- Email: [email protected]
Idiopathic Neuralgic Amyotrophy: An Illustrative Case Report
CASE REPORTS IDIOPATHIC NEURALGIC AMYOTROPHY: AN ILLUSTRATIVE CASE REPORT George D. W. Rix, DC,a Edward H. Rothman, DC,b and Aidan W. D. Robinson, MSc(Chiro)c
ABSTRACT Objective: To describe the case of a patient diagnosed with neuralgic amyotrophy (NA) illustrating pertinent aspects of differential diagnosis, the use of clinical neurophysiological procedures to aid in establishing the diagnosis, and issues of management. Clinical Features: A 39-year-old male soldier presented with a rapid onset of marked loss of left shoulder movement. This started acutely early one morning as a sharp, severe lower neck pain progressing over the following 2 weeks to a less severe dull ache in the left shoulder and arm. Pain was rapidly replaced with weakness. Physical examination and electrodiagnostic investigation helped establish a diagnosis of NA. Intervention and Outcome: The patient was reassured that this is normally a self-limiting condition. Range of motion exercises progressing to a strengthening program was prescribed. He was progressing well; however, we lost contact because of his commitments in the armed service. Conclusion: When a patient presents with shoulder and arm pain of neurogenic origin, NA should be a consideration. Differentiating NA from radiculopathy is especially important in making management decisions. With a careful history and physical examination, the diagnosis may be made without the need for ancillary investigations. Neuralgic amyotrophy is a self-limiting condition requiring reassurance and monitoring. (J Manipulative Physiol Ther 2006;29:52-59) Key Indexing Terms: Brachial Plexus Neuropathies; Amyotrophy, Neuralgic; Radiculopathy
I
diopathic neuralgic amyotrophy (NA) is a rare disorder of unknown etiology that mimics many common conditions with acute pain and weakness around the shoulder. This condition has several confusing descriptors, including acute brachial neuritis/plexitis/neuropathy/radiculitis and shoulder girdle neuritis/syndrome.1 - 3 Parsonage and Turner coined the term neuralgic amyotrophy in the late 1940s.4 Subsequently, some clinicians refer to the condition as Parsonage-Turner syndrome.5 The term neuralgic amyotrophy works well as a descriptor because it does not presume a clear etiology and site of pathology, yet describes a
Senior Clinical Tutor, Anglo-European College of Chiropractic, Bournemouth, UK. b Senior Clinical Tutor, Anglo-European College of Chiropractic, Bournemouth, UK. c Private Practice of Chiropractic, Doncaster, UK. Sources of support: No external funds were provided for this research. Submit requests for reprints to: George Rix, DC, AngloEuropean College of Chiropractic, 13-15 Parkwood Rd., BH5 2DF Bournemouth, UK (e-mail: [email protected]). Paper submitted July 13, 2004; in revised form July 7, 2005. 0161-4754/$32.00 Copyright D 2006 by National University of Health Sciences. doi:10.1016/j.jmpt.2005.11.008
52
the clinical presentation.1,3,4,6 Characterized by severe pain followed by muscle weakness, atrophy, and variable sensory deficits, the diagnosis is made from the history and physical examination findings and confirmed by clinical neurophysiology testing. Although NA is a quite well-defined entity, establishing the diagnosis can be challenging, particularly as the presentation is considerably more diverse than generally appreciated.3 Consideration is often given to nerve root lesions, primarily C5.6 Other neurological diagnostic considerations within the peripheral neural axis include traction and compressive lesions of the brachial plexus that may affect one or several nerves, including one of the most devastating injuries for athletes, suprascapular nerve entrapment. However, a careful history is often diagnostic. Fortunately, nerve injuries involving the shoulder are uncommon. However, it is important that the clinician differentiates peripheral nerve injuries from lesions affecting the brachial plexus and proximal lesions resulting in radiculopathy. The latter differentiation is especially important to avoid unnecessary therapeutic interventions, such as surgery for coexisting cervical spondylotic changes in a patient.6 An in-depth understanding of peripheral nervous system conditions affecting the shoulder and
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
Fig 1. Moderate atrophy of the left shoulder girdle. Note loss of left deltoid and biceps bulk as compared with the right arm. Some atrophy of the left triceps appears as well.
Rix et al Neuralgic Amyotrophy
Fig 3. Moderate atrophy of the left anterior shoulder girdle. Note loss of left deltoid and biceps bulk as compared with the right arm. There appears to be a mild asymmetry of the pectoralis major muscles. This could be confused with atrophy, but in most cases, it is a simple anatomic variation.
Fig 2. Moderate atrophy of the left posterior shoulder girdle. Note loss of left deltoid bulk as compared with the right arm. There is winging of the left scapula. As in the lateral photographic view, the left triceps appears thinner than the right.
neurological localizing skill is integral to appropriate diagnosis and management. We present the case of a patient with an acute onset of left shoulder pain to illustrate pertinent aspects of differential diagnosis, the use of clinical neurophysiological procedures to aid in establishing the working diagnosis, and issues of management. Neuralgic amyotrophy is often a self-limiting phenomenon that requires nothing more than monitoring for a period of time, range of motion exercises, followed by a strengthening program. However, there are instances when recovery does not occur or is incomplete. Also, possibilities of more serious conditions require careful evaluation and critical thought illustrating the need for careful observation and monitoring.
CASE REPORT A 39-year-old male British Army physical trainer presented to the teaching clinic of Anglo-European College
Fig 4. Marked loss of left shoulder abduction. Note hiking of the shoulder during attempted abduction secondary to loss of primary and secondary muscle action. of Chiropractic complaining of a rapid onset of marked loss of left shoulder movement. Problems with his left shoulder began 3 weeks before his initial clinic visit when he reported waking up at 4:00 am with a sharp pain in the left lower neck. He tried using an ice pack and applying an ibuprofenbased topical gel, which provided no relief. Over the following 24 hours, the sharp pain changed in character to a slightly less severe dull ache. Over the following 2 weeks, the dull ache spread into the left shoulder and arm, stopping at the elbow. Various medications prescribed by an Army medical officer, including aspirin, a paracetamol (acetaminophen) and codeine preparation, and diazepam, oral corticosteroid, and amitryptilline, provided no relief or change in
53
54
Rix et al Neuralgic Amyotrophy
Journal of Manipulative and Physiological Therapeutics January 2006
Table 1. Results of clinical neurophysiology examination Anglo European College of Chiropractic Clinical Neurophysiology Laboratory 13-15 Parkwood Road Bournemouth, BH5 2DF Clinic Tel: (01202) 436222
Patient: DR Date: 16-05-01 Clinical Concern: Atrophy and Weakness Left Shoulder Girdle
Upper extremity nerve conduction studies performed after warming of extremities. NR, no response. Motor and sensory amplitudes are measured baseline to peak. Sensory latencies are measured to peak whereas motor latencies are measured to initial negative onset. DSL, Distal sensory latency; S Amp, sensory amplitude; DML, distal motor latency; M Amp, motor amplitude; NCV, nerve conduction velocity; BE, below elbow; AE, above elbow.
Nerve R L R L R L R L
Lateral cutaneous antebrachial at 12 cm Lateral cutaneous antebrachial at 12 cm Musculocutaneous Musculocutaneous Axillary Axillary Long thoracic Long thoracic
DSL (ms)
S Amp (lV)
2.68
16.0
2.39
33.0
DML (ms)
M Amp (mV)
NCV (m/s)
4.16 4.99 3.53 4.78 3.74 4.16
6.050K 0.850K 5.000K 0.450K 1.000K 0.450K
67.30 54.08 50.90 41.80 66.77 55.28
F wave (ms)
Electromyography using a sterile disposable concentric needle electrode. Ins activity, Insertional activity (n = normal); PSW, positive sharp wave; Fib, fibrillation potential; 0 = absent, 1+ minimal to 4+ maximal; LT, long trains; FASC, fasciculation potential; CRD, complex repetitive discharge; MYK, myokymic discharge; MYT, myotonic discharge; NMT, neuromyotonic discharge. Spontaneous activity
Voluntary
Muscle side
Ins activity
PSW
Fib
Other
MUAP
Recrt
L Deltoid L Biceps L Supraspinatus L Infraspinatus L Teres major L Cervical paraspinal
Incr N N N N N
1+ 2+ 0 2+ 0 0
2+ 2+ 1+ 3+ 1+ 0
FASC FASC 0 0 0 0
N N N N Sparse
Incomp Incomp Incomp Incomp Incomp
the symptoms throughout this time. During the following week, the pain subsided. On the initial visit, the patient noted the dull ache in the neck, shoulder, and arm had disappeared. He reported significant difficulty in flexing and abducting his left shoulder. He denied any recent history of trauma to the area. The day before the incident of sharp pain, he engaged in his usual exercise routine at the gym that included 20 minutes of stationary cycling and 5 sets of 5 repetitions of 50-kg clean and jerk lifts. His medical history was noncontributory with only a few incidents of exercise related low back pain, right fibular fracture, right knee anterior cruciate injury, and tonsillectomy. He was taking no medications at the time of examination. The complete review of systems was unremarkable. On examination, he appeared to be a generally wellmuscled man in no acute distress. All vital signs were well within normal limits. He had good posture, although the left trapezius muscle appeared taut. There was moderate atrophy of the left shoulder girdle, especially considering his excellent muscle tone and bulk (Figs 1 -3). Occasional
fasciculations were observed in the left biceps and deltoid muscles. These were more pronounced on percussion of the muscles. He had a normal gait. Upper and lower extremity muscle stretch reflexes were present and symmetric with the exception of the left biceps, which was diminished as compared with the right. There was no clonus at the ankles. Plantar reflexes were flexor. Muscle strength in the lower extremities was 5/5. Motor examination of the upper extremities revealed 3/5 weakness of the left teres minor, deltoid, and serratus anterior; 4/5 weakness of the left biceps, brachioradialis, and infraspinatus; and 4/5 weakness of the left supraspinatus. There was only slight give-way of the left flexor carpi ulnaris. The remainder of the left shoulder girdle and the right upper extremity muscles were 5/5. Gross sensory examination of all four extremities to sharp and soft touch was intact. Cervical ranges of motion were full and unencumbered. Cervical compression tests, including all variants, were unproductive. There were marked limitations of left shoulder ranges of motion, with loss most evident in abduction to 608 and flexion to 458 (Fig 4). Full movement of the left shoulder was obtained
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
Rix et al Neuralgic Amyotrophy
Table 2. Typical clinical features of idiopathic NA Incidence Male:female Age of onset Etiology Antecedent or associated illness Initial symptom
Mode of onset Weakness Sensory deficit Patterns and distributions of neurological insult
Other neurological findings Laterality Laboratory Electrodiagnosis
Approximately 1.5 per 100 000 Reports vary from 2:1 to 11:1 3 mo to 75 y; highest incidence in the third and seventh decades Exact cause unknown; postulated factors include trauma, infection, viral diseases, unfamiliar strenuous exercise, immunization, autoimmune mechanisms, and surgery Antecedent febrile illness in approximately 25% of patients Pain (severe) in 95% of patients often aggravated by extremity movement; location: in or around the shoulder girdle (possibly related to the region of nervous system affected), may radiate from the shoulder down into the lateral arm or up along the neck; quality: lancinating, sharp, burning, throbbing, boring severe ache; progression: intense pain may persist for a few hours to 3 weeks, often replaced by musculoskeletal pain and dysfunction Sudden, sometimes awakening patient during the night Usually occurs after the pain subsides although there can be an overlap (can occur simultaneously with onset of pain): 70% in 2 weeks, 85% within first month after symptoms begin Variable frequency reported; usually incomplete, less marked than motor deficits; correlates with affected nerves Flaccid paresis associated with wasting (lower motor neuron lesion)—most commonly evident in deltoid, supraspinatus, infraspinatus, serratus anterior, biceps, triceps, and wrist and finger extensors; categories: (1) mononeuropathy, (2) combined mononeuropathy, and plexopathy (least common); nerves affected: primarily the axillary, suprascapular, long thoracic, and musculocutaneous nerves Tendon reflexes may be diminished depending on site of lesion/s; occasionally, fasciculations are present Unilateral, 66% (right side 54%); bilateral, 34% (onset and presentation are usually asymmetric); no correlation with hand dominance Normal Aids in establishing diagnosis by localizing the lesion/s; NCS: median and ulnar velocities usually normal; CMAPs from proximal muscles show abnormalities in 50% of patients (however, helps to rule out other conditions); CMAP amplitudes may be diminished indicating axonal loss; needle EMG: more helpful than NCS in localizing the lesion/s
Table created from information from References [1] and [2]. NCS, Nerve conduction studies; EMG, electromyography.
passively. There were full active ranges in all directions of the right shoulder. The results of electrodiagnostic studies are shown in Table 1. Nerve conduction studies of the musculocutaneous, axillary, and long thoracic nerves were carried out bilaterally with stimulation at Erb point. Compound motor action potential (CMAP) amplitudes for the musculocutaneous, axillary, and long thoracic nerves were markedly decreased on the left. The left musculocutaneous CMAP amplitude was 14%, the axillary amplitude was 9%, and the long thoracic amplitude was 45% of the respective right counterpart. There was mild slowing of the distal motor latencies for these nerves with decreased nerve conduction velocities. Sensory nerve action potentials were also obtained for the lateral cutaneous antebrachial nerve bilaterally. The sensory latencies and amplitudes were normal. Electromyography of the left shoulder girdle was completed with a concentric needle electrode. Increased insertional activity, occasional positive sharp waves, 2+ fibrillation, and fasciculation potentials were noted in the deltoid muscle. There were 2+ positive sharp waves, fibrillation potentials, and fasciculation potentials noted in the biceps muscle. Rare fibrillation potentials were evident in the supraspinatus and teres major muscles. Examination of the infraspinatus muscle revealed trains of positive sharp waves and 3+ fibrillation potentials. Recruitment patterns were incomplete for all of these muscles.
Because the patient was being cared for in a teaching clinic, a fifth-year student intern first assessed the patient. Before consultation with clinical tutors and electrodiagnosis, the intern considered a C5 radiculopathy. However, considering the onset and progression, including the rapid resolution of pain, lack of sensory signs or symptoms, distribution and severity of muscle involvement, lack of cervical spine findings, and inability to provoke symptoms with cervical compression tests even with consideration of pain absence, the presumptive diagnosis became idiopathic NA. The electrodiagnostic studies revealed a motor axonal neuropathy affecting multiple peripheral nerves around the shoulder. This could be classified as a mononeuropathy multiplex. Axonal loss was evident for the left musculocutaneous, axillary, and long thoracic nerves. Acute denervation potentials were noted in multiple sites of the left shoulder girdle. Because idiopathic NA is usually a selflimiting problem, the patient was reassured. Because of his Army status, he returned to his base for rehabilitative management with our recommendation for range of motion exercises progressing to a strengthening program. A report was sent to his medical officer with the suggestion that his condition be monitored. On follow-up, he was making good progress. However, he was keen to undertake rehabilitative exercise to maximize the probability of regaining mobility and strength as quickly as possible. Unfortunately, because of his
55
56
Rix et al Neuralgic Amyotrophy
commitments as a member of the armed forces, we lost contact with him for further follow-up.
DISCUSSION This case reflects the typical presentation of idiopathic NA (Table 2). The diagnosis was suggested because the patient was seen in the subacute setting at a time when the classic features had already evolved and a reasonably obvious nonradicular pattern of weakness and atrophy had developed. However, if a patient presents soon after onset when pain is the predominant feature, the diagnosis of NA can be challenging.2 The potential differential diagnoses for the patient with acute severe pain in or around the shoulder covers a reasonably broad range of musculoskeletal and neurological conditions.7,8 Consideration must also be given to visceral causes of pain. When there is exacerbation of pain with shoulder movements, visceral causes are improbable. The list of possible differential diagnoses narrows more definitively as neurological symptoms and signs emerge. A careful history, even in the acute phase, often reveals features indicative of a neurological process. Cervical spine radiculopathy is usually the first neurological consideration in the acute painful phase, particularly when weakness and paresthesia are reported. Differentiation based on pain distributions alone is difficult because many patients with radiculopathy do not present with pain following a discrete dermatome pattern.9 While nerve root disorders are often misdiagnosed or unrecognized, the emergence of the neurological signs as the condition progresses may lead to a misdiagnosis of cervical spine radiculopathy.10 This differentiation is particularly important to avoid unnecessary investigations and inappropriate therapeutic or surgical interventions.6 A key differential diagnostic feature is the provocation of pain or paresthesia with variants of cervical compression maneuvers. Although strongly suggestive of cervical radiculopathy, head movements and compression tests do not increase the pain associated with NA. However, as in this case, it is not uncommon for patients with NA to experience exacerbation of pain with shoulder movement. This may represent mechanical provocation of sensitized neural tissues distal to the nerve root. However, shoulder and arm movements may affect pain levels in some cases of cervical radiculopathy. For instance, abduction of the arm may relieve radicular pain, that is, arm abduction sign. In this patient, the neurological deficits could be mistaken for a C5 radiculopathy. Although the C5 root level is common to all the muscles affected, a root lesion does not manifest weakness in as broad a distribution as seen in this patient. This is especially evident with the serratus anterior weakness, not seen in a C5 lesion. Another confusing localizing issue may be an absent or
Journal of Manipulative and Physiological Therapeutics January 2006
diminished muscle stretch reflex. In this case, the left biceps reflex was diminished. In isolation, this is consistent with a C5 or C6 root lesion. Assuming NA is a mononeuropathy multiplex, a reflex (C5-7) can be absent or diminished if the process involves the radial or musculocutaneous nerves. In this case, involvement of the musculocutaneous nerve produced the physical examination results. In addition, a radiculopathy was less likely with the absence of peripheral symptom generation caused by nerve root provocation tests such as cervical compression maneuvers. Cervical spine special imaging may be helpful in appreciating anatomic changes that may result in radiculopathy. These changes must be interpreted in the context of the clinical picture and moderated by an appreciation of the occurrence of these findings in asymptomatic subjects. The demonstration of an imaging study abnormality does not automatically imply causality. For instance, in a patient with NA, there exists the possibility of asymptomatic cervical spine imaging abnormalities appearing to affect the nerve root, such as spondylotic changes with encroachment of the intervertebral foramen, especially when occurring at multiple levels.11 Furthermore, in the authors’ experience, not all clinical presentations strongly suggestive of cervical radiculopathy have clear correlative imaging findings. This may suggest a chemical rather than mechanical compressive factor producing the radicular symptoms and sensitization of the dorsal root ganglia.12 When obvious weakness and perhaps atrophy accompany the acute pain, a lack of clear nerve impression on imaging is more helpful in lowering the probability of a root cause. As an investigation procedure, electromyography produces a variable diagnostic yield in differentiating cervical radiculopathy from NA. Results are dependent on the severity of the neural damage, timing of the investigation, and skill of the examiner.1,6 Electromyography commonly shows spontaneous electrical activity in the paraspinal muscles in radiculopathy but is normal in NA because the posterior dorsal rami nerves are not involved in this condition. Although trauma and unaccustomed strenuous activity have been cited as possible etiological factors in NA (Table 2), direct trauma is not readily identifiable as part of the clinical picture. A consideration when there is a history of trauma is a true brachial plexus or peripheral nerve injury. History and descriptions are important in developing likely differential diagnostic scenarios. Injuries to the brachial plexus in the supraclavicular fossa are unusual in the athlete.13 The incident is highest, outside of birth trauma, in young men engaged in manual labor.14 True supraclavicular brachial plexus injuries may have mixed central nervous system and peripheral nervous system features because there is a high incidence of rupture or preganglionic injury to spinal nerves.14 The fifth and sixth nerve roots may be involved. The injury can be devastating
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
and carries a varied prognosis for full recovery. Pain proximal to the plexus begins immediately in at least one half of the cases.14 The pain has various descriptors but is often described as constant intense burning or crushing and may involve the forearm and hand, although this is not a common presentation. Injuries involving the lower plexus are often the result of traction on the arm or compressive due to direct trauma or tumors from the lung apex. The intrinsic hand muscles are often involved and, therefore, the examiner may appreciate weakness and atrophy. Sensory changes are most commonly limited to the medial forearm and hand because of ulnar nerve involvement. Peripheral nerve lesions may be the most difficult to distinguish from NA.3 Nerves crossing the shoulder may be injured, especially in an athlete. The musculocutaneous, axillary, long thoracic, suprascapular, and spinal accessory nerves can be injured from a concussive traumatic event, single strain force, or multiple strain forces. Signs and symptoms can vary from mild neuropraxia to axonotmesis. Fortunately, most injuries are neuropraxic,13 that is, a conduction block within an intact nerve. Therefore, prognosis for complete recovery is excellent. Although axonotmesis is a serious injury with distal axonal degeneration, the connective tissues remain intact and expectations for full recovery are good, albeit with prolonged healing time. Neurotmesis or complete nerve disruption is usually secondary to high-energy trauma and penetrating injuries has a poor prognosis for recovery. Differential diagnosis of peripheral nerve injuries requires a knowledge base that includes a detailed understanding of anatomy. For instance, the axillary nerve, which is the most frequently injured peripheral nerve around the shoulder,13 passes through the quadrilateral space near the inferior portion of the joint before dividing into anterior and posterior branches to supply the anterior and posterior deltoid muscles, respectively. Smaller branches supply the teres minor muscle and innervate the skin over the deltoid insertion. There are several fixation points of the nerve making it prone to throwing injuries. Symptoms, especially initially, are vague, making it difficult to accurately diagnose. The clinical picture is not unlike a nonneurogenic shoulder injury. Meticulous palpation of the deltoid muscle is required to appreciate decreased firing activity and atrophy. Another example of the difficulty in isolating an injured nerve about the shoulder is entrapment of the suprascapular nerve. Formed from branches arising from the C5 and C6 nerve roots, it comes off the upper trunk of the plexus and traverses laterally passing through the suprascapular notch. Motor branches supply the supraspinatus and infraspinatus muscles. Afferent branches cover the posterior capsule and areas over the acromioclavicular joint. Interestingly, there are still reports in the literature that there are no surface cutaneous branches.13 However, cutaneous innervation has been reported and commented on for 20 years.15 Considering its course and sites of fixation, it is prone to traction
Rix et al Neuralgic Amyotrophy
and compressive injuries. Shoulder pain with numbness over the superior aspect of the shoulder may suggest an injury to the suprascapular nerve and prompt the examiner to search for this possibility. Surgical decompression may be necessary for recovery.15 It may be difficult to differentiate NA from entrapment of the suprascapular nerve. Timing is a consideration because most cases of NA resolve within 6 weeks. A better method of differentiation is electromyography because in NA, spontaneous activity will be present in shoulder muscles beyond the supraspinatus and infraspinatus muscles. Other considerations for a differential diagnosis of peripheral mononeuropathy about the shoulder are the musculocutaneous, long thoracic, and spinal accessory nerves. As noted above, a detailed understanding of anatomy is important in these cases. Injuries to the musculocutaneous nerve present with weakness and atrophy of the biceps and brachioradialis muscles; therefore, elbow flexion is often compromised to some degree. True scapular winging, compromised scapular rhythm, and atrophy of the serratus anterior muscle are hallmark signs of a long thoracic nerve lesion.16 Winging of the scapula may also be present in spinal accessory nerve lesions because the trapezius muscle aids in stabilization of the shoulder and rotation against the posterior thoracic wall. However, the patient with a lesion to the spinal accessory nerve will also present with posterior shoulder ache and, most likely, a dropped shoulder on the involved side with atrophy of the trapezius.16 Again, electromyographic evaluation offers invaluable help in the differential diagnosis. In young patients such as the one reported here, consideration in the differential diagnosis may be given to hereditary neuropathies, such as hereditary neuropathies with liability to pressure palsies (HNPP) and hereditary NA. However, these conditions are rare. For example, only 100 cases of hereditary NA have been reported since first recognized in 1886.17 Both conditions are benign and autosomal dominant. Symptoms of HNPP start in the second or third decade. Hereditary NA has variable upper limb weakness and pain whereas HNPP rarely has any associated pain, which contrasts with the typical presentation of NA. Brachial plexus involvement shows up in many of the cases in electrophysiological studies without evidence of a generalized neuropathy.17 In most cases, electrophysiological examination is unnecessary. Electrodiagnostic evaluation in a patient with suspected NA is usually undertaken when there is some ambiguity in the clinical picture to tease out any possible concomitant neurogenic conditions, to avoid unnecessary surgical intervention, and to increase confidence levels in advising the patient on the natural history. These studies commonly include nerve conduction and needle electromyography. As with the investigation of patients with suspected cervical radiculopathy, electrophysiological studies may be inconclusive. However, in the differential
57
58
Rix et al Neuralgic Amyotrophy
diagnosis of nerve lesions about the shoulder, electromyography is the best way to localize the lesion.1 Evoking and recording compound muscle action potentials for deltoid, biceps, and serratus anterior muscles and the lateral antebrachial cutaneous reveals abnormalities in only approximately 50% of the cases of NA.1 Electromyography sampling allows localization of the lesion to specific muscles, generally in 3 patterns, that is, mononeuropathy, plexopathy, and mononeuropathy combined with plexopathy.1 Sampling of shoulder girdle muscles innervated by the same and different nerves and cervical paraspinal muscles should be included in the examination. Distal muscles should not be routinely done but considered if a cervical radicular process appears possible. However, it is rare that paraspinal muscles are involved.1,2 Therefore, spontaneous activity in these muscles strongly suggests nerve root involvement. Evoked potentials may reveal conduction slowing. More importantly, the surface recording of CMAPs with amplitude measurements is useful in determining the extent of axonal loss. There is controversy on localization of the lesion in NA. Not all studies/case reports provide electrophysiological data. Those that have provided data suggest a mononeuropathy multiplex.3,18 In this case, there was no electromyographic evidence of spontaneous paraspinal activity confirming the clinical impression that radiculopathy was unlikely. For this patient, nerve conduction studies and electromyography categorized the lesion to a likely combined mononeuropathy and plexopathy as opposed to a plexopathy alone or mononeuropathy.1 It also provided some quantification of the degree of axonal loss. Another ancillary examination that may have value in the acute and subacute stages is magnetic resonance imaging (MRI) of the involved muscles. T2-weighted fast spin echo images may reveal high signal intensity of the affected muscles related to neurogenic inflammation. During the chronic phase, a T1-weighted spin echo image may show muscle atrophy.6,19,20 Although interesting, there is often little additional clinical benefit in completing an MRI of the shoulder musculature after an electrophysiological investigation. Recent advances in enhanced MRI techniques allow for imaging with a particular sensitivity to neural tissues. Magnetic resonance neurography is a new technique to evaluate peripheral nerve disorders. This diagnostic approach may prove valuable especially if NA is considered an immune-mediated inflammatory reaction. With this technique, increased signal intensity may be seen in the involved neural tissue. To the authors’ knowledge, there is only one case study using magnetic resonance neurography as a diagnostic tool in NA.21 Because of the dramatic nature of the NA presentation, in particular the motor deficits, we clinicians feel compelled to intervene. Considering the clinical picture of this condition, an empirical management plan could include treatment aimed at pain, the underlying neuropathological
Journal of Manipulative and Physiological Therapeutics January 2006
process, muscle atrophy and weakness, and any secondary musculoskeletal adaptive responses. However, the natural history of NA (nonhereditary form) suggests that the prognosis is favorable for full functional recovery in most patients with no intervention.22 This slow but progressive recovery of motor function is reported to occur over 6 to 18 months.19 There are attempts at physical intervention by some clinicians; however, there are no outcome studies suggesting that natural history is improved by the use of modalities such as ultrasound, electrotherapy, and acupuncture.2,23 During the pain phase, analgesics may be used. In this phase, rest also helps in reducing activities that may exacerbate symptoms. Corticosteroids have not shown any effectiveness in altering the course of the condition.22 It is possible that the slowly recovering motor deficit may lead to secondary musculoskeletal dysfunction and adaptive responses.24 There is an absence of evidence suggesting that this slow recovery results in frozen shoulder. There is one published report of two cases where NA coexisted with frozen shoulder.25 However, complex regional pain syndrome was an additional complicating feature in these cases. Simotas and Tsairis 26 published a case report of a 37-year-old woman with 7 months of unilateral shoulder girdle stiffness, pain, and weakness. This had previously been diagnosed as frozen shoulder. The authors speculated that there was a coexisting neuropathic process suggestive of NA. In the absence of evidence, it may be prudent to have the patient perform range of motion exercises to maintain preserved amounts progressing to a strengthening program. The patient was given this recommendation particularly in view of his occupation.
CONCLUSION Patients presenting with shoulder girdle and arm pain are common in manual therapy practices. When neurogenic in origin, most represent cervical radiculopathy. Neuralgic amyotrophy represents an important consideration when there are neurogenic signs and symptoms. Differentiating NA from radiculopathy is especially important in making management decisions, especially when surgery is considered. In most cases, NA is a self-limiting condition requiring reassurance and monitoring.
REFERENCES 1. Dumitru D. Electrodiagnostic medicine. Philadelphia7 Hanley and Belfus Inc; 1995. p. 623 - 4. 2. McCarty EC, Tsairis P, Warren RF. Brachial neuritis. Clin Orthop 1999;37 - 43. 3. England JD, Sumner AJ. Neuralgic amyotrophy: an increasingly diverse entity. Muscle Nerve 1987;10:60 - 8. 4. Parsonage MJ, Turner JWA. The shoulder-girdle syndrome. Lancet 1948;1:973 - 8.
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
5. Auge WK, Velazquez PA. Parsonage-Turner syndrome in the Native American Indian. J Shoulder Elb Surg 2000;9:99 - 103. 6. Miller JD, Pruitt S, McDonald TJ. Acute brachial plexus neuritis: an uncommon cause of shoulder pain. Am Fam Physician 2000;62:2067 - 72. 7. Manifold SG, McCann PD. Cervical radiculitis and shoulder disorders. Clin Orthop Relat Res 1999;368:105 - 13. 8. McGillicuddy JE. Cervical radiculopathy, entrapment neuropathy, and thoracic outlet syndrome: how to differentiate? Invited submission from the Joint Section Meeting on Disorders of the Spine and Peripheral Nerves, March 2004. J Neurosurg Spine 2004;1:179 - 87. 9. Henderson CM, Hennessy RG, Shuey HM, Shackelford EG. Posterior-lateral foraminotomy as an exclusive operative technique for cervical radiculopathy: a review of 846 consecutively operated cases. Neurosurgery 1983;13: 504 - 12. 10. Gifford L. Acute low cervical nerve root conditions: symptom presentations and pathobiological reasoning. Man Ther 2001; 6:106 - 15. 11. Humphreys SC, Hodges SD, Patwardhan A, Eck JC, Covington LA, Sartori M. The natural history of the cervical foramen in symptomatic and asymptomatic individuals aged 20 - 60 years as measured by magnetic resonance imaging. A descriptive approach. Spine 1998;23:2180 - 4. 12. Hasue M. Pain and the nerve root. An interdisciplinary approach. Spine 1993;18:2053 - 8. 13. McIlveen SJ, Duralde XA, D’Alessandro DF, Bigliani LU. Isolated nerve injuries about the shoulder. Clin Orthop Relat Res 1994;306:54 - 63. 14. Birch R. Injuries to the brachial plexus: controversies and possibilities. Neurosurg Clin N Am 2001;12:285 - 94. 15. Harbaugh KS, Swenson R, Saunders RL. Shoulder numbness in a patient with suprascapular nerve entrapment syndrome:
Rix et al Neuralgic Amyotrophy
16. 17.
18. 19. 20.
21. 22. 23. 24. 25.
26.
cutaneous branch of the suprascapular nerve: case report. Neurosurgery 2000;47:1452 - 5. Duralde XA. Evaluation and treatment of the winged scapula. J South Orthop Assoc 1995;4:38 - 52. Orstavik K, Skard Heier M, Young P, Stogbauer F. Brachial plexus involvement as the only expression of hereditary neuropathy with liability to pressure palsies. Muscle Nerve 2001; 24:1093 - 6. Cruz-Martinez A, Barrio M, Arpa J. Neuralgic amyotrophy: variable expression in 40 patients. J Peripher Nerv Syst 2002;7:198 - 204. Gonzalez-Alegre P, Recober A, Kelkar P. Idiopathic brachial neuritis. Iowa Orthop J 2002;22:81 - 5. Elsayes KM, Shariff A, Staveteig PT, Mukundan G, Khosla A, Rubin DA. Value of magnetic resonance imaging for muscle denervation syndromes of the shoulder girdle. J Comput Assist Tomogr 2005;29:326 - 9. Sarikaya S, Sumer M, Ozdolap S, Erdem CZ. Magnetic resonance neurography diagnosed brachial plexitis: a case report. Arch Phys Med Rehabil 2005;86:1058 - 9. Tsairis P, Dyck PJ, Mulder DW. Natural history of brachial plexus neuropathy. Report on 99 patients. Arch Neurol 1972; 27:109 - 17. Aymond JK, Goldner JL, Hardaker WT. Neuralgic amyotrophy. Orthop Rev 1989;18:1275 - 9. Behar Y, Thiel H. Neuralgic amyotrophy. Eur J Chiropr 1994; 42:47 - 51. Billey T, Dromer C, Vedrenne C, Caulier M, Fournie B. Parsonage-Turner syndrome complicated by sympathetic dystrophy syndrome with adhesive capsulitis of the shoulder. Apropos of 2 cases. Rev Rhum Mal Osteo-artic 1992;59:765 - 7. Simotas AC, Tsairis P. Adhesive capsulitis of the glenohumeral joint with an unusual neuropathic presentation: a case report. Am J Phys Med Rehabil 1999;78:577 - 81.
59
ABSTRACT Objective: To describe the case of a patient diagnosed with neuralgic amyotrophy (NA) illustrating pertinent aspects of differential diagnosis, the use of clinical neurophysiological procedures to aid in establishing the diagnosis, and issues of management. Clinical Features: A 39-year-old male soldier presented with a rapid onset of marked loss of left shoulder movement. This started acutely early one morning as a sharp, severe lower neck pain progressing over the following 2 weeks to a less severe dull ache in the left shoulder and arm. Pain was rapidly replaced with weakness. Physical examination and electrodiagnostic investigation helped establish a diagnosis of NA. Intervention and Outcome: The patient was reassured that this is normally a self-limiting condition. Range of motion exercises progressing to a strengthening program was prescribed. He was progressing well; however, we lost contact because of his commitments in the armed service. Conclusion: When a patient presents with shoulder and arm pain of neurogenic origin, NA should be a consideration. Differentiating NA from radiculopathy is especially important in making management decisions. With a careful history and physical examination, the diagnosis may be made without the need for ancillary investigations. Neuralgic amyotrophy is a self-limiting condition requiring reassurance and monitoring. (J Manipulative Physiol Ther 2006;29:52-59) Key Indexing Terms: Brachial Plexus Neuropathies; Amyotrophy, Neuralgic; Radiculopathy
I
diopathic neuralgic amyotrophy (NA) is a rare disorder of unknown etiology that mimics many common conditions with acute pain and weakness around the shoulder. This condition has several confusing descriptors, including acute brachial neuritis/plexitis/neuropathy/radiculitis and shoulder girdle neuritis/syndrome.1 - 3 Parsonage and Turner coined the term neuralgic amyotrophy in the late 1940s.4 Subsequently, some clinicians refer to the condition as Parsonage-Turner syndrome.5 The term neuralgic amyotrophy works well as a descriptor because it does not presume a clear etiology and site of pathology, yet describes a
Senior Clinical Tutor, Anglo-European College of Chiropractic, Bournemouth, UK. b Senior Clinical Tutor, Anglo-European College of Chiropractic, Bournemouth, UK. c Private Practice of Chiropractic, Doncaster, UK. Sources of support: No external funds were provided for this research. Submit requests for reprints to: George Rix, DC, AngloEuropean College of Chiropractic, 13-15 Parkwood Rd., BH5 2DF Bournemouth, UK (e-mail: [email protected]). Paper submitted July 13, 2004; in revised form July 7, 2005. 0161-4754/$32.00 Copyright D 2006 by National University of Health Sciences. doi:10.1016/j.jmpt.2005.11.008
52
the clinical presentation.1,3,4,6 Characterized by severe pain followed by muscle weakness, atrophy, and variable sensory deficits, the diagnosis is made from the history and physical examination findings and confirmed by clinical neurophysiology testing. Although NA is a quite well-defined entity, establishing the diagnosis can be challenging, particularly as the presentation is considerably more diverse than generally appreciated.3 Consideration is often given to nerve root lesions, primarily C5.6 Other neurological diagnostic considerations within the peripheral neural axis include traction and compressive lesions of the brachial plexus that may affect one or several nerves, including one of the most devastating injuries for athletes, suprascapular nerve entrapment. However, a careful history is often diagnostic. Fortunately, nerve injuries involving the shoulder are uncommon. However, it is important that the clinician differentiates peripheral nerve injuries from lesions affecting the brachial plexus and proximal lesions resulting in radiculopathy. The latter differentiation is especially important to avoid unnecessary therapeutic interventions, such as surgery for coexisting cervical spondylotic changes in a patient.6 An in-depth understanding of peripheral nervous system conditions affecting the shoulder and
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
Fig 1. Moderate atrophy of the left shoulder girdle. Note loss of left deltoid and biceps bulk as compared with the right arm. Some atrophy of the left triceps appears as well.
Rix et al Neuralgic Amyotrophy
Fig 3. Moderate atrophy of the left anterior shoulder girdle. Note loss of left deltoid and biceps bulk as compared with the right arm. There appears to be a mild asymmetry of the pectoralis major muscles. This could be confused with atrophy, but in most cases, it is a simple anatomic variation.
Fig 2. Moderate atrophy of the left posterior shoulder girdle. Note loss of left deltoid bulk as compared with the right arm. There is winging of the left scapula. As in the lateral photographic view, the left triceps appears thinner than the right.
neurological localizing skill is integral to appropriate diagnosis and management. We present the case of a patient with an acute onset of left shoulder pain to illustrate pertinent aspects of differential diagnosis, the use of clinical neurophysiological procedures to aid in establishing the working diagnosis, and issues of management. Neuralgic amyotrophy is often a self-limiting phenomenon that requires nothing more than monitoring for a period of time, range of motion exercises, followed by a strengthening program. However, there are instances when recovery does not occur or is incomplete. Also, possibilities of more serious conditions require careful evaluation and critical thought illustrating the need for careful observation and monitoring.
CASE REPORT A 39-year-old male British Army physical trainer presented to the teaching clinic of Anglo-European College
Fig 4. Marked loss of left shoulder abduction. Note hiking of the shoulder during attempted abduction secondary to loss of primary and secondary muscle action. of Chiropractic complaining of a rapid onset of marked loss of left shoulder movement. Problems with his left shoulder began 3 weeks before his initial clinic visit when he reported waking up at 4:00 am with a sharp pain in the left lower neck. He tried using an ice pack and applying an ibuprofenbased topical gel, which provided no relief. Over the following 24 hours, the sharp pain changed in character to a slightly less severe dull ache. Over the following 2 weeks, the dull ache spread into the left shoulder and arm, stopping at the elbow. Various medications prescribed by an Army medical officer, including aspirin, a paracetamol (acetaminophen) and codeine preparation, and diazepam, oral corticosteroid, and amitryptilline, provided no relief or change in
53
54
Rix et al Neuralgic Amyotrophy
Journal of Manipulative and Physiological Therapeutics January 2006
Table 1. Results of clinical neurophysiology examination Anglo European College of Chiropractic Clinical Neurophysiology Laboratory 13-15 Parkwood Road Bournemouth, BH5 2DF Clinic Tel: (01202) 436222
Patient: DR Date: 16-05-01 Clinical Concern: Atrophy and Weakness Left Shoulder Girdle
Upper extremity nerve conduction studies performed after warming of extremities. NR, no response. Motor and sensory amplitudes are measured baseline to peak. Sensory latencies are measured to peak whereas motor latencies are measured to initial negative onset. DSL, Distal sensory latency; S Amp, sensory amplitude; DML, distal motor latency; M Amp, motor amplitude; NCV, nerve conduction velocity; BE, below elbow; AE, above elbow.
Nerve R L R L R L R L
Lateral cutaneous antebrachial at 12 cm Lateral cutaneous antebrachial at 12 cm Musculocutaneous Musculocutaneous Axillary Axillary Long thoracic Long thoracic
DSL (ms)
S Amp (lV)
2.68
16.0
2.39
33.0
DML (ms)
M Amp (mV)
NCV (m/s)
4.16 4.99 3.53 4.78 3.74 4.16
6.050K 0.850K 5.000K 0.450K 1.000K 0.450K
67.30 54.08 50.90 41.80 66.77 55.28
F wave (ms)
Electromyography using a sterile disposable concentric needle electrode. Ins activity, Insertional activity (n = normal); PSW, positive sharp wave; Fib, fibrillation potential; 0 = absent, 1+ minimal to 4+ maximal; LT, long trains; FASC, fasciculation potential; CRD, complex repetitive discharge; MYK, myokymic discharge; MYT, myotonic discharge; NMT, neuromyotonic discharge. Spontaneous activity
Voluntary
Muscle side
Ins activity
PSW
Fib
Other
MUAP
Recrt
L Deltoid L Biceps L Supraspinatus L Infraspinatus L Teres major L Cervical paraspinal
Incr N N N N N
1+ 2+ 0 2+ 0 0
2+ 2+ 1+ 3+ 1+ 0
FASC FASC 0 0 0 0
N N N N Sparse
Incomp Incomp Incomp Incomp Incomp
the symptoms throughout this time. During the following week, the pain subsided. On the initial visit, the patient noted the dull ache in the neck, shoulder, and arm had disappeared. He reported significant difficulty in flexing and abducting his left shoulder. He denied any recent history of trauma to the area. The day before the incident of sharp pain, he engaged in his usual exercise routine at the gym that included 20 minutes of stationary cycling and 5 sets of 5 repetitions of 50-kg clean and jerk lifts. His medical history was noncontributory with only a few incidents of exercise related low back pain, right fibular fracture, right knee anterior cruciate injury, and tonsillectomy. He was taking no medications at the time of examination. The complete review of systems was unremarkable. On examination, he appeared to be a generally wellmuscled man in no acute distress. All vital signs were well within normal limits. He had good posture, although the left trapezius muscle appeared taut. There was moderate atrophy of the left shoulder girdle, especially considering his excellent muscle tone and bulk (Figs 1 -3). Occasional
fasciculations were observed in the left biceps and deltoid muscles. These were more pronounced on percussion of the muscles. He had a normal gait. Upper and lower extremity muscle stretch reflexes were present and symmetric with the exception of the left biceps, which was diminished as compared with the right. There was no clonus at the ankles. Plantar reflexes were flexor. Muscle strength in the lower extremities was 5/5. Motor examination of the upper extremities revealed 3/5 weakness of the left teres minor, deltoid, and serratus anterior; 4/5 weakness of the left biceps, brachioradialis, and infraspinatus; and 4/5 weakness of the left supraspinatus. There was only slight give-way of the left flexor carpi ulnaris. The remainder of the left shoulder girdle and the right upper extremity muscles were 5/5. Gross sensory examination of all four extremities to sharp and soft touch was intact. Cervical ranges of motion were full and unencumbered. Cervical compression tests, including all variants, were unproductive. There were marked limitations of left shoulder ranges of motion, with loss most evident in abduction to 608 and flexion to 458 (Fig 4). Full movement of the left shoulder was obtained
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
Rix et al Neuralgic Amyotrophy
Table 2. Typical clinical features of idiopathic NA Incidence Male:female Age of onset Etiology Antecedent or associated illness Initial symptom
Mode of onset Weakness Sensory deficit Patterns and distributions of neurological insult
Other neurological findings Laterality Laboratory Electrodiagnosis
Approximately 1.5 per 100 000 Reports vary from 2:1 to 11:1 3 mo to 75 y; highest incidence in the third and seventh decades Exact cause unknown; postulated factors include trauma, infection, viral diseases, unfamiliar strenuous exercise, immunization, autoimmune mechanisms, and surgery Antecedent febrile illness in approximately 25% of patients Pain (severe) in 95% of patients often aggravated by extremity movement; location: in or around the shoulder girdle (possibly related to the region of nervous system affected), may radiate from the shoulder down into the lateral arm or up along the neck; quality: lancinating, sharp, burning, throbbing, boring severe ache; progression: intense pain may persist for a few hours to 3 weeks, often replaced by musculoskeletal pain and dysfunction Sudden, sometimes awakening patient during the night Usually occurs after the pain subsides although there can be an overlap (can occur simultaneously with onset of pain): 70% in 2 weeks, 85% within first month after symptoms begin Variable frequency reported; usually incomplete, less marked than motor deficits; correlates with affected nerves Flaccid paresis associated with wasting (lower motor neuron lesion)—most commonly evident in deltoid, supraspinatus, infraspinatus, serratus anterior, biceps, triceps, and wrist and finger extensors; categories: (1) mononeuropathy, (2) combined mononeuropathy, and plexopathy (least common); nerves affected: primarily the axillary, suprascapular, long thoracic, and musculocutaneous nerves Tendon reflexes may be diminished depending on site of lesion/s; occasionally, fasciculations are present Unilateral, 66% (right side 54%); bilateral, 34% (onset and presentation are usually asymmetric); no correlation with hand dominance Normal Aids in establishing diagnosis by localizing the lesion/s; NCS: median and ulnar velocities usually normal; CMAPs from proximal muscles show abnormalities in 50% of patients (however, helps to rule out other conditions); CMAP amplitudes may be diminished indicating axonal loss; needle EMG: more helpful than NCS in localizing the lesion/s
Table created from information from References [1] and [2]. NCS, Nerve conduction studies; EMG, electromyography.
passively. There were full active ranges in all directions of the right shoulder. The results of electrodiagnostic studies are shown in Table 1. Nerve conduction studies of the musculocutaneous, axillary, and long thoracic nerves were carried out bilaterally with stimulation at Erb point. Compound motor action potential (CMAP) amplitudes for the musculocutaneous, axillary, and long thoracic nerves were markedly decreased on the left. The left musculocutaneous CMAP amplitude was 14%, the axillary amplitude was 9%, and the long thoracic amplitude was 45% of the respective right counterpart. There was mild slowing of the distal motor latencies for these nerves with decreased nerve conduction velocities. Sensory nerve action potentials were also obtained for the lateral cutaneous antebrachial nerve bilaterally. The sensory latencies and amplitudes were normal. Electromyography of the left shoulder girdle was completed with a concentric needle electrode. Increased insertional activity, occasional positive sharp waves, 2+ fibrillation, and fasciculation potentials were noted in the deltoid muscle. There were 2+ positive sharp waves, fibrillation potentials, and fasciculation potentials noted in the biceps muscle. Rare fibrillation potentials were evident in the supraspinatus and teres major muscles. Examination of the infraspinatus muscle revealed trains of positive sharp waves and 3+ fibrillation potentials. Recruitment patterns were incomplete for all of these muscles.
Because the patient was being cared for in a teaching clinic, a fifth-year student intern first assessed the patient. Before consultation with clinical tutors and electrodiagnosis, the intern considered a C5 radiculopathy. However, considering the onset and progression, including the rapid resolution of pain, lack of sensory signs or symptoms, distribution and severity of muscle involvement, lack of cervical spine findings, and inability to provoke symptoms with cervical compression tests even with consideration of pain absence, the presumptive diagnosis became idiopathic NA. The electrodiagnostic studies revealed a motor axonal neuropathy affecting multiple peripheral nerves around the shoulder. This could be classified as a mononeuropathy multiplex. Axonal loss was evident for the left musculocutaneous, axillary, and long thoracic nerves. Acute denervation potentials were noted in multiple sites of the left shoulder girdle. Because idiopathic NA is usually a selflimiting problem, the patient was reassured. Because of his Army status, he returned to his base for rehabilitative management with our recommendation for range of motion exercises progressing to a strengthening program. A report was sent to his medical officer with the suggestion that his condition be monitored. On follow-up, he was making good progress. However, he was keen to undertake rehabilitative exercise to maximize the probability of regaining mobility and strength as quickly as possible. Unfortunately, because of his
55
56
Rix et al Neuralgic Amyotrophy
commitments as a member of the armed forces, we lost contact with him for further follow-up.
DISCUSSION This case reflects the typical presentation of idiopathic NA (Table 2). The diagnosis was suggested because the patient was seen in the subacute setting at a time when the classic features had already evolved and a reasonably obvious nonradicular pattern of weakness and atrophy had developed. However, if a patient presents soon after onset when pain is the predominant feature, the diagnosis of NA can be challenging.2 The potential differential diagnoses for the patient with acute severe pain in or around the shoulder covers a reasonably broad range of musculoskeletal and neurological conditions.7,8 Consideration must also be given to visceral causes of pain. When there is exacerbation of pain with shoulder movements, visceral causes are improbable. The list of possible differential diagnoses narrows more definitively as neurological symptoms and signs emerge. A careful history, even in the acute phase, often reveals features indicative of a neurological process. Cervical spine radiculopathy is usually the first neurological consideration in the acute painful phase, particularly when weakness and paresthesia are reported. Differentiation based on pain distributions alone is difficult because many patients with radiculopathy do not present with pain following a discrete dermatome pattern.9 While nerve root disorders are often misdiagnosed or unrecognized, the emergence of the neurological signs as the condition progresses may lead to a misdiagnosis of cervical spine radiculopathy.10 This differentiation is particularly important to avoid unnecessary investigations and inappropriate therapeutic or surgical interventions.6 A key differential diagnostic feature is the provocation of pain or paresthesia with variants of cervical compression maneuvers. Although strongly suggestive of cervical radiculopathy, head movements and compression tests do not increase the pain associated with NA. However, as in this case, it is not uncommon for patients with NA to experience exacerbation of pain with shoulder movement. This may represent mechanical provocation of sensitized neural tissues distal to the nerve root. However, shoulder and arm movements may affect pain levels in some cases of cervical radiculopathy. For instance, abduction of the arm may relieve radicular pain, that is, arm abduction sign. In this patient, the neurological deficits could be mistaken for a C5 radiculopathy. Although the C5 root level is common to all the muscles affected, a root lesion does not manifest weakness in as broad a distribution as seen in this patient. This is especially evident with the serratus anterior weakness, not seen in a C5 lesion. Another confusing localizing issue may be an absent or
Journal of Manipulative and Physiological Therapeutics January 2006
diminished muscle stretch reflex. In this case, the left biceps reflex was diminished. In isolation, this is consistent with a C5 or C6 root lesion. Assuming NA is a mononeuropathy multiplex, a reflex (C5-7) can be absent or diminished if the process involves the radial or musculocutaneous nerves. In this case, involvement of the musculocutaneous nerve produced the physical examination results. In addition, a radiculopathy was less likely with the absence of peripheral symptom generation caused by nerve root provocation tests such as cervical compression maneuvers. Cervical spine special imaging may be helpful in appreciating anatomic changes that may result in radiculopathy. These changes must be interpreted in the context of the clinical picture and moderated by an appreciation of the occurrence of these findings in asymptomatic subjects. The demonstration of an imaging study abnormality does not automatically imply causality. For instance, in a patient with NA, there exists the possibility of asymptomatic cervical spine imaging abnormalities appearing to affect the nerve root, such as spondylotic changes with encroachment of the intervertebral foramen, especially when occurring at multiple levels.11 Furthermore, in the authors’ experience, not all clinical presentations strongly suggestive of cervical radiculopathy have clear correlative imaging findings. This may suggest a chemical rather than mechanical compressive factor producing the radicular symptoms and sensitization of the dorsal root ganglia.12 When obvious weakness and perhaps atrophy accompany the acute pain, a lack of clear nerve impression on imaging is more helpful in lowering the probability of a root cause. As an investigation procedure, electromyography produces a variable diagnostic yield in differentiating cervical radiculopathy from NA. Results are dependent on the severity of the neural damage, timing of the investigation, and skill of the examiner.1,6 Electromyography commonly shows spontaneous electrical activity in the paraspinal muscles in radiculopathy but is normal in NA because the posterior dorsal rami nerves are not involved in this condition. Although trauma and unaccustomed strenuous activity have been cited as possible etiological factors in NA (Table 2), direct trauma is not readily identifiable as part of the clinical picture. A consideration when there is a history of trauma is a true brachial plexus or peripheral nerve injury. History and descriptions are important in developing likely differential diagnostic scenarios. Injuries to the brachial plexus in the supraclavicular fossa are unusual in the athlete.13 The incident is highest, outside of birth trauma, in young men engaged in manual labor.14 True supraclavicular brachial plexus injuries may have mixed central nervous system and peripheral nervous system features because there is a high incidence of rupture or preganglionic injury to spinal nerves.14 The fifth and sixth nerve roots may be involved. The injury can be devastating
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
and carries a varied prognosis for full recovery. Pain proximal to the plexus begins immediately in at least one half of the cases.14 The pain has various descriptors but is often described as constant intense burning or crushing and may involve the forearm and hand, although this is not a common presentation. Injuries involving the lower plexus are often the result of traction on the arm or compressive due to direct trauma or tumors from the lung apex. The intrinsic hand muscles are often involved and, therefore, the examiner may appreciate weakness and atrophy. Sensory changes are most commonly limited to the medial forearm and hand because of ulnar nerve involvement. Peripheral nerve lesions may be the most difficult to distinguish from NA.3 Nerves crossing the shoulder may be injured, especially in an athlete. The musculocutaneous, axillary, long thoracic, suprascapular, and spinal accessory nerves can be injured from a concussive traumatic event, single strain force, or multiple strain forces. Signs and symptoms can vary from mild neuropraxia to axonotmesis. Fortunately, most injuries are neuropraxic,13 that is, a conduction block within an intact nerve. Therefore, prognosis for complete recovery is excellent. Although axonotmesis is a serious injury with distal axonal degeneration, the connective tissues remain intact and expectations for full recovery are good, albeit with prolonged healing time. Neurotmesis or complete nerve disruption is usually secondary to high-energy trauma and penetrating injuries has a poor prognosis for recovery. Differential diagnosis of peripheral nerve injuries requires a knowledge base that includes a detailed understanding of anatomy. For instance, the axillary nerve, which is the most frequently injured peripheral nerve around the shoulder,13 passes through the quadrilateral space near the inferior portion of the joint before dividing into anterior and posterior branches to supply the anterior and posterior deltoid muscles, respectively. Smaller branches supply the teres minor muscle and innervate the skin over the deltoid insertion. There are several fixation points of the nerve making it prone to throwing injuries. Symptoms, especially initially, are vague, making it difficult to accurately diagnose. The clinical picture is not unlike a nonneurogenic shoulder injury. Meticulous palpation of the deltoid muscle is required to appreciate decreased firing activity and atrophy. Another example of the difficulty in isolating an injured nerve about the shoulder is entrapment of the suprascapular nerve. Formed from branches arising from the C5 and C6 nerve roots, it comes off the upper trunk of the plexus and traverses laterally passing through the suprascapular notch. Motor branches supply the supraspinatus and infraspinatus muscles. Afferent branches cover the posterior capsule and areas over the acromioclavicular joint. Interestingly, there are still reports in the literature that there are no surface cutaneous branches.13 However, cutaneous innervation has been reported and commented on for 20 years.15 Considering its course and sites of fixation, it is prone to traction
Rix et al Neuralgic Amyotrophy
and compressive injuries. Shoulder pain with numbness over the superior aspect of the shoulder may suggest an injury to the suprascapular nerve and prompt the examiner to search for this possibility. Surgical decompression may be necessary for recovery.15 It may be difficult to differentiate NA from entrapment of the suprascapular nerve. Timing is a consideration because most cases of NA resolve within 6 weeks. A better method of differentiation is electromyography because in NA, spontaneous activity will be present in shoulder muscles beyond the supraspinatus and infraspinatus muscles. Other considerations for a differential diagnosis of peripheral mononeuropathy about the shoulder are the musculocutaneous, long thoracic, and spinal accessory nerves. As noted above, a detailed understanding of anatomy is important in these cases. Injuries to the musculocutaneous nerve present with weakness and atrophy of the biceps and brachioradialis muscles; therefore, elbow flexion is often compromised to some degree. True scapular winging, compromised scapular rhythm, and atrophy of the serratus anterior muscle are hallmark signs of a long thoracic nerve lesion.16 Winging of the scapula may also be present in spinal accessory nerve lesions because the trapezius muscle aids in stabilization of the shoulder and rotation against the posterior thoracic wall. However, the patient with a lesion to the spinal accessory nerve will also present with posterior shoulder ache and, most likely, a dropped shoulder on the involved side with atrophy of the trapezius.16 Again, electromyographic evaluation offers invaluable help in the differential diagnosis. In young patients such as the one reported here, consideration in the differential diagnosis may be given to hereditary neuropathies, such as hereditary neuropathies with liability to pressure palsies (HNPP) and hereditary NA. However, these conditions are rare. For example, only 100 cases of hereditary NA have been reported since first recognized in 1886.17 Both conditions are benign and autosomal dominant. Symptoms of HNPP start in the second or third decade. Hereditary NA has variable upper limb weakness and pain whereas HNPP rarely has any associated pain, which contrasts with the typical presentation of NA. Brachial plexus involvement shows up in many of the cases in electrophysiological studies without evidence of a generalized neuropathy.17 In most cases, electrophysiological examination is unnecessary. Electrodiagnostic evaluation in a patient with suspected NA is usually undertaken when there is some ambiguity in the clinical picture to tease out any possible concomitant neurogenic conditions, to avoid unnecessary surgical intervention, and to increase confidence levels in advising the patient on the natural history. These studies commonly include nerve conduction and needle electromyography. As with the investigation of patients with suspected cervical radiculopathy, electrophysiological studies may be inconclusive. However, in the differential
57
58
Rix et al Neuralgic Amyotrophy
diagnosis of nerve lesions about the shoulder, electromyography is the best way to localize the lesion.1 Evoking and recording compound muscle action potentials for deltoid, biceps, and serratus anterior muscles and the lateral antebrachial cutaneous reveals abnormalities in only approximately 50% of the cases of NA.1 Electromyography sampling allows localization of the lesion to specific muscles, generally in 3 patterns, that is, mononeuropathy, plexopathy, and mononeuropathy combined with plexopathy.1 Sampling of shoulder girdle muscles innervated by the same and different nerves and cervical paraspinal muscles should be included in the examination. Distal muscles should not be routinely done but considered if a cervical radicular process appears possible. However, it is rare that paraspinal muscles are involved.1,2 Therefore, spontaneous activity in these muscles strongly suggests nerve root involvement. Evoked potentials may reveal conduction slowing. More importantly, the surface recording of CMAPs with amplitude measurements is useful in determining the extent of axonal loss. There is controversy on localization of the lesion in NA. Not all studies/case reports provide electrophysiological data. Those that have provided data suggest a mononeuropathy multiplex.3,18 In this case, there was no electromyographic evidence of spontaneous paraspinal activity confirming the clinical impression that radiculopathy was unlikely. For this patient, nerve conduction studies and electromyography categorized the lesion to a likely combined mononeuropathy and plexopathy as opposed to a plexopathy alone or mononeuropathy.1 It also provided some quantification of the degree of axonal loss. Another ancillary examination that may have value in the acute and subacute stages is magnetic resonance imaging (MRI) of the involved muscles. T2-weighted fast spin echo images may reveal high signal intensity of the affected muscles related to neurogenic inflammation. During the chronic phase, a T1-weighted spin echo image may show muscle atrophy.6,19,20 Although interesting, there is often little additional clinical benefit in completing an MRI of the shoulder musculature after an electrophysiological investigation. Recent advances in enhanced MRI techniques allow for imaging with a particular sensitivity to neural tissues. Magnetic resonance neurography is a new technique to evaluate peripheral nerve disorders. This diagnostic approach may prove valuable especially if NA is considered an immune-mediated inflammatory reaction. With this technique, increased signal intensity may be seen in the involved neural tissue. To the authors’ knowledge, there is only one case study using magnetic resonance neurography as a diagnostic tool in NA.21 Because of the dramatic nature of the NA presentation, in particular the motor deficits, we clinicians feel compelled to intervene. Considering the clinical picture of this condition, an empirical management plan could include treatment aimed at pain, the underlying neuropathological
Journal of Manipulative and Physiological Therapeutics January 2006
process, muscle atrophy and weakness, and any secondary musculoskeletal adaptive responses. However, the natural history of NA (nonhereditary form) suggests that the prognosis is favorable for full functional recovery in most patients with no intervention.22 This slow but progressive recovery of motor function is reported to occur over 6 to 18 months.19 There are attempts at physical intervention by some clinicians; however, there are no outcome studies suggesting that natural history is improved by the use of modalities such as ultrasound, electrotherapy, and acupuncture.2,23 During the pain phase, analgesics may be used. In this phase, rest also helps in reducing activities that may exacerbate symptoms. Corticosteroids have not shown any effectiveness in altering the course of the condition.22 It is possible that the slowly recovering motor deficit may lead to secondary musculoskeletal dysfunction and adaptive responses.24 There is an absence of evidence suggesting that this slow recovery results in frozen shoulder. There is one published report of two cases where NA coexisted with frozen shoulder.25 However, complex regional pain syndrome was an additional complicating feature in these cases. Simotas and Tsairis 26 published a case report of a 37-year-old woman with 7 months of unilateral shoulder girdle stiffness, pain, and weakness. This had previously been diagnosed as frozen shoulder. The authors speculated that there was a coexisting neuropathic process suggestive of NA. In the absence of evidence, it may be prudent to have the patient perform range of motion exercises to maintain preserved amounts progressing to a strengthening program. The patient was given this recommendation particularly in view of his occupation.
CONCLUSION Patients presenting with shoulder girdle and arm pain are common in manual therapy practices. When neurogenic in origin, most represent cervical radiculopathy. Neuralgic amyotrophy represents an important consideration when there are neurogenic signs and symptoms. Differentiating NA from radiculopathy is especially important in making management decisions, especially when surgery is considered. In most cases, NA is a self-limiting condition requiring reassurance and monitoring.
REFERENCES 1. Dumitru D. Electrodiagnostic medicine. Philadelphia7 Hanley and Belfus Inc; 1995. p. 623 - 4. 2. McCarty EC, Tsairis P, Warren RF. Brachial neuritis. Clin Orthop 1999;37 - 43. 3. England JD, Sumner AJ. Neuralgic amyotrophy: an increasingly diverse entity. Muscle Nerve 1987;10:60 - 8. 4. Parsonage MJ, Turner JWA. The shoulder-girdle syndrome. Lancet 1948;1:973 - 8.
Journal of Manipulative and Physiological Therapeutics Volume 29, Number 1
5. Auge WK, Velazquez PA. Parsonage-Turner syndrome in the Native American Indian. J Shoulder Elb Surg 2000;9:99 - 103. 6. Miller JD, Pruitt S, McDonald TJ. Acute brachial plexus neuritis: an uncommon cause of shoulder pain. Am Fam Physician 2000;62:2067 - 72. 7. Manifold SG, McCann PD. Cervical radiculitis and shoulder disorders. Clin Orthop Relat Res 1999;368:105 - 13. 8. McGillicuddy JE. Cervical radiculopathy, entrapment neuropathy, and thoracic outlet syndrome: how to differentiate? Invited submission from the Joint Section Meeting on Disorders of the Spine and Peripheral Nerves, March 2004. J Neurosurg Spine 2004;1:179 - 87. 9. Henderson CM, Hennessy RG, Shuey HM, Shackelford EG. Posterior-lateral foraminotomy as an exclusive operative technique for cervical radiculopathy: a review of 846 consecutively operated cases. Neurosurgery 1983;13: 504 - 12. 10. Gifford L. Acute low cervical nerve root conditions: symptom presentations and pathobiological reasoning. Man Ther 2001; 6:106 - 15. 11. Humphreys SC, Hodges SD, Patwardhan A, Eck JC, Covington LA, Sartori M. The natural history of the cervical foramen in symptomatic and asymptomatic individuals aged 20 - 60 years as measured by magnetic resonance imaging. A descriptive approach. Spine 1998;23:2180 - 4. 12. Hasue M. Pain and the nerve root. An interdisciplinary approach. Spine 1993;18:2053 - 8. 13. McIlveen SJ, Duralde XA, D’Alessandro DF, Bigliani LU. Isolated nerve injuries about the shoulder. Clin Orthop Relat Res 1994;306:54 - 63. 14. Birch R. Injuries to the brachial plexus: controversies and possibilities. Neurosurg Clin N Am 2001;12:285 - 94. 15. Harbaugh KS, Swenson R, Saunders RL. Shoulder numbness in a patient with suprascapular nerve entrapment syndrome:
Rix et al Neuralgic Amyotrophy
16. 17.
18. 19. 20.
21. 22. 23. 24. 25.
26.
cutaneous branch of the suprascapular nerve: case report. Neurosurgery 2000;47:1452 - 5. Duralde XA. Evaluation and treatment of the winged scapula. J South Orthop Assoc 1995;4:38 - 52. Orstavik K, Skard Heier M, Young P, Stogbauer F. Brachial plexus involvement as the only expression of hereditary neuropathy with liability to pressure palsies. Muscle Nerve 2001; 24:1093 - 6. Cruz-Martinez A, Barrio M, Arpa J. Neuralgic amyotrophy: variable expression in 40 patients. J Peripher Nerv Syst 2002;7:198 - 204. Gonzalez-Alegre P, Recober A, Kelkar P. Idiopathic brachial neuritis. Iowa Orthop J 2002;22:81 - 5. Elsayes KM, Shariff A, Staveteig PT, Mukundan G, Khosla A, Rubin DA. Value of magnetic resonance imaging for muscle denervation syndromes of the shoulder girdle. J Comput Assist Tomogr 2005;29:326 - 9. Sarikaya S, Sumer M, Ozdolap S, Erdem CZ. Magnetic resonance neurography diagnosed brachial plexitis: a case report. Arch Phys Med Rehabil 2005;86:1058 - 9. Tsairis P, Dyck PJ, Mulder DW. Natural history of brachial plexus neuropathy. Report on 99 patients. Arch Neurol 1972; 27:109 - 17. Aymond JK, Goldner JL, Hardaker WT. Neuralgic amyotrophy. Orthop Rev 1989;18:1275 - 9. Behar Y, Thiel H. Neuralgic amyotrophy. Eur J Chiropr 1994; 42:47 - 51. Billey T, Dromer C, Vedrenne C, Caulier M, Fournie B. Parsonage-Turner syndrome complicated by sympathetic dystrophy syndrome with adhesive capsulitis of the shoulder. Apropos of 2 cases. Rev Rhum Mal Osteo-artic 1992;59:765 - 7. Simotas AC, Tsairis P. Adhesive capsulitis of the glenohumeral joint with an unusual neuropathic presentation: a case report. Am J Phys Med Rehabil 1999;78:577 - 81.
59