Keywords: Nerve compression syndromes, Upper extremity, Median nerve, Radial nerve, Ulnar nerve, Ultrasonography

Introduction

The development of high-frequency linear array transducers has led to an improvement in the resolution of ultrasonography (US), and thus, US can nowadays satisfactorily depict most of the peripheral nerves. Therefore, US has been widely used, along with magnetic resonance imaging (MRI) and a nerve conduction study, in cases of common nerve compression syndromes or other neuropathic conditions including trauma. Although MRI is very accurate and superior for imaging soft tissues and nerves, it is expensive, takes more time, and may have artifacts. More importantly, MRI may not be practical when a number of nerves need to be examined over the long course [1]. Although US has a few limitations like a small field of view, limited penetration, and an anisotropic effect when imaging nerves [2], major nerves in the upper extremity can usually be visualized without much difficulty. US of peripheral nerves requires the use of transducers with high insonation frequencies (7-12 MHz or more). In this article, we review the anatomy and US features of the main nerves of the upper extremity and evaluate the clinical and US features of common nerve compression syndromes of the upper extremity.

Median Nerve

The median nerve arises from the medial and lateral cord of the brachial plexus and runs down along the medial side of the distal arm with the brachial artery and vein. It passes through the antecubital fossa deeply relative to the biceps aponeurosis (also called the lacertus fibrosus) and anterior to the brachialis muscle. It is located between the biceps brachii and the brachialis muscle at the elbow level. The nerve lies between the humeral (superficial) and ulnar (deep) heads of the pronator teres muscle at the level of the elbow joint [3]. Transverse US with a high-resolution linear array transducer (5-17 MHz) can demonstrate the normal median nerve between the two heads of the pronator teres muscle (Fig. 1). The anterior interosseous nerve (AIN) arises from the median nerve at the level of the humeral head of the pronator teres muscle and travels along the anterior aspect of the interosseous membrane of the forearm between the flexor pollicis longus (FPL) and the flexor digitorum profundus (FDP) muscles. The AIN is a purely motor nerve and supplies the pronator quadratus (PQ) muscle, FPL muscle, and radial-side FDP muscle. At US, the identification of the normal AIN may be difficult because of the deep location and small size of the nerve. After exiting the pronator teres muscle, the main median nerve enters the anterior compartment of the forearm by passing beneath the fibrous arch of the heads of the flexor digitorum superficialis muscle and runs down to the wrist level to enter the carpal tunnel.

Pronator Teres Syndrome

Pronator Teres Syndrome

Median nerve entrapment can occur around the elbow joint. The most common site of median nerve compression at the elbow level is between the two heads of the pronator teres muscle [3]. The patients having median nerve compression at this level may have pain and numbness in the volar side of the elbow and forearm. The hand symptoms may be similar to those in the case of carpal tunnel syndrome (CTS). This is called pronator teres syndrome. The causes of pronator teres syndrome may relate to trauma with hematoma, pronator teres muscle hypertrophy, or congenital abnormalities [4]. The demonstration of the causes of the pronator teres syndrome by US may be possible if there is a mass or hematoma causing compression of the median nerve. However, in the absence of such findings, it may not be easy to make a diagnosis or to find the cause of nerve compression with US, since the fibrous bands or scar tissue may be too small to visualize with US [5]. MRI can demonstrate the denervation muscle signal changes and determine the level of nerve compression [6].

AIN Syndrome (Kiloh-Nevin Syndrome)

AIN Syndrome (Kiloh-Nevin Syndrome)

AIN syndrome is caused by entrapment or compression of the AIN. The AIN innervates muscles in the deep anterior compartment of the forearm: FPL, radial-side FDP, and PQ. Lesions of the AIN can result in a variety of clinical symptoms, depending on the location and the degree of nerve damage [7]. Typically, the patients have motor disturbance in the function of the affected muscles and weakness of the thumb, index finger, and occasionally the middle finger. Therefore, patients with AIN syndrome have the characteristic circle sign; that is, these patients cannot form an “O” shape with their index finger and thumb due to the lack of innervation of the FPL and FDP of the index finger [4]. Some patients may have isolated weakness of the thumb because of the isolated involvement of the particular fascicle that innervates the FPL [8]. The causes of AIN syndrome can be external compression with hematoma or mass or direct nerve trauma [5]. However, some patients without direct trauma or demonstrable causes may have AIN syndrome. The AIN is usually compressed by fibrous bands, most commonly originating from the deep head of the pronator teres, flexor digitorum superficialis, and brachialis fascia [7]. Although US is usually limited for the evaluation of AIN syndrome because of the small size of the nerve and relatively deep location, US can identify the anterior interosseous artery at the volar aspect of the interosseous membrane by using color or power Doppler. The identification of the anterior interosseous artery helps in the evaluation of the lesion along the course of the AIN adjacent to the anterior interosseous artery [5]. In some cases, US may identify the small volume and denervation echo changes of the denervated muscles (Fig. 2).

Carpal Tunnel Syndrome

Carpal Tunnel Syndrome

CTS is the most common nerve compression syndrome in the upper extremity. The causes of CTS are diverse depending on the origin: tenosynovitis of flexor tendons (keyboard operator/inflammatory arthritis), space-occupying lesions such as ganglions or tumors (Fig. 3), nerve swelling related to thyroid disease or pregnancy, amyloid deposition, post-traumatic fibrosis, excess fat, anatomic variation such as a persistent median artery with or without a bifid median nerve (Fig. 4), and anomalous muscle [9]. In most cases, the diagnosis of CTS is usually made on the basis of typical clinical signs and symptoms, and an electrodiagnostic study is performed to confirm the diagnosis [9]. US has been used for patients with CTS as an additional diagnostic tool, since US can depict the morphological changes and size abnormalities of the median nerve and demonstrate the cause of nerve compression [10-15]. On US, the normal median nerve is round in the distal forearm, oval at the level of the pisiform, and flat at the level of the hook of hamate (Fig. 5) [16]. The most common US finding of CTS is the enlargement of the median nerve, and this is usually most prominent at the scaphoid-pisiform level. There have been many studies aiming to provide the most appropriate cutoff value of the median nerve cross-sectional area for the diagnosis of CTS [10-14,17]. By using the ellipse formula, researchers have suggested a cutoff value between 9 mm² and 10 mm² at the scaphoid-pisiform level as the diagnostic criteria of CTS with acceptable sensitivity and specificity [13,14,17,18]. According to Buchberger et al. [17,19], four characteristic findings can be found in patients with CTS: (1) a significant increase in the cross-sectional area of the median nerve at the level of the pisiform and, to a lesser degree, at the level of the hamate; (2) a significant increase in the cross-sectional area of the median nerve at the level of the pisiform as compared to that at the level of the distal radius (swelling ratio); (3) a significant increase in the flattening ratio at the level of the hook of hamate; and (4) significant palmar bowing of the flexor retinaculum (palmar displacement of the flexor retinaculum of more than 4 mm from the line between the hook of hamate and the tubercle of the trapezium). US could also reveal the hypoechoic change of the median nerve and the altered fascicular pattern caused by neural edema (Fig. 6). In addition, US is useful for the postoperative evaluation of CTS [20,21]. According to the studies by Ozturk et al. [20] and Apfelberg and Larson [21], US could reveal the decrease in the cross-sectional area of the median nerve after transverse carpal ligament release. US may demonstrate the causes of recurrent CTS after surgery (Fig. 7).

Ulnar Nerve

The ulnar nerve arises from the medial cord of the brachial plexus and runs down along the m0 level, the nerve penetrates the medial intermuscular septum to enter the posterior compartment and descends along the anterior and medial aspects of the triceps muscle. At the distal arm level, the ulnar nerve passes posterior to the medial humeral epicondyle and finally enters the cubital tunnel [3]. The cubital tunnel is a fibro-osseous channel formed by the olecranon process laterally, the posterior cortex of the medial epicondyle medially, the elbow joint capsule and posterior bundle of the medial collateral ligament anteriorly, and the cubital tunnel retinaculum (Osborne ligament) posteriorly [3]. The nerve exits the distal aspect of the cubital tunnel to enter the medial aspect of the forearm between the superficial and deep heads of the flexor carpi ulnaris (FCU) muscle. At the elbow level, the ulnar nerve gives off motor branches to the FCU and ulnar-side FDP muscles [4]. At the wrist level, it passes through another fibro-osseous canal called Guyon’s canal and branches into superficial sensory and deep motor nerves within the canal. High-resolution US can demonstrate the normal ulnar nerve at the level of the cubital tunnel and the wrist. The ulnar nerve is easy to identify in the cubital tunnel between the medial humeral epicondyle and the olecranon process with transverse US (Fig. 8). The elbow should be extended during the initial evaluation since the ulnar nerve may be dislocated or displaced anteriorly during elbow flexion (Fig. 9) [5]. According to the study of Ozturk et al. [20] on the ultrasonographic appearance of the normal ulnar nerve in the cubital tunnel in 212 elbows, 77.8% of the cases showed the ulnar nerve with one fascicle, and the rest showed two or three fascicles at the level of the cubital tunnel. The size and morphology of the ulnar nerve can differ with the elbow flexion position and the extension position [20,21]. During elbow flexion, 31.6% of ulnar nerves showed anterior displacement, and the volume of the cubital tunnel and the cross-sectional area of the ulnar nerve decreased [20]. At the level of Guyon’s canal, the hyperechoic cortex of the pisiform can be used as a landmark to find the ulnar nerve. The normal fibrillar pattern of the ulnar nerve is well demonstrated in Guyon’s canal with US, and bifurcation of the ulnar nerve is identified (Fig. 10).

Cubital Tunnel Syndrome

Cubital Tunnel Syndrome

Cubital tunnel syndrome is the second most common nerve compression syndrome in the upper extremity [4]. Cubital tunnel syndrome is caused by external compression or injury of the ulnar nerve within the cubital tunnel. The possible causes of this syndrome include bone fragments, loose bodies or the spur arising from the elbow joints, space-occupying lesions such as tumors, ganglia, hematomas, synovitis from the elbow joint, regional ligamentous inflammation, accessory muscle (anconeus epitrochlearis), and dislocation of the nerve. Patients with cubital tunnel syndrome may present medial elbow pain, numbness in the ring and little fingers, and weakness in the intrinsic hand muscles. Patients with chronic cubital tunnel syndrome may show a claw hand deformity due to muscle volume loss in the first interosseous space and hypothenar eminence and semi-flexion deformity of the ring and the little fingers [4]. The ultrasonographic appearance of cubital tunnel syndrome is the enlargement of the ulnar nerve at the level of the cubital tunnel, similar to CTS (Fig. 11). There have been several reports aiming to provide the cutoff value of the ulnar nerve cross-sectional area for the diagnosis of cubital tunnel syndrome [22-24]. According to these previous studies, the cutoff point of 10 mm² or higher for the cross-sectional area led to a sensitivity and specificity of more than 88% for the diagnosis of cubital tunnel syndrome [22,23]. Thoirs et al. [24] suggested a cutoff value for the crosssectional area of the asymptomatic ulnar nerve of 9 mm², derived as the upper limit of the 95% confidence interval. An additional study used a ratio of 1.5:1, comparing the ulnar nerve area at the level of the cubital tunnel with that proximal to the cubital tunnel, and the 8.3-mm² cross-sectional area of the ulnar nerve at the epicondyle level showed 100% sensitivity in the diagnosis of cubital tunnel syndrome [25]. The ulnar nerve in patients with cubital tunnel syndrome is usually hypoechoic in US because of neural edema. In cases of chronic cubital tunnel syndrome, US may identify the echogenic FCU and ulnar-side FDP muscles with small volume because of the muscle hypotrophy caused by chronic denervation.

Guyon’s Canal Syndrome

Guyon’s Canal Syndrome

Guyon’s canal is an oblique fibro-osseous tunnel with a length of about 4 cm between the hook of hamate and the pisiform. The borders of Guyon’s canal vary along its entire course and are not distinct [26]. The roof of the canal consists of the palmar aponeurosis, palmaris brevis, and hypothenar fibroadipose tissue; the floor is made up of the FDP tendons, transverse carpal ligament, pisohamate ligament, pisometacarpal ligament, and opponens digiti minimi; the medial wall is composed of the FCU tendon, the pisiform, and the abductor digiti minimi; and the lateral wall is formed by the extrinsic flexor tendons, the hook of hamate, and the transverse carpal ligament [27-29]. The contents of Guyon’s canal are the ulnar artery, nerve, communicating vein, and loose fibrofatty tissue. Guyon’s canal syndrome is a compressive neuropathy of the ulnar nerve at the level of Guyon’s canal. One cause of Guyon’s canal syndrome is related to trauma. Direct trauma may cause a nerve injury related to the compression between the external force and the hook of hamate [5]. Repetitive trauma to the hypothenar area by the handlebar can happen in cyclists and can cause Guyon’s canal syndrome. This is called cyclist’s palsy. “Hypothenar hammer syndrome” results from direct trauma to the ulnar artery between the hook of hamate and the palmaris brevis in those using jackhammers or people using vibratory tools occupationally [26]. Repetitive trauma to the ulnar artery can cause thrombosis and occlusion of the ulnar artery and resultant ulnar nerve compression (Fig. 12). Fracture of the hook of hamate or other carpal bones can also cause Guyon’s canal syndrome. A ganglion is one of the most common causes of Guyon’s canal syndrome [26], and other space-occupying lesions including tumorous conditions can cause ulnar nerve compression as well. Other causes of Guyon’s canal syndrome are anomalous muscles, abnormally thickened ligaments, and an anomalous course of the ulnar nerve [26]. US can identify the cause of Guyon’s canal syndrome and the morphologic change of the ulnar nerve (Fig. 13).

Radial Nerve

The radial nerve is the terminal branch of the posterior cord of the brachial plexus. At the arm level, it obliquely runs posterior to the humerus in the spiral groove. The radial nerve is closely attached to the posterior cortex of the humerus in the spiral groove, at this level (Fig. 14). At the level of the distal arm, the radial nerve pierces the intermuscular septum to enter the anterior aspect of the humeral lateral condyle. Anterior to the lateral epicondyle, the radial nerve divides into a superficial sensory branch and a deep motor branch [4]. The superficial sensory branch runs in the forearm along the deep surface of the brachioradialis muscle along with the radial artery. After bifurcation of the radial nerve, the deep motor branch enters the radial tunnel [3]. The radial tunnel extends from the level of the radiocapitellar joint to the level of the proximal aspect of the supinator muscle. The radial tunnel is bounded by the joint capsule posteriorly, the brachialis muscle and biceps tendon medially, and the brachioradialis muscle and the extensor carpi radialis brevis and longus muscles laterally. At the distal aspect of the radial tunnel, the deep branch pierces the supinator muscle and passes through the supinator muscle to enter the posterior compartment of the forearm (Fig. 15). Thereafter, the deep motor branch of the radial nerve leaves the supinator muscle; this branch is referred to as the posterior interosseous nerve (PIN). At the level of the upper arm, the radial nerve gives off branches to innervate the triceps and anconeus muscles. At the level of the radial tunnel, the radial nerve gives off branches to innervate the brachioradialis, extensor carpi radialis longus and brevis, and supinator muscles, in this order. After exiting the supinator muscle, the PIN innervates the dorsally located extensor muscles (the extensor digitorum, extensor carpi ulnaris, extensor digiti minimi, abductor pollicis longus, extensor pollicis brevis, extensor pollicis longus, and extensor indicis muscles) [30]. US can identify the normal radial nerve in the spiral groove, over the posterior aspect of the humerus (Fig. 14). The radial nerve in the radial tunnel is also easy to identify in the anterior elbow with transverse US. The fascicular pattern of the radial nerve can be seen in the fascial plane between the brachioradialis (laterally) and brachialis (deep medially) muscles [5]. When the radial nerve is traced down, the bifurcation of the radial nerve is seen. More distally, the deep motor branch can be followed with transverse US as it enters the supinator muscle. An oblique scan at the level of the supinator muscle can demonstrate the deep motor branch passing through the supinator muscle and continuing as the PIN (Fig. 16). The superficial branch of the radial nerve runs down along the deep portion of the brachioradialis and becomes superficial at about 9 cm proximal to the styloid process of the radius [31]. More distally, it divides into three separate branches. US is able to identify the superficial branch of the radial nerve crossing the first extensor compartment of the wrist (Fig. 17). At the level of the distal forearm, the superficial radial nerve lies close to the cephalic vein [32].

Radial Tunnel Syndrome and PIN Syndrome

Radial Tunnel Syndrome and PIN Syndrome

PIN syndrome is a compressive neuropathy of the deep branch of the radial nerve in the region of the supinator muscle [33]. It can have various etiologies. Most commonly, repetitive overuse of the forearm (repetitive pronation-supination or flexion-extension) can cause a radial nerve injury in this region [34]. This is common to athletes (tennis players). The thickened or hypertrophied anatomic structures can entrap the nerve, such as a thickened proximal tendinous edge of the supinator muscle (arcade of Frohse), thickened leading edge of the extensor carpi radialis brevis muscle, and distal ligamentous margin of the supinator muscle [30]. The arcade of Frohse is the most common area of compression. Other causes are space-occupying lesions (such as tumor/ganglion/bicipitoradial bursitis), prominent recurrent radial vessels, fascial band of the radial head, and systemic diseases such as diabetes, rheumatoid arthritis, polyarteritis, neuralgic amyotrophy, chronic hypoperfusion, and postsystemic illness angioneuropathy [35]. Clinical manifestation of the PIN syndrome varies depending on the level of nerve compression and the affected nerve fibers [34]. Compression of the deep branch of the radial nerve mostly causes painless palsy of the extensor muscles of the forearm. However, tenderness and pain at the lateral aspect of the proximal forearm mimicking lateral epicondylitis can be clinically presented without motor weakness in some patients. This is referred to as the “radial tunnel syndrome” (Fig. 18) [3]. The most commonly observed US finding of PIN syndrome is the enlargement of the PIN at the proximal portion of the compression site [33-37]. According to the study of Djurdjevic et al. [33] on high-resolution US findings in 13 patients with PIN syndrome, US was able to reveal the edema and caliber change of the PIN in all patients. Nine of these 13 patients underwent surgery in this study and intraoperative exploration showed PIN compression by the tight tendinous arcade of Frohse in all of the patients. The researchers also suggested a 15-mm cutoff value of the PIN diameter for the diagnostic criteria of PIN syndrome by comparison with a normal control group. US can also show the presence of hyperemia of the nerve on color Doppler imaging [37]. Rarely, space-occupying lesions causing PIN compression can be found with US. In addition, US may reveal an echo difference of the dorsal extensor muscles caused by denervation, as compared to the contralateral side.

Wartenberg’s Syndrome

Wartenberg’s Syndrome

Wartenberg’s syndrome is an entrapment neuropathy of the superficial branch of the radial nerve at the level of the distal forearm and wrist [32]. The patients present with pain, numbness, and paresthesia in the radial-side wrist and thumb. Therefore, de Quervain’s disease and intersection syndrome should be differentiated. The superficial branch of the radial nerve is easily injured by trauma. The nerve can be injured during the placement of fixator pins due to Colles fractures. The superficial branch of the radial nerve injury by penetrating trauma, and cephalic vein cannulation are also reported [38]. Some physical activities require forearm pronation with simultaneous flexion and ulnar deviation of the hand predisposed to superficial radial nerve entrapment between the brachioradialis muscle and the extensor carpi radialis longus muscle [32]. Wartenberg’s syndrome is commonly associated with de Quervain’s disease, although the reason for this is not yet known [31]. US is helpful in distinguishing Wartenberg's syndrome from de Quervain's disease or arthritis of the trapeziometacarpal joint [32]. High-resolution US may depict the abnormal changes of the superficial branch of the radial nerve [5,31,32,33]. US in patients with Wartenberg’s syndrome can show secondary nerve compression from the adjacent scar tissue or post-traumatic/postoperative changes of the soft tissue. These changes could appear as abnormal heterogeneous hypoechoic tissue [5].

Conclusion

High-resolution US is a useful method of examination for the evaluation of peripheral nerves, particularly the median, ulnar, and radial nerves of the upper extremity. However, the quality of US may differ depending on the examiner’s knowledge. The anatomic location and normal ultrasonographic appearances of the peripheral nerves should be noted when the US exam is performed. Radiologists should also inform themselves about common nerve compression syndromes in the upper extremity and their causes to make an accurate assessment of the disease.

NOTES

No potential conflict of interest relevant to this article was reported.

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