pronated. Injury to the lateral antebrachial cutaneous nerve has been reported with a number of repetitive activities, including inserting 3000 screws in a single weekends and playing tennis. Compression of the lateral antebrachial cutaneous nerve may also occur where the nerve assumes its subcutaneous superficial position. Injury has been reported as being caused by the strap of a heavy a waitress's tray,Io5and during v e n i p u n c t ~ r e . ~ ~ ~ ~ Practical Management

Initial conservative therapy includes restriction of precipitating activities and oral anti-inflammatory agents. If conservative therapy fails, further treatment recommendations depend on the site of musculocutaneous nerve injury. If nonoperative therapy fails to alleviate symptoms of entrapment at the elbow, surgical decompression is suggested with excision of a triangular wedge of biceps tendon directly over the nerve. This procedure has produced excellent results.8 When there is a more proximal injury to the nerve with severe axon loss and failure of recovery within 6 months, surgery is recommended to reinnervate the paralyzed biceps muscle and provide some elbow flexi ~ nA .variety ~ ~of ~nerves ~ ~have been used as grafts for the musculocutaneous nerve (pectoral, thoracodorsal, intercostal, spinal accessory, ulnar). The outcome of nerve-grafting procedures becomes progressively ' ~cases , ~ ~ for worse when delayed more than 6 months p o s t i n j ~ r y . ~ ,In which surgery is delayed for more than 6 months, a free muscle transfer innervated by an intercostal nerve may be the best ~ p t i o nSurgical .~ procedures should only be performed after needle EMG demonstrates complete absence of axonal continuity to the biceps muscle, thereby excluding the possibility of spontaneous recovery.

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Prognosis Most isolated musculocutaneous neuropathies, particularly those caused by stretch injuries or neuralgic amyotrophy, are incomplete and respond to conservative therapy with good recovery. Severe proximal injuries of the musculocutaneous nerve, treated with nerve-grafting or neurotization techniques, have a more variable outcome, with an estimated 64% of patients regaining functional elbow flexion 2 years after surgery.h4,ss Residual sensory loss in all types of musculocutaneous neuropathies is common.

SUMMARY

Isolated lesions of the proximal nerves of the shoulder and arm, including the long thoracic, suprascapular, axillary, and musculocutaneous nerves, are uncommon. These nerves are more commonly injured in combination by trauma or in idiopathic brachial neuritis (neuralgic amyotrophy). The evaluation of these mononeuropathies relies heavily on electrodiagnostic testing, particularly needle EMG, because most are axon-loss lesions. The differential diagnosis of each of these mononeuropathies includes cervical radiculopathy, brachial neuritis, and soft-tissue injury to the shoulder girdle. As with all nerve injuries, prognosis for recovery of function depends on the extent of axon loss.

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Address reprint requests to Kimberly L. Goslin, MD, PhD Department of Neurology L226 Oregon Health Sciences University 3181 SW Sam Jackson Park Road Portland, OR 97201 e-mail: [email protected]