OVERVIEW

CERVICAL RADICULOPATHY: PATHOPHYSIOLOGY, PRESENTATION, AND CLINICAL EVALUATION

Khalid M. Abbed, M.D. CERVICAL RADICULOPATHY IS a common condition that usually results from compres- Department of Neurosurgery, sion and inflammation of the cervical nerve root or roots in the region of the neural Massachusetts General Hospital, foramen. It is frequently caused by cervical disc herniation and cervical spondylosis. The Harvard Medical School, Boston, Massachusetts diagnosis can be established by history and physical examination, but care should be taken, as diagnoses can mimic or coexist with cervical radiculopathy, such as entrap- Jean-Valéry C.E. Coumans, M.D. ment neuropathies. The pathophysiology, presentation, and clinical evaluation of cer- Department of Neurosurgery, vical radiculopathy are discussed. Massachusetts General Hospital, Harvard Medical School, KEY WORDS: Cervical spine, Cervical spondylosis, Nerve root, Radiculopathy Boston, Massachusetts Neurosurgery 60[Suppl 1]:S-28–S-34, 2007 DOI: 10.1227/01.NEU.0000249223.51871.C2 Reprint requests: Jean-Valéry C.E. Coumans, M.D., Department of Neurosurgery, Massachusetts General Hospital, ervical spondylosis is a term used to or extraspinal tumors, trauma with nerve root 15 Parkman Street, WACC 021, describe the degenerative aging process avulsion, synovial cysts, meningeal cysts, dural Boston, MA 02114. that encompasses a sequence of changes arteriovenous fistulae (19), or tortuous vertebral Email: [email protected] C in the intervertebral discs, vertebral bodies, arteries (16). Cervical radiculopathy may also facet joints, and ligaments of the cervical spine. occur without an identifiable cause. Other condi- It is a common condition that occurs as a natu- tions that can mimic cervical radiculopathy, ral consequence of aging in the majority of the which should be included in the differential adult population. As a result, it is often difficult diagnosis, are upper extremity nerve entrap- to distinguish normal physiological degen- ment, primary shoulder disease, brachial plexus eration from pathological changes. Anatomic disorders, and peripheral neuropathies. This changes should only be considered pathologi- article focuses on radiating pain secondary to cal if they are etiologically related to specific compression of cervical nerve roots by herniated clinical syndromes. disc material or pain that is associated with cer- There are three main categories of cervical vical spondylosis. spondylosis: cervicalgia (non-radiating neck pain), cervical radiculopathy, and cervical PATHOPHYSIOLOGY myelopathy. This article concerns the patho- physiology, presentation, and clinical evalua- The cervical intervertebral disc is taller ven- tion of cervical radiculopathy and the spectrum trally than dorsally, and it is the cervical disc, of radicular syndromes attributable to cervical not the vertebral body, that is responsible for spine degenerative disease. Cervicalgia and the maintenance of cervical lordosis. The outer myelopathy, which are commonly associated portion of the disc is made up of the anulus with radiculopathy and the treatment of cervi- fibrosus. The latter is crescent-shaped, and, cal radiculopathy, are covered elsewhere in this when viewed in the axial plane, it is thicker issue. ventrally than dorsally. Ventrally, it is multil- Cervical radiculopathy is a pathological aminated with interweaving fibers of alternat- process involving the cervical nerve root. It is ing orientation, but dorsally, it is only present the result of compression and inflammation of as a thin layer of collagen fibers (23). Before the nerve root or roots at or near the cervical the age of 20 years, few morphological changes neural foramen (Fig. 1–3). It occurs annually in occur in the cervical spine. Beginning in the 85 out of 100,000 people (22). The most com- third decade of life, a progressive decline in mon causes for radiculopathy are cervical disc the water content of the intervertebral disc herniation (Fig. 2 and 3) (17), followed by cervi- occurs and continues with age. The nucleus cal spondylosis (Fig. 1) (1, 35). Cervical radicu- pulposus becomes an indistinct fibrocartilage- lopathy is less commonly caused by intraspinal nous mass (29). In patients younger than 30

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AB ing the lumbar disc. In the cer- vical spine, true disc prolapse and herniation of the nucleus pulposus is uncommon (23). The neural foramen is bor- dered ventrally by the unco- vertebral joint and dorsally by the superior articular process of the caudal vertebra (2). Compressive radiculo- FIGURE 3. Axial T2 MRI demon- FIGURE 1. Axial T2 MRI image (A) and CT scan (B) in a patient with a left pathies occur as a result of strating C7–T1 disc herniation in a C6 radiculopathy. There is a left-sided C5 to C6 osteophyte causing neural mechanical distortion of the patient with a left-sided C8 radicu- lopathy. The patient was referred after foraminal stenosis and C6 nerve root compression. nerve root by either the unsuccessful attempted dorsal resec- hypertrophied facet joint or tion of the disc. uncovertebral joints (Fig. 1), A B disc protrusion (Fig. 2 and 3), spondylotic spurring of the verte- bral body, or a combination of these factors. Pressure on the nerve root may lead to sensory deficits, motor weakness, or radicular pain. Pain is related to mechanical compression and to an inflammatory response.

PRESENTATION

Radiculopathy can be divided into acute, subacute, and chronic. Acute cervical radiculopathy occurs in relatively FIGURE 2. A, parasagittal reformat young patients in the setting of a tear in the annulus fibrosus of CT myelogram and axial CT mye- and subsequent prolapse of the nucleus pulposus. Subacute logram (B) demonstrating a left- radiculopathy occurs in patients with pre-existing cervical sided C6–C7 disc herniation in a spondylosis, without persistent symptoms except for occa- patient who was unable to have an sional neck pain. Patients develop insidious symptoms, which MRI scan due to prior aneurysm clip are often polyradicular in nature. Chronic radiculopathies placement. materialize from acute or subacute radiculopathies that have failed to respond to treatment. Pain is most prominent in acute cervical radiculopathy and years, the water content of the intervertebral disc approaches diminishes as the condition becomes more chronic. It may be 90%, and it decreases to less than 70% by the eighth decade of life. described as sharp, achy, or burning and may be located in the The basic structural unit of the nucleus pulposus is glycosamino- neck, shoulder, arm, or chest, depending on the nerve root glycan protein, which consists of a proteoglycan protein core and involved. Classically, an acute radiculopathy presents with pain bulky, sterically active polysaccharide attachments of chondroitin radiating in a myotomal distribution. For example, patients with sulfate and keratin sulfate. Because of their high molecular a C7 radiculopathy often experience pain in the triceps region weight and overall negative charge, glycosaminoglycan proteins rather than the distal dermatomal region. Sensory symptoms, have a strong attraction for water molecules. With aging, these predominantly parasthesias and numbness, are more common large, sterically active glycosaminoglycan proteins gradually than motor loss and diminished reflexes. The clinician should diminish in size and number. As a result, the intervertebral disc’s keep in mind that the sensory symptoms frequently do not match ability to retain water also diminishes. These age-related changes the dermatomes illustrated in medical textbooks. Henderson et al. in the chemical composition of the nucleus pulposus and annu- (13) reviewed the clinical presentations of cervical radiculopathy lus fibrosus cause the degenerated disc to become more com- in more than 800 patients and found arm pain in 99.4%, sensory pressible and less elastic (3). Consequently, the disc loses height deficits in 85.2%, neck pain in 79.7%, reflex deficits in 71.2%, and bulges dorsally into the spinal canal. As the vertebral bodies motor deficits in 68%, scapular pain in 52.5%, anterior chest pain drift toward one another (i.e., subsidence), the ligamentum in 17.8%, headaches in 9.7%, anterior chest and arm pain in 5.9%, flavum and facet joint capsule fold in dorsally, causing a further and left-sided chest and arm pain in 1.3%. decrease in the canal and foraminal dimensions. This approxima- Radicular pain is often accentuated by maneuvers that stretch tion of adjacent vertebral bodies leads to a reactive process that the involved nerve root, such as coughing, sneezing, Valsalva, produces osteophytes around the disc margins and at the and certain cervical movements and positions. Several clinical uncovertebral and facet joints. However, the degenerative signs suggestive of radiculopathy have been described. changes of the cervical intervertebral disc differ from those affect- Davidson et al. (9) described the “shoulder abduction sign” in

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which the patient experiences significant relief of arm pain with unexplained pain along the base of the neck that radiates to the shoulder abduction. The patient holds the arm over the head superior aspect of the shoulder and posteriorly to the scapula. and typically rests the wrist or forearm on the top of the head. The rhomboid, trapezius, and levator scapulae muscles are The Spurling test is a maneuver that provokes the patient’s arm supplied, in part, by the fourth nerve root, but a motor deficit pain with induced narrowing of the neural foramen. It is per- may be hard to detect. A sensory deficit may be present over formed by extending the neck and rotating the head to the side the anterolateral aspect of the neck, along the distribution of the of the pain and then applying downward pressure on the head. transverse cervical and supraclavicular nerves. The C3, C4, and The test is thought to cause a narrowing of the intervertebral C5 nerve roots innervate the diaphragm. Involvement of these foramina and is considered positive if the limb pain or paresthe- three nerve roots may lead to diaphragmatic weakness (6, 7). sia is provoked with the maneuver. This test has been found to Radiculopathy of the fifth cervical nerve root results from be specific, but not sensitive, for cervical radiculopathy (33). pathology at the C4–C5 level. Patients often present with numb- The type and location of the radicular symptoms are deter- ness and localized shoulder pain that can be confused with a mined by the level at which the cervical nerve root compres- pathological shoulder condition (Table 2) (2). When it is due to sion occurs (Table 1). Radiculopathy of the third cervical nerve a rotator cuff tear, shoulder disease can present with weakness root results from pathological changes between the C2 and C3 of abduction and external rotation. However, unlike pain from vertebrae and is not common. Patients may experience pain in primary shoulder disease, radicular pain is not significantly the suboccipital region, often extending to the back of the ear, affected by motion of the shoulder. The numbness follows the and in the dorsal or lateral aspect of the neck. This pain is often C5 sensory distribution, which is located over the top of the difficult to distinguish from other causes of headache. shoulder along its midportion, and extends laterally to the mid- Numbness may be present along the occiput and in the distri- portion of the arm. The principal motor deficit is supraspinatus bution of the great auricular and lesser occipital nerves. and deltoid muscle weakness with impaired shoulder abduc- Although the third cervical nerve root supplies, in part, the tion. Weakness of the clavicular head of the pectoralis major, suboccipital muscles, the trapezius, the levator scapulae, the biceps, and infraspinatus muscles can also occur. The pectoralis sternocleidomastoid, and the strap muscles, an isolated motor reflex and the biceps reflex, which are innervated by the fifth deficit generally cannot be detected clinically. and sixth cervical nerve roots, may be decreased. Radiculopathy of the fourth cervical nerve root results from Compression of the C6 nerve root is the second most common pathological changes between the C3 and C4 vertebrae and is cause of cervical radiculopathy and results from disc herniations more common than a C3 radiculopathy. It may be a cause of or spondylosis at the C5–C6 level. Patients present with pain

TABLE 1. The cervical radicular syndromes Nerve root Dermatome Myotome Reflex C3 Supraclavicular, suboccipital, and Trapezius, levator scapulae, strap muscles, None posterior auricular regions sternocleidomastoid, diaphragm C4 Infraclavicular and posterior Trapezius, rhomboids, levator scapulae, diaphragm None cervical regions, posterior shoulder C5 Superolateral aspect of the arm Pectoralis major (clavicular head), supraspinatus, Pectoralis, biceps infraspinatus, deltoid, biceps, brachialis, brachioradialis, diaphragm C6 Lateral arm and forearm, thumb and Biceps, brachialis, brachioradialis, extensor carpi radialis Biceps, brachioradialis index finger longus, supinator, pronator teres, flexor carpi radialis, triceps C7 Posterolateral arm and forearm, Triceps, latissimus dorsi, pronator teres, flexor carpi Triceps middle finger radialis, extensor carpi ulnaris, extensor digitorum, abductor pollicis longus, extensor pollicis brevis and longus, extensor indicis C8 Medial arm and forearm, fourth and Flexor digitorum superficialis, pronator quadratus, flexor None fifth digits digitorum profundus, flexor pollicis longus, flexor carpi ulnaris, lumbricals 3 and 4 T1 Axillary and pectoral region, medial Adductor pollicis, abductor pollicis brevis, opponens None arm and proximal medial forearm pollicis, flexor pollicis brevis, interossei, lumbricals 1 and 2. Horner’s syndrome may be present

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TABLE 2. Conditions that can mimic specific cervical radicular syndromes Nerve root Entity mimicking radiculopathy Differentiating factor C5 Rotator cuff tear Both present with weakness of abduction, but the rotator cuff tear is not associated with weakness of other C5 innervated muscles. C5 radiculopathy not associated with painful shoulder movement or significant tenderness C5 Suprascapular nerve entrapment Suprascapular nerve entrapment is not associated with weakness of other C5 innervated muscles, such as the deltoid, biceps, and pectoralis major

C6 or C7 Carpal tunnel syndrome Carpal tunnel syndrome is associated with nocturnal dysesthesias, and the hypoesthesia is present distally, over the palmar side of the hand and over the first three to three and one- half digits. There can be weakness and atrophy of the thenar and first two lumbrical muscles, which are innervated by C8 and T1. Phalen’s test may be positive, and Tinel’s sign may be present C7 Posterior interosseus nerve Posterior interosseus nerve compression is not associated with sensory findings and does compression not affect the triceps, pronator teres, and flexor carpi radialis

C8 Anterior interosseus nerve Anterior interosseus nerve entrapment usually presents with pain over the proximal entrapment forearm and may have a positive “pinch sign” because of weakness of flexion at the interphalyngeal thumb joint and at the distal interphalyngeal joint of the index. There is no sensory loss with anterior interosseus nerve compression C8 Ulnar entrapment at the elbow Entrapment at the level of the elbow may cause clinical tenderness along the medial aspect of the elbow; may have positive Tinel’s sign. C8 radiculopathy is associated with weakness of the pronator quadratus and flexor digitorum superficialis and of the first two flexor digitorum profundus muscles, which are innervated by the median nerve. Sensory change does not extend proximal to the wrist in ulnar nerve entrapment

and/or numbness radiating from the neck to the lateral aspect Electrodiagnostic studies may be necessary to evaluate periph- of the biceps, the lateral aspect of the forearm, the dorsum of the eral nerve function to differentiate entrapment syndromes from hand at the web space between the thumb and index finger, cervical radiculopathies. and into the tips of those digits. Motor deficits in the wrist To complicate matters, entrapment syndromes may coexist extensors and biceps are common. Weakness of the supinator, with cervical radiculopathy. This is known as the “double pronator teres, and triceps muscles may be present. The brachio- crush” phenomenon and was first described by Upton and radialis and biceps reflexes may be decreased or absent. The McComas (32) in 1973. According to this hypothesis, a proximal pain and paresthesias of C6 radiculopathy may mimic carpal injury along an axon, such as a cervical root lesion, causes tunnel syndrome, which is caused by median nerve entrapment impaired axoplasmic flow, which predisposes affected axons to at the wrist by the transverse carpal ligament. injury at a more distal site. Upton and McComas found that in Unlike cervical radiculopathy, upper limb nerve entrapments, 81 out of 115 cases of carpal tunnel syndrome, there was an such as carpal tunnel syndrome, are characterized by pain, associated cervical radiculopathy as well. However, more paresthesia, and weakness in multiple nerve root distributions. recently, Morgan and Wilbourn (26) retrospectively studied Referred pain with entrapment neuropathy, however, is com- 12,736 cases of carpal tunnel syndrome and ulnar neuropathy mon and pain can radiate proximally to the site of entrapment. at the elbow and found that 435 of these cases (3.4%) had a Compression of the median nerve at the wrist, for example, coexisting cervical root lesion. However, in only 98 (0.8%) of may cause referred pain to the arm and even to the neck. Carpal these cases were the lesions on the same nerve. tunnel syndrome is characterized by nocturnal dysesthesias, Most studies that employ clinical examination to diagnose weakness, and, occasionally, thenar atrophy. The thenar and cervical radiculopathy have demonstrated the seventh cervical first two lumbrical muscles are innervated via the median nerve nerve root to be the most frequently involved in cervical by the C8 and T1 nerve roots. The sensory loss in carpal tunnel radiculopathy (12, 15, 30). It is caused by degenerative changes syndrome is located over the palmar side of the hand and over at the C6–C7 level. The patient may present with pain and/or the first three digits. Weakness and atrophy are late findings and numbness radiating across the back of the shoulder, over the predominantly involve the abductor pollicis brevis muscle. The triceps, the dorsolateral aspect of the forearm, and over the symptoms of carpal tunnel syndrome are often reproduced with dorsum of the long finger. Triceps weakness can be significant, Phalen’s test, and Tinel’s sign may be present at the wrist. but may not be noticed by the patient until it becomes severe,

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perhaps because gravity aids in extension of the forearm. The Plain Films latissimus dorsi muscle, wrist flexors, and finger extensors may Historically, clinicians have used cervical spine plain films to also be involved. The motor symptoms of C7 radiculopathy infer nerve root compression by the presence of degenerative may be confused with entrapment of the posterior interosseus changes; however, it has been shown that degenerative changes nerve, which may present with weakness in the extensor digi- within the cervical spine are age-related and present in asymp- torum, extensor pollicis longus, brevis, and extensor carpi tomatic as well as symptomatic individuals (4, 11, 14, 34). ulnaris muscles. Notably, entrapment of the posterior inter- Despite the poor correlation between the clinical symptoms of osseus nerve does not cause sensory changes, and the triceps patients and the degenerative cervical spine, plain films remain and wrist flexors are not affected. In C7 radiculopathy, the tri- an important screening tool in the evaluation of patients present- ceps reflex may be diminished or absent. ing with neck and limb symptoms. They are inexpensive, read- Nerve root compression at the C7–T1 level causes radicu- ily available, and provide information regarding sagittal bal- lopathy of the eighth cervical nerve root. This usually manifests ance, congenital abnormalities, fractures, deformity, and with symptoms extending over the medial aspect of the arm instability. Flexion-extension lateral cervical spine radiographs and forearm and into the medial hand and the last two digits. can disclose occult instability that may be the cause of intermit- Numbness usually involves both the dorsal and volar aspects tent or positional symptoms. Because plain films cannot visual- of the digits and hand and may extend proximal to the wrist ize neural structures, either directly or indirectly, other diagnos- over the medial aspect of the forearm. Unlike a T1 radiculopa- tic modalities, including myelography, computed tomography thy, the sensory findings produced by the C8 nerve root syn- (CT), and magnetic resonance imaging (MRI), are more com- drome do not extend to the axillary region (25). The C8 nerve monly used in the evaluation of nerve root compression. root innervates the small muscles of the hand, particularly the interossei, and the flexors and extensors of the wrist and fingers Myelography (with the exception of the flexor carpi radialis and extensor carpi radialis muscles). Thus, patients complain of difficulty Neural compression is diagnosed indirectly with myelogra- using their hands for routine daily activities. Compression of phy by observing changes in the contour of a contrast-filled the C8 nerve root may initially be difficult to differentiate from spinal canal. Today, water-soluble contrast agents are used. ulnar entrapment at the elbow. C8 nerve root compression may These are associated with less toxicity and enable improved affect the function of the flexor digitorum profundus in the visualization of neural structures compared with the original index and long fingers, the flexor pollicis longus in the thumb, oil-based agents. The major disadvantage of plain myelography and the pronator quadratus, but these muscles are not affected is its invasive nature. Because the diagnosis of neural compres- by entrapment of the ulnar nerve. Also, the short thenar mus- sion is inferred only indirectly, the exact nature of the com- cles, except for the adductor pollicis, may be involved with C8 pression is not always clear. For example, with myelography or T1 compression but are spared with ulnar nerve involve- alone, it can be difficult to distinguish between a “hard disc” ment. Furthermore, sensory changes seen with ulnar neu- with bony osteophytes and a “soft disc” herniation. Because ropathies include numbness, tingling, and/or pain in the plain myelograms do not rely on the sagittal or coronal recon- fourth and fifth fingers and the hand just below these fingers, struction of an axially acquired image, excellent spatial resolu- but not proximal to the wrist (medial antebrachial cutaneous tion is achievable with these images. nerve distribution), as may be seen with C8 radiculopathy. Accuracy rates for water-soluble nonionic cervical myelogra- Anterior interosseus nerve entrapment may also mimic C8 or phy in the diagnosis of clinical nerve root compression ranges T1 radiculopathy but lacks sensory changes, and thenar muscle between 67% and 92% when compared with intraoperative involvement is absent. findings (8, 24, 31). Myelography was associated with no false- T1 radiculopathy is uncommon but has been reported in positive results, a 15% false-negative rate, and an overall accu- association with T1-T2 disc herniations (25). Intrinsinc hand racy rate of 85% in a study of 53 patients who had surgical muscle weakness is common because the T1 root is the main confirmation of the cervical spine pathology (15). contributor to the adductor pollicis, the thenar muscles, and to the interossei and first two lumbricals. Axillary numbness is Computed Tomography common, and Horner’s syndrome can occur ipsilaterally. Unlike myelography, CT allows for the direct visualization of pathology causing compression of neural structures. Compared CLINICAL EVALUATION to myelography, CT emits less radiation, has improved visual- ization of lateral pathology, such as foraminal stenosis, has no The diagnosis of cervical radiculopathy depends on the cor- significant adverse reactions, and can visualize structures relation of the history and physical examination with radi- above or below myelographic blocks (2). CT also has a high ographic imaging studies. The value of these imaging studies spatial resolution and is especially helpful in visualizing the as an adjunct to the diagnosis and treatment of patients with foraminal region. Another important advantage of CT is that it cervical radiculopathy depends on their accuracy associated can distinguish neural compression caused by soft tissue from with demonstrating the precise anatomic features of the nerve compression related to bony structures, such as facet hypertro- root compression. phy. This is a major advantage from a surgical planning per-

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spective. The main disadvantage of CT is the partial volume noted in the paraspinal musculature before they become appar- averaging effect and streak artifacts. These can cause distortion ent in the appendicular muscles. EMG may be normal in the of images, particularly at the lower cervical levels, or in indi- presence of mild radiculopathy or a predominantly sensory viduals with wide shoulders. radiculopathy and are less likely to be positive in patients with The reported accuracy of CT of the cervical spine ranges no demonstrable weakness (28). Nerve conduction studies and from 72 to 91% (10). By combining myelography with com- EMG have been shown to be useful in diagnosing nerve root puted tomography (CT myelogram), the diagnostic accuracy dysfunction and distinguishing cervical radiculopathy from has approached 96% (18, 20). When there is a discrepancy other lesions that are unclear on physical examination (22). between the findings found via myelography and those found They have also been found to correlate well with findings on via CT myelography, CT myelography generally has been myelography and surgery (35). A reference chart detailing the found to be more accurate (27), although other authors have results of needle electrode examination of upper extremity found the two to be comparably useful (31). muscles in patients with surgically proven solitary root lesions has been published (21). Magnetic Resonance Imaging Because magnetic resonance imaging (MRI) can detect the CONCLUSION neural structures directly and non-invasively, it has become the most common method of imaging the cervical spine to Cervical radiculopathy is usually the result of disc herniation detect significant pathology (22). The accurate assessment of or cervical spondylosis and is a common cause of upper disc herniations and spinal stenosis is due to the intrinsic con- extremity symptoms. A thorough history and neurological trast and good spatial resolution. Brown et al. (5), in a blinded, examination, combined with confirmatory radiographic and retrospective review, studied 34 patients who underwent MRI electrodiagnostic studies enable accurate localization of the prior to surgery. MRI correctly predicted 88% of the lesions as pathology and allow the exclusion of other common causes of opposed to 81% for CT myelography, 57% for plain myelogra- upper extremity dysfunction, such as shoulder pathology and phy, and 50% for CT. Disc herniations are commonly observed entrapment neuropathies. with MRI scans of asymptomatic individuals (22). They may be observed in 10% of asymptomatic people younger than REFERENCES 40 years of age and 5% of those older than 40 years of age. 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