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Ultrasonography of peripheral nerves
Ultrasonography of Peripheral Nerves Carlo Martinoli, Stefano Bianchi, and Lorenzo E. Derchi With recent improvements in ultrasound (US) imaging equipment and refinements in scanning technique, an increasing number of peripheral nerves and related pathologic conditions can be identified. US imaging can support clinical and electrophysiologic testing for detection of nerve abnormalities caused by trauma, tumors, and a variety of nonneoplastic conditions, including entrapment neuropathies. This article addresses the normal US appearance of peripheral nerves and discusses the potential role of US nerve imaging in specific clinical settings. A series of US images of diverse pathologic processes involving peripheral nerves is presented. Copyright © 2000 by W.B. Saunders Company
HE DIAGNOSIS of peripheral neuropathies has traditionally relied upon information obtained from the clinical history, physical examination, and electrodiagnostic studies. In the past, these clinical methods were the only tests available. In fact, before the 1970s, radiographic studies of peripheral nerve lesions were limited to conventional plain-film radiography to evaluate for secondary skeletal changes. Direct imaging of peripheral nerves only became possible with the development of cross-sectional imaging techniques, such as ultrasound (US), CT, and MRI. In the1990s, the development and continuing improvement of US technology provided the means for precise, noninvasive diagnosis of musculoskeletal abnormalities in a variety of clinical settings.l.2 The applications of US in the musculoskeletal system have increased rapidly, and the use of US in routine clinical practice has become commonplace, influencing the diagnosis and the clinical management in the symptomatic patient. Current high-end US systems equipped with modern linear array transducers in the 5 to 15 MHz range have given radiologists the opportunity to generate highconspicuity images of most nerves in the body. These instruments permit the delineation of the normal fascicular structure of peripheral nerves, the recognition of specific and sometimes treatable abnormalities, the differentiation of endoneural and extraneural tumors, the evaluation of the extent of lesions, and the assessment of involved nerves at follow-up examination. 3 Other appropriate methods for noninvasive diagnosis of nerve disorders are currently available, particularly MRI and MR neurography, which combines fat and flow suppression with T2weighting and 3D reconstruction.4,5 Although sophisticated advances in MRI have recently enhanced both resolution and conspicuity of nerve structures, MRI is expensive, time-consuming and not readily available for routine clinical use. Con-
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versely, high-resolution US, in experienced hands, provides economic and noninvasive imaging, is quick to perform, and provides specific advantages over MRI, including the ability to explore long segments of nerve trunks in a single study, and the ability to examine tissues in both static and dynamic states. This article discusses the diagnostic capabilities and limitations of US in the study of peripheral nerves. It reviews and illustrates the current role of peripheral nerve sonography, and compares US with other diagnostic methods. ANATOMIC CONSIDERATIONS
High-frequency linear array transducers are needed to scan peripheral nerves. The central frequency varies from 7.5 to 15 MHz, depending on the patient's body habitus and the equipment used. When examined with these transducers, peripheral nerves show a peculiar arrangement of their internal structure, made of multiple hypoechoic parallel linear areas separated by hyperechoic bands (Fig 1A). 6 On transverse scans, nerves have a honeycomb-like appearance, with hypoechoic, rounded areas embedded in a hyperechoic background (Fig 1B). 6 Histologic correlation has shown that the hypoechoic structures correspond to the neuronal fascicles that run longitudinally within the nerve, and the hyperechoic background relates to the interfascicular epineurium (Fig IC). 6 The outer boundaries of nerves are usually undefined, because of a similar hyperechoic
From Cattedra "R" di Radiologia--Universitgt di Genova, Genova, Italy and the Division de Radiodiagnostic--HOpital Cantonal Universitaire, Geneve, Switzerland. Address reprint requests to Carlo Martinoli, MD, Cattedra "R" di Radiologia--Universith di Genova, Largo Rosanna BenzL 8. 1-16132, Genova, Italy. Copyright © 2000 by W.B. Saunders Company 0887-2171/00/2103-0004510.00/0 doi: 10.1053/suit.2000. 8562
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Fig 1. US appearance of normal nerves (12 to 5 MHz US image of MN at the middle third of forearm). (A) In a long axis view, the nerve (arrows) is composed of parallel linear hypoechoic areas separated by hyperechoic bands. (B) in a transverse (short axis) view, the nerve (arrows) is characterized by rounded hypoechoic areas (asterisk) in a hyperechoic background. (C) A transverse histologic cross-section of a bovine sciatic nerve shows the nerve fascicles (asterisk) that correlate well with the hypoechoic rounded areas seen in image B.
MARTINOLI, BIANCHi, AND DERCHI
appearance of both the superficial epineurium and the surrounding fat. A careful scanning technique based on precise knowledge of nerve position and analysis of the anatomic relations of the nerve with surrounding structures is essential for the identification of peripheral nerves with US. Systematic scanning in transverse planes is preferred, to follow the nerves along their course throughout the limbs. Longitudinal scans are less useful for following peripheral nerves, because the nerve fascicles might easily be confused with echoes from muscles and tendons coursing along the same plane. Color Doppler can aid in differentiating between the hypoechoic nerve fascicles and adjacent small vessels. The visualization of nerves with US primarily depends on their size and course. Current US equipment is able to confidently identify almost all the main nerve trunks running in the limbs and extremities, including the median, ulnar, and radial nerves in the upper limbs, and the sciatic, common peroneal, and posterior tibial nerves in the lower limbs. 6,7 Evaluation of the brachial plexus is also feasible, although US is not able to depict its roots and cords as completely and reliably as MRI. 8,9 Because of problems of access, US cannot visualize the epidural space, the C8 and T1 roots, and variable portions of the brachial plexus trunks behind the clavicle and in the infraclavicular region. With the exception of the vagus, recurrent laryngeal nerves in the neck, 1° and the femoral nerve in the retroperitoneum, 11 the cranial nerves, the nerve roots exiting the dorsal, lumbar and sacral spine, the sympathetic chains, and the splancnic nerves in abdomen cannot be examined with US,
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either because they are positioned too deeply or because of interposed bony structures. Given the characteristic US appearance of normal nerves, some anatomic variants such as anomalous branching and congenital anomalies can be recognized with US. Among these are the fusiform enlargement of the median nerve (MN) at the distal forearm and through the palm caused by fibrofatty tissue in patients with macrodactyly (fibrolipomatous hamartoma). 12-14 Also visible is the striking hypertrophy of peripheral nerves that occurs in the Charcot-Marie-Tooth syndrome (hereditary motor and sensory neuropathy type I and II).15 ENTRAPMENT NEUROPATHIES Damage to a peripheral nerve by pressure results in a compression neuropathy. This might occur at several points along the course of a nerve, although the involvement by extrinsic causes is more common at narrow anatomic passageways such as osteofibrous canals, abnormal bands of muscle, and connective tissue or bony ridges that tether the nerve. Although the diagnostic evaluation of nerve compressive syndromes basically relies on clinical features and electrophysiological testing, these studies only indicate the level of the lesion. They do not provide spatial information about the nerve or its surroundings that could help in determining the etiology of neuropathy. Direct visualization of nerve abnormalities with imaging modalities might enhance the diagnosis and the surgical result by providing exact information on the nature of constricting findings, especially in cases with confusing clinical pictures or equivocal or contradictory functional studies. Although MRI has been established as a useful imaging technique in this field, high-resolution US is now increasingly proposed as an efficient and low-cost alternative. Until now, most of the experience with US has been focused on carpal tunnel syndrome. ~2,16,17US criteria for MN compression at the carpal tunnel include a classic triad of findings: (1) flattening or deformity of the nerve at the hamate level (distal tunnel), (2) swelling of the nerve at the pisiform level (proximal tunnel) or at the distal radius, and (3) palmar bowing of the flexor retinaculum 12A6,17 (Fig 2). Reduced transverse sliding movement of the nerve beneath the retinaculum during flexion and extension of the index finger also might be observed. 12,18 Because the nerve shape is variable through the tunnel, measurement indices have been
® Fig 2. Carpal tunnel syndrome. (A) Longitudinal 8 to 15 MHz US scan shows extensive flattening (straight arrows) of the MN in the carpal tunnel and swelling of the nerve proximal to the compression point (curved arrow). FT, flexor tendons. (B) Transverse US image at the distal radius. The MN is markedly enlarged. (C) Transverse US image at the distal tunnel. The MN (open arrow) is reduced in size, and the shape of the overlying flexor retinaculum (arrowheads) is convex.
introduced to better assess nerve swelling. Among these, a nerve cross-sectional area greater than 0.09 cm 2 at the level of pisiform is currently reported as the best criterion for MN swelling. 19 Interestingly, it has been shown that the area of the MN measured by US correlates well with the severity of electromyographic findings. 2° Similarly, a larger crosssectional area of the ulnar nerve at the medial
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epicondyle occurs in patients with the cubital tunnel syndrome. 21This finding suggests that quantitative analysis with US might be applied equally well in the diagnosis of nerve compressive syndromes at sites other than the carpal tunnel. Extrinsic causes for nerve entrapment, such as tenosynovitis, ganglia, and soft-tissue masses, might be identified with US. 12,22-25If the patient's symptoms are not typical, US can be an effective means for exploring the entire course of the MN to rule out other more proximal sites of compression. Furthermore, in the carpal tunnel syndrome, US has recently been proposed as a guide to assist with endoscopic release of the flexor retinaculum. 26,27 Postoperative complications, such as incomplete sectioning of the retinaculum or scarfing involving the nerve, might further be identified with US in patients with unrelieved or recurrent symptoms (Fig 3). 12 There are few studies in which US and MR results are compared. From these, it emerges that US is capable of producing results at least equal in value to MRI in the diagnosis of carpal tunnel syndrome. 16MRI seems superior to US in identifying subtle abnormalities, because it has the additional diagnostic feature of showing signal changes caused by nerve edema and blood perfusion abnormalities. 16,28 However, recently developed, sensitive color and power Doppler technology made it possible to image hyperemic changes with US through the depiction of increased flow signals within and around peripheral nerves. 7 Among other possible sites of nerve compression, US has the ability to detect the entrapment of the sciatic nerve at the posterior thigh by a variety of soft-tissue masses, 29 and to show entrapment of the radial nerve in the arm after fracture of the humeral shaft. 3° In the case of entrapment of the suprascapular nerve at the spinoglenoid notch by ganglion cysts, US can guide the aspiration of the cyst for decompression purposes. 31,32This application illustrates the therapeutic potential of US in cases of extrinsic compression elsewhere in the body caused by fluid-filled, space-occupying lesions. Cases in which US was used to diagnose nerve compression have been reported only occasionally at sites other than the ones described above. Nevertheless, we believe current US equipment might be equally effective in the depiction of many of the possible extrinsic causes involving other, even smaller, peripheral nerves. When the
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Fig 3. Postoperative findings. Transverse 10 to 13 MHz US images obtained at the proximal and distal tunnel in a patient with unrelieved symptoms after carpal tunnel release. (A) At the proximal end of the tunnel, the flexor retinaculum (arrowheads) is open and the MN is normal in shape. (B) At the distal end of the tunnel, the retinaculum is closed (arrowheads) and the nerve (arrow) remains compressed. Note the change in the cross-sectional area of MN between the proximal and distal level of the tunnel.
nerves are too small to be detected sonographically, indirect signs of nerve damage can be obtained by the evaluation of the appropriate group of muscles innervated by the involved nerve. With US, the affected muscles might show decreased bulk and increased reflectivity (caused by fatty replacement) when compared with their counterparts on the contralateral side (Fig 4). Furthermore, the ease of obtaining real-time information with US can rapidly verify muscle paralysis and can exclude tendon rupture through active and passive movement of the affected extremity. The failure to observe a normal increase in muscle vascularity with color Doppler US after exercise is consistent with paralysis. These signs of muscle paralysis have proven useful in the evaluation of patients with the anterior interosseous nerve syndrome. 33
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Fig 4. Neurogenic atrophy of muscles in a patient with longstanding cubitsl tunnel syndrome and functional deficit in the ulnar nerve. (A} Transverse 12 to 5 MHz US image at the dorsal aspect of the hand, showing the interosseous muscles (asterisks) among the metacarpals (M). The muscles are reduced in bulk and appear hyperechogenic. (B) Transverse US scan showing the normal contralateral muscles for comparison.
NERVE TUMORS
The US appearance of nerve tumors has been
extensively reported. 14,34-37Most reports deal with tumors located in a superficial position, suitable for US examination. In patients with nerve tumors, US should theoretically address 4 main issues: (1) US
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should establish whether the mass originates from a nerve or compresses it extrinsically, (2) US should indicate histopathologic characteristics of the mass, (3) US should detect signs of malignancy, and (4) US should guide the biopsy of the mass. Nerve tumors have a nonspecific appearance on US because they usually are fusiform hypoechoic masses with well-defined margins. 34A presumptive diagnosis of neurogenic tumor can reliably be made with US only if a soft tissue mass is found to be connected to a nerve bundle at its proximal and distal poles (Fig 5). 34 This determination requires careful scanning technique because, in some cases, the nerve ends might be extrinsic to the tumor and distorted and stretched over the tumor capsule, whereas in other instances, the tumor might originate from small nerve branches that are difficult to visualize. The latter problem particularly can occur with superficially located tumors. Outside the tumor, the entering and exiting nerve might be thickened and present loss of fascicular structure. Thickening of the nerve causes tapering of the mass at the nerve attachment, giving it an ovoid shape .8 Classically, nerve tumors include 2 major benign histotypes, schwannoma (also referred to as neurilemoma or neurinoma) and neurofibroma. Malignant peripheral nerve sheath tumor originates most often from the sarcomatous transformation of a neurofibroma. Von Recklinghausen neurofibromatosis is a genetically-transmitted disorder in which numerous, widely dispersed neurofibromas can be encountered as skin nodules. These tumors typically arise from superficial cutaneous nerves, but neurofibromas can also arise from deep and large nerves in this condition 14 (Fig 6).
Fig 5. Schwannoma of the ulnar nerve at the bicipital sulcus. Longitudinal 12 to 5 MHz US scan depicts the tumor (T) as an oval homogeneous hypoechoic mass in continuity with the ulnar nerve (arrowheads). Note the flared shape of the tumor at its attachment to the nerve.
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Similarly, confident differentiation between benign and malignant neurogenic masses is impossible with US. The only findings that might make the examiner suspect that the lesion is malignant are a sudden increase in size of a previously stable mass, the presence of indistinct tumor margins, and adhesions between the mass and surrounding tissues. 3'14 Despite these limitations, US can contribute in the preoperative assessment of the extent of disease by defining the relationship of the tumor to adjacent neurovascular structures and surrounding muscles and in assisting surgical planning. After imaging assessment, a fine needle aspiration biopsy of the mass can be confidently performed under US guidance. It should be noted that during biopsy, an excruciating pain is frequently triggered by the needle insertion. NONNEOPLASTIC INTRINSIC LESIONS
Fig 6. Neurofibromas of the ulnar nerve in a patient with von Recklinghausen neurofibromatosis. (A) Longitudinal 10 to 13 MHz US image at the elbow depicts 2 neuroflbromas (T) shown as small hypoechoic foci located in series along the ulnar nerve (arrowheads). ME, medial epicondyle of the humerus. (B,C) On the correlative transverse T2-weighted (2,000/ 86) MR images (B, caudal; C, cranial), both tumors (curved arrows) show high signal intensity.
US (and also CT and MRI) has many shortcomings in regard to determining the histopathologic characteristics of nerve tumors, as well as identifying signs of malignancy. Most schwannomas appear as eccentric masses with homogeneous texture, posterior acoustic enhancement, intratumor cystic changes, and hypervascularity on color Doppler imaging. Neurofibromas, on the other hand, commonly have a coarse, echogenic, and hypovascular pattern. 38-41 However, these differences are not reliable for histopathologic differentiation based on US findings. 27 In addition, it must be remembered that, although rare, nerve sheath ganglions (ie, intraneural ganglions) might mimic nerve tumors, based on a hypoechoic appearance, and (in some cases) the presence of septations. 3
A wide spectrum of nerve abnormalities can be seen with US in patients with leprosy, caused by inflammatory and degenerative changes, acute reactional states, and entrapment syndromes.42 In this condition, nerve hypertrophy is considered a main feature. By measuring the cross-sectional area of the involved nerves with US, it was noted that nerve size was larger in lepromatous patients during acute reactional states. 42 During these reactions, endoneural color flow signals were increased as well as T2-signal and gadolinium-enhancement. These findings indicated rapid progression of nerve damage and a poor prognosis unless antireaction treatment was started. 42 In tuberculoid leprosy, a caseous pouch surrounding a thickened external popliteal nerve also has been described with US. 43 Subtle abnormalities, including focal loss of fascicular pattern and intranervous hypervascularity, can be recognized in minor traumas, such as the inadvertent punture of a nerve with a needle (Fig 7). However, we believe US can provide an important contribution in the treatment of patients with major trauma with partial or complete interruption of nerve continuity. In these cases, US is able to assess the integrity of a peripheral nerve, image the defect in the nerve, and predict the level of nerve section preoperatively. After surgery, US can identify early complications. 29,44Diagnostic difficulties might arise in the acute phases of trauma, in which open wounds, fluid, and hematomas can obscure findings and interfere with the interpretation of US images.
ULTRASONOGRAPHY OF PERIPHERAL NERVES
When the nerve is transected and nerve continuity cannot be reestablished because of too wide a gap between the separated ends or interposed fibrosis, a bulbous neuroma usually develops at the nerve end. The neuroma can be appreciated as an elongated, hypoechoic mass connected to the proximal end of the severed nerve. These masses grow rapidly at the site of injury. In nerve reconstructive surgery, US allows for reliable postoperative evaluation of the continuity of a nerve anastomosis and can detect perineural fluid collection or nerve healing problems. Irregular bulging of hypoechoic fibrous tissue at the anastomosis suggests inadequate fusion of the nerve edges caused by excessive tension or infection. 29 Although not a true neuroma, the term "Morton neuroma" is used widely to define a benign mass of perineural fibrosis affecting the plantar interdigital nerve. Possible causes include local entrapment below the distal edge of the intermetatarsal ligament, ischemia, and compression of the nerve by an inflamed intermetatarsal bursa. Morton neuromas occur most commonly at the III-IV intermetatarsal spaces and also at the II-III intermetatarsal spaces. Sonographically, they appear as well-defined, ovoid, hypoechoic masses that are elongated along the major axis of metatarsals 46-48 (Fig 8). Longitudinal US scans may show continuity of the mass with the interdigital nerve. Power Doppler US may help to identify these lesions based on increased vascularity. 14 In the appropriate clinical setting, US has a reported sensitivity of 95% to 1 0 0 % 46,49,50 for the detection of Morton neuromas, with aspecificity of
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Fig 8. Morton's neuroma. (A) Transverse 10 to 13 MHz US scans with the transducer over the plantar aspect of the metatarsals (M). A small hypoechoic neuroma (arrow) is detected in the third intermetatarsal space. (B) A longitudinal scan obtained in the intermetatarsal space better shows the fusiform and irregular shape of the lesion (arrow). The small interdigital nerve (arrowheads) can be seen proximal to the mass.
83% and an accuracy of 95%. 49 Similar results have been reported with MRI, which has shown a sensitivity of 87%, a specificity of 100%, and an accuracy of 89%. 51,52 It must be noted that small lesions (less than 5 mm in size) can be difficult to identify with US; this can explain the higher sensitivity of MR reported in some series. 46 US can help show the exact location of the neuroma; thus, it can guide surgery to the appropriate intermetatarsal space. 51 In a postoperative setting, US is able to detect recurrences. 53 CONCLUSION
Fig 7. Nerve trauma. A longitudinal 10 to 13 MHz US image shows a traumatic neuroma (open arrow) within the substance of the ulnar nerve (arrowheads) in the forearm of a patient with partial transection of the nerve by a penetrating wound. The neuroma develops from the resected fascicles as a hypoechoic irregular mass contained within the nerve sheath.
Although the application of US is limited by its inherent operator dependence and a relatively long skill-development learning curve, clinical studies are showing that US is accurate and cost-effective for diagnosing a large spectrum of nerve abnormalities. In our opinion, US can be the first-line approach to patients with suspected lesions of the peripheral nervous system, and can avoid the use of
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MRI in many cases. A careful US approach with accurate, meticulous scanning technique and good knowledge of the course and anatomic relationships of nerves can provide the clinician with precise information regarding the involved nerve and the site and nature of a disease process. This
information facilitates the choice of appropriate treatment. With continued experience and research, newer applications for nerve US will likely become established, further advancing the role of this technique in the evaluation of the peripheral nervous system.
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19. Duncan I, Sullivan P, Lomas F: Sonography in the diagnosis of carpal tunnel syndrome. Am J Roentgenol 173:681683, 1999 20. Lee D, van Holsbeeck MT, Janevski PK, et al: Diagnosis of carpal tunnel syndrome. Ultrasound versus electromyography. Radiol Clin North Am. 37:859-872, 1999 21. Chiou HJ, Chou YH, Cheng SP, et al: Cubital tunnel syndrome: Diagnosis by high-resolution ultrasonography. J Ultrasound Med 17:643-648, 1998 22. Bertolotto M, Rosenberg I, Parodi RC, et al: Case report: Fibroma of tendon sheath in the distal forearm with associated median nerve neuropathy: US, CT and MR appearance. Clin Radio151:370-372, 1996 23. Van Vugt RM, van Dalen A, Bijlsma JW: The current role of high-resolution ultrasonography of the hand and wrist in rheumatic diseases. Clin Exp Rheumatol 16:454-458, 1998 24. Kato H, Ogino T, Nanbu T et al: Compression neuropathy of the motor branch of the median nerve caused by palmar ganglion. J Hand Surg [Am] 16:751-752, 1991 25. Puig S, Turkof E, Sedivy R, et al: Sonographic diagnosis of recurrent ulnar nerve compression by ganglion cysts. J Ultrasound Med 18:433-436, 1999 26. Nakamichi K, Tachibana S: Distance between the median nerve and ulnar neurovascular bundle: Clinical significance with ultrasonographically assisted carpal tunnel release. J Hand Surg [Am] 23:870-874, 1998 27. Nakamichi K, Tachibana S: Ultrasonographically assisted carpal tunnel release. J Hand Surg [Am] 22:853-862, 1997 28. Sugimoto H, Miyaji N, Ohsawa T: Carpal tunnel syndrome: Evaluation of median nerve circulation with dynamic contrast-enhanced MR imaging. Radiology 190:459-466, 1994 29. Graif M, Seton A, Nerubali J, et al: Sciatic nerve: Sonographic evaluation and anatomic-pathologic considerations. Radiology 181:405-408, 1991 30. Bodner G, Huber B, Schwabegger A, et al: Sonographic detection of radial nerve entrapment within a humerus fracture. J Ultrasound Med 18:703-706, 1999 31. HashimotoBE, HayesAS, Ager JD: Sonographic diagnosis and treatment of ganglion cysts causing suprascapular nerve entrapment. J Ultrasound Med 13:671-674, 1994 32. Chiou ILl, Chou YH, Wn JJ, et al: Alternative and effective treatment of shoulder ganglion cyst: ultrasonographically guided aspiration. J Ultrasound Med 1999; 18:531-535 33. Hide IG, Grainger AJ, Naisby GP: Sonographic findings in the anterior interosseous nerve syndrome. J Clin Ultrasound 27:459-464, 1999 34. Fornage BD: Peripheral nerves of the extremities: Imaging with US. Radiology 167:179-182, 1988 35. Beggs I: Sonographic appearances of nerve tumors. J Clin Ultrasound 27:363-368, 1999 36. Kuo CH, Changchien CS: Sonographic features of retroperitoneal neurilemmoma, J Clin Ultrasound 21:309-311, 1993
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37. Reuter KL, Raptopoulos V, De Girolami U: Ultrasonography of a plexiform neurofibroma of the popliteal fossa. J Ultrasound Med 1:209-211, 1982 38. King AD, Ahuja AT, King W, et al: Sonography of peripheral nerve tumors of the neck. Am J Roentgeno1169:16951698, 1997 39. Chinn DH, Filly RA, Callen PW: Unusual ultrasonographic appearance of a solid schwannoma. J Clin Ultrasound 10:243-245, 1982 40. Hoddick WK, Callen PW, Filly RA, et al: Ultrasound evaluation of benign sciatic nerve sheath tumors. J Ultrasound Med 3:505-507, 1984 41. Hughes DG, Wilson DJ: Ultrasound appearances of peripheral nerve tumors. Br J Radio159:1 04 1-1 043, 1986 42. Martinoli C, Derchi LE, Bertolotto M, et al: US and MR imaging of peripheral nerves in leprosy. Skeletal Radiol 29:142150, 2000 43. Fornage BD, Nerot C. Sonographic diagnosis of tuberculoid leprosy. J Ultrasound Med 6:105-107, 1987 44. Graif M. Peripheral nerves, in Fornage B (ed): Musculoskeletal Ultrasound. New York, NY, Churchill Livingstone, 1995, pp 73-83 45. Simonetti S, Bianchi S, Martinoli C: Neurophysiological and ultrasound findings in sural nerve lesions following strip-
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ping of the small saphenous vein. Muscle Nerve 22:1724-1726, 1999 46. Redd RA, Peters VJ, Emery SF, et al: Morton neuroma: Sonographic evaluation. Radiology 171:415-417, 1989 47. Shapiro PP, Shapiro SL: Sonographic evaluation of interdigital neuromas. Foot Ankle Int 16:604-606, 1995 48. Oliver TB, Beggs I: Ultrasound in the assessment of metatarsalgia: A surgical and histologic correlation. Clin Radiol 53:287-289, 1998 49. Sobiesk GA, Wertheimer SJ, Schulz R, et al: Sonographic evaluation of interdigital neuromas. J Foot Ankle Surg 36:364366, 1997 50. Read JW, Noakes JB, Kerr D, et al: Morton's metatarsalgia: Sonographic findings and correlated histopathology. Foot Ankle Int 20:153-161, 1999 51. Kaminski S, Griffin L, Milsap J: Is ultrasonography a reliable way to confirm the diagnosis of Morton's neuroma? Orthopedics 20:37-39, 1997 52. Zanetti M, Ledermann T, Zollinger H et al: Efficacy of MR imaging in patients suspected of having Morton's neuroma. Am J Roentgenol 168:529-532, 1997 53. Levine SE, Myerson MS, Shapiro PP, et al: Ultrasonographic diagnosis of recurrence after excision of an interdigital neuroma. Foot Ankle Int 19:79-84, 1998
HE DIAGNOSIS of peripheral neuropathies has traditionally relied upon information obtained from the clinical history, physical examination, and electrodiagnostic studies. In the past, these clinical methods were the only tests available. In fact, before the 1970s, radiographic studies of peripheral nerve lesions were limited to conventional plain-film radiography to evaluate for secondary skeletal changes. Direct imaging of peripheral nerves only became possible with the development of cross-sectional imaging techniques, such as ultrasound (US), CT, and MRI. In the1990s, the development and continuing improvement of US technology provided the means for precise, noninvasive diagnosis of musculoskeletal abnormalities in a variety of clinical settings.l.2 The applications of US in the musculoskeletal system have increased rapidly, and the use of US in routine clinical practice has become commonplace, influencing the diagnosis and the clinical management in the symptomatic patient. Current high-end US systems equipped with modern linear array transducers in the 5 to 15 MHz range have given radiologists the opportunity to generate highconspicuity images of most nerves in the body. These instruments permit the delineation of the normal fascicular structure of peripheral nerves, the recognition of specific and sometimes treatable abnormalities, the differentiation of endoneural and extraneural tumors, the evaluation of the extent of lesions, and the assessment of involved nerves at follow-up examination. 3 Other appropriate methods for noninvasive diagnosis of nerve disorders are currently available, particularly MRI and MR neurography, which combines fat and flow suppression with T2weighting and 3D reconstruction.4,5 Although sophisticated advances in MRI have recently enhanced both resolution and conspicuity of nerve structures, MRI is expensive, time-consuming and not readily available for routine clinical use. Con-
T
versely, high-resolution US, in experienced hands, provides economic and noninvasive imaging, is quick to perform, and provides specific advantages over MRI, including the ability to explore long segments of nerve trunks in a single study, and the ability to examine tissues in both static and dynamic states. This article discusses the diagnostic capabilities and limitations of US in the study of peripheral nerves. It reviews and illustrates the current role of peripheral nerve sonography, and compares US with other diagnostic methods. ANATOMIC CONSIDERATIONS
High-frequency linear array transducers are needed to scan peripheral nerves. The central frequency varies from 7.5 to 15 MHz, depending on the patient's body habitus and the equipment used. When examined with these transducers, peripheral nerves show a peculiar arrangement of their internal structure, made of multiple hypoechoic parallel linear areas separated by hyperechoic bands (Fig 1A). 6 On transverse scans, nerves have a honeycomb-like appearance, with hypoechoic, rounded areas embedded in a hyperechoic background (Fig 1B). 6 Histologic correlation has shown that the hypoechoic structures correspond to the neuronal fascicles that run longitudinally within the nerve, and the hyperechoic background relates to the interfascicular epineurium (Fig IC). 6 The outer boundaries of nerves are usually undefined, because of a similar hyperechoic
From Cattedra "R" di Radiologia--Universitgt di Genova, Genova, Italy and the Division de Radiodiagnostic--HOpital Cantonal Universitaire, Geneve, Switzerland. Address reprint requests to Carlo Martinoli, MD, Cattedra "R" di Radiologia--Universith di Genova, Largo Rosanna BenzL 8. 1-16132, Genova, Italy. Copyright © 2000 by W.B. Saunders Company 0887-2171/00/2103-0004510.00/0 doi: 10.1053/suit.2000. 8562
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Fig 1. US appearance of normal nerves (12 to 5 MHz US image of MN at the middle third of forearm). (A) In a long axis view, the nerve (arrows) is composed of parallel linear hypoechoic areas separated by hyperechoic bands. (B) in a transverse (short axis) view, the nerve (arrows) is characterized by rounded hypoechoic areas (asterisk) in a hyperechoic background. (C) A transverse histologic cross-section of a bovine sciatic nerve shows the nerve fascicles (asterisk) that correlate well with the hypoechoic rounded areas seen in image B.
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appearance of both the superficial epineurium and the surrounding fat. A careful scanning technique based on precise knowledge of nerve position and analysis of the anatomic relations of the nerve with surrounding structures is essential for the identification of peripheral nerves with US. Systematic scanning in transverse planes is preferred, to follow the nerves along their course throughout the limbs. Longitudinal scans are less useful for following peripheral nerves, because the nerve fascicles might easily be confused with echoes from muscles and tendons coursing along the same plane. Color Doppler can aid in differentiating between the hypoechoic nerve fascicles and adjacent small vessels. The visualization of nerves with US primarily depends on their size and course. Current US equipment is able to confidently identify almost all the main nerve trunks running in the limbs and extremities, including the median, ulnar, and radial nerves in the upper limbs, and the sciatic, common peroneal, and posterior tibial nerves in the lower limbs. 6,7 Evaluation of the brachial plexus is also feasible, although US is not able to depict its roots and cords as completely and reliably as MRI. 8,9 Because of problems of access, US cannot visualize the epidural space, the C8 and T1 roots, and variable portions of the brachial plexus trunks behind the clavicle and in the infraclavicular region. With the exception of the vagus, recurrent laryngeal nerves in the neck, 1° and the femoral nerve in the retroperitoneum, 11 the cranial nerves, the nerve roots exiting the dorsal, lumbar and sacral spine, the sympathetic chains, and the splancnic nerves in abdomen cannot be examined with US,
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either because they are positioned too deeply or because of interposed bony structures. Given the characteristic US appearance of normal nerves, some anatomic variants such as anomalous branching and congenital anomalies can be recognized with US. Among these are the fusiform enlargement of the median nerve (MN) at the distal forearm and through the palm caused by fibrofatty tissue in patients with macrodactyly (fibrolipomatous hamartoma). 12-14 Also visible is the striking hypertrophy of peripheral nerves that occurs in the Charcot-Marie-Tooth syndrome (hereditary motor and sensory neuropathy type I and II).15 ENTRAPMENT NEUROPATHIES Damage to a peripheral nerve by pressure results in a compression neuropathy. This might occur at several points along the course of a nerve, although the involvement by extrinsic causes is more common at narrow anatomic passageways such as osteofibrous canals, abnormal bands of muscle, and connective tissue or bony ridges that tether the nerve. Although the diagnostic evaluation of nerve compressive syndromes basically relies on clinical features and electrophysiological testing, these studies only indicate the level of the lesion. They do not provide spatial information about the nerve or its surroundings that could help in determining the etiology of neuropathy. Direct visualization of nerve abnormalities with imaging modalities might enhance the diagnosis and the surgical result by providing exact information on the nature of constricting findings, especially in cases with confusing clinical pictures or equivocal or contradictory functional studies. Although MRI has been established as a useful imaging technique in this field, high-resolution US is now increasingly proposed as an efficient and low-cost alternative. Until now, most of the experience with US has been focused on carpal tunnel syndrome. ~2,16,17US criteria for MN compression at the carpal tunnel include a classic triad of findings: (1) flattening or deformity of the nerve at the hamate level (distal tunnel), (2) swelling of the nerve at the pisiform level (proximal tunnel) or at the distal radius, and (3) palmar bowing of the flexor retinaculum 12A6,17 (Fig 2). Reduced transverse sliding movement of the nerve beneath the retinaculum during flexion and extension of the index finger also might be observed. 12,18 Because the nerve shape is variable through the tunnel, measurement indices have been
® Fig 2. Carpal tunnel syndrome. (A) Longitudinal 8 to 15 MHz US scan shows extensive flattening (straight arrows) of the MN in the carpal tunnel and swelling of the nerve proximal to the compression point (curved arrow). FT, flexor tendons. (B) Transverse US image at the distal radius. The MN is markedly enlarged. (C) Transverse US image at the distal tunnel. The MN (open arrow) is reduced in size, and the shape of the overlying flexor retinaculum (arrowheads) is convex.
introduced to better assess nerve swelling. Among these, a nerve cross-sectional area greater than 0.09 cm 2 at the level of pisiform is currently reported as the best criterion for MN swelling. 19 Interestingly, it has been shown that the area of the MN measured by US correlates well with the severity of electromyographic findings. 2° Similarly, a larger crosssectional area of the ulnar nerve at the medial
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epicondyle occurs in patients with the cubital tunnel syndrome. 21This finding suggests that quantitative analysis with US might be applied equally well in the diagnosis of nerve compressive syndromes at sites other than the carpal tunnel. Extrinsic causes for nerve entrapment, such as tenosynovitis, ganglia, and soft-tissue masses, might be identified with US. 12,22-25If the patient's symptoms are not typical, US can be an effective means for exploring the entire course of the MN to rule out other more proximal sites of compression. Furthermore, in the carpal tunnel syndrome, US has recently been proposed as a guide to assist with endoscopic release of the flexor retinaculum. 26,27 Postoperative complications, such as incomplete sectioning of the retinaculum or scarfing involving the nerve, might further be identified with US in patients with unrelieved or recurrent symptoms (Fig 3). 12 There are few studies in which US and MR results are compared. From these, it emerges that US is capable of producing results at least equal in value to MRI in the diagnosis of carpal tunnel syndrome. 16MRI seems superior to US in identifying subtle abnormalities, because it has the additional diagnostic feature of showing signal changes caused by nerve edema and blood perfusion abnormalities. 16,28 However, recently developed, sensitive color and power Doppler technology made it possible to image hyperemic changes with US through the depiction of increased flow signals within and around peripheral nerves. 7 Among other possible sites of nerve compression, US has the ability to detect the entrapment of the sciatic nerve at the posterior thigh by a variety of soft-tissue masses, 29 and to show entrapment of the radial nerve in the arm after fracture of the humeral shaft. 3° In the case of entrapment of the suprascapular nerve at the spinoglenoid notch by ganglion cysts, US can guide the aspiration of the cyst for decompression purposes. 31,32This application illustrates the therapeutic potential of US in cases of extrinsic compression elsewhere in the body caused by fluid-filled, space-occupying lesions. Cases in which US was used to diagnose nerve compression have been reported only occasionally at sites other than the ones described above. Nevertheless, we believe current US equipment might be equally effective in the depiction of many of the possible extrinsic causes involving other, even smaller, peripheral nerves. When the
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Fig 3. Postoperative findings. Transverse 10 to 13 MHz US images obtained at the proximal and distal tunnel in a patient with unrelieved symptoms after carpal tunnel release. (A) At the proximal end of the tunnel, the flexor retinaculum (arrowheads) is open and the MN is normal in shape. (B) At the distal end of the tunnel, the retinaculum is closed (arrowheads) and the nerve (arrow) remains compressed. Note the change in the cross-sectional area of MN between the proximal and distal level of the tunnel.
nerves are too small to be detected sonographically, indirect signs of nerve damage can be obtained by the evaluation of the appropriate group of muscles innervated by the involved nerve. With US, the affected muscles might show decreased bulk and increased reflectivity (caused by fatty replacement) when compared with their counterparts on the contralateral side (Fig 4). Furthermore, the ease of obtaining real-time information with US can rapidly verify muscle paralysis and can exclude tendon rupture through active and passive movement of the affected extremity. The failure to observe a normal increase in muscle vascularity with color Doppler US after exercise is consistent with paralysis. These signs of muscle paralysis have proven useful in the evaluation of patients with the anterior interosseous nerve syndrome. 33
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Fig 4. Neurogenic atrophy of muscles in a patient with longstanding cubitsl tunnel syndrome and functional deficit in the ulnar nerve. (A} Transverse 12 to 5 MHz US image at the dorsal aspect of the hand, showing the interosseous muscles (asterisks) among the metacarpals (M). The muscles are reduced in bulk and appear hyperechogenic. (B) Transverse US scan showing the normal contralateral muscles for comparison.
NERVE TUMORS
The US appearance of nerve tumors has been
extensively reported. 14,34-37Most reports deal with tumors located in a superficial position, suitable for US examination. In patients with nerve tumors, US should theoretically address 4 main issues: (1) US
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should establish whether the mass originates from a nerve or compresses it extrinsically, (2) US should indicate histopathologic characteristics of the mass, (3) US should detect signs of malignancy, and (4) US should guide the biopsy of the mass. Nerve tumors have a nonspecific appearance on US because they usually are fusiform hypoechoic masses with well-defined margins. 34A presumptive diagnosis of neurogenic tumor can reliably be made with US only if a soft tissue mass is found to be connected to a nerve bundle at its proximal and distal poles (Fig 5). 34 This determination requires careful scanning technique because, in some cases, the nerve ends might be extrinsic to the tumor and distorted and stretched over the tumor capsule, whereas in other instances, the tumor might originate from small nerve branches that are difficult to visualize. The latter problem particularly can occur with superficially located tumors. Outside the tumor, the entering and exiting nerve might be thickened and present loss of fascicular structure. Thickening of the nerve causes tapering of the mass at the nerve attachment, giving it an ovoid shape .8 Classically, nerve tumors include 2 major benign histotypes, schwannoma (also referred to as neurilemoma or neurinoma) and neurofibroma. Malignant peripheral nerve sheath tumor originates most often from the sarcomatous transformation of a neurofibroma. Von Recklinghausen neurofibromatosis is a genetically-transmitted disorder in which numerous, widely dispersed neurofibromas can be encountered as skin nodules. These tumors typically arise from superficial cutaneous nerves, but neurofibromas can also arise from deep and large nerves in this condition 14 (Fig 6).
Fig 5. Schwannoma of the ulnar nerve at the bicipital sulcus. Longitudinal 12 to 5 MHz US scan depicts the tumor (T) as an oval homogeneous hypoechoic mass in continuity with the ulnar nerve (arrowheads). Note the flared shape of the tumor at its attachment to the nerve.
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Similarly, confident differentiation between benign and malignant neurogenic masses is impossible with US. The only findings that might make the examiner suspect that the lesion is malignant are a sudden increase in size of a previously stable mass, the presence of indistinct tumor margins, and adhesions between the mass and surrounding tissues. 3'14 Despite these limitations, US can contribute in the preoperative assessment of the extent of disease by defining the relationship of the tumor to adjacent neurovascular structures and surrounding muscles and in assisting surgical planning. After imaging assessment, a fine needle aspiration biopsy of the mass can be confidently performed under US guidance. It should be noted that during biopsy, an excruciating pain is frequently triggered by the needle insertion. NONNEOPLASTIC INTRINSIC LESIONS
Fig 6. Neurofibromas of the ulnar nerve in a patient with von Recklinghausen neurofibromatosis. (A) Longitudinal 10 to 13 MHz US image at the elbow depicts 2 neuroflbromas (T) shown as small hypoechoic foci located in series along the ulnar nerve (arrowheads). ME, medial epicondyle of the humerus. (B,C) On the correlative transverse T2-weighted (2,000/ 86) MR images (B, caudal; C, cranial), both tumors (curved arrows) show high signal intensity.
US (and also CT and MRI) has many shortcomings in regard to determining the histopathologic characteristics of nerve tumors, as well as identifying signs of malignancy. Most schwannomas appear as eccentric masses with homogeneous texture, posterior acoustic enhancement, intratumor cystic changes, and hypervascularity on color Doppler imaging. Neurofibromas, on the other hand, commonly have a coarse, echogenic, and hypovascular pattern. 38-41 However, these differences are not reliable for histopathologic differentiation based on US findings. 27 In addition, it must be remembered that, although rare, nerve sheath ganglions (ie, intraneural ganglions) might mimic nerve tumors, based on a hypoechoic appearance, and (in some cases) the presence of septations. 3
A wide spectrum of nerve abnormalities can be seen with US in patients with leprosy, caused by inflammatory and degenerative changes, acute reactional states, and entrapment syndromes.42 In this condition, nerve hypertrophy is considered a main feature. By measuring the cross-sectional area of the involved nerves with US, it was noted that nerve size was larger in lepromatous patients during acute reactional states. 42 During these reactions, endoneural color flow signals were increased as well as T2-signal and gadolinium-enhancement. These findings indicated rapid progression of nerve damage and a poor prognosis unless antireaction treatment was started. 42 In tuberculoid leprosy, a caseous pouch surrounding a thickened external popliteal nerve also has been described with US. 43 Subtle abnormalities, including focal loss of fascicular pattern and intranervous hypervascularity, can be recognized in minor traumas, such as the inadvertent punture of a nerve with a needle (Fig 7). However, we believe US can provide an important contribution in the treatment of patients with major trauma with partial or complete interruption of nerve continuity. In these cases, US is able to assess the integrity of a peripheral nerve, image the defect in the nerve, and predict the level of nerve section preoperatively. After surgery, US can identify early complications. 29,44Diagnostic difficulties might arise in the acute phases of trauma, in which open wounds, fluid, and hematomas can obscure findings and interfere with the interpretation of US images.
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When the nerve is transected and nerve continuity cannot be reestablished because of too wide a gap between the separated ends or interposed fibrosis, a bulbous neuroma usually develops at the nerve end. The neuroma can be appreciated as an elongated, hypoechoic mass connected to the proximal end of the severed nerve. These masses grow rapidly at the site of injury. In nerve reconstructive surgery, US allows for reliable postoperative evaluation of the continuity of a nerve anastomosis and can detect perineural fluid collection or nerve healing problems. Irregular bulging of hypoechoic fibrous tissue at the anastomosis suggests inadequate fusion of the nerve edges caused by excessive tension or infection. 29 Although not a true neuroma, the term "Morton neuroma" is used widely to define a benign mass of perineural fibrosis affecting the plantar interdigital nerve. Possible causes include local entrapment below the distal edge of the intermetatarsal ligament, ischemia, and compression of the nerve by an inflamed intermetatarsal bursa. Morton neuromas occur most commonly at the III-IV intermetatarsal spaces and also at the II-III intermetatarsal spaces. Sonographically, they appear as well-defined, ovoid, hypoechoic masses that are elongated along the major axis of metatarsals 46-48 (Fig 8). Longitudinal US scans may show continuity of the mass with the interdigital nerve. Power Doppler US may help to identify these lesions based on increased vascularity. 14 In the appropriate clinical setting, US has a reported sensitivity of 95% to 1 0 0 % 46,49,50 for the detection of Morton neuromas, with aspecificity of
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Fig 8. Morton's neuroma. (A) Transverse 10 to 13 MHz US scans with the transducer over the plantar aspect of the metatarsals (M). A small hypoechoic neuroma (arrow) is detected in the third intermetatarsal space. (B) A longitudinal scan obtained in the intermetatarsal space better shows the fusiform and irregular shape of the lesion (arrow). The small interdigital nerve (arrowheads) can be seen proximal to the mass.
83% and an accuracy of 95%. 49 Similar results have been reported with MRI, which has shown a sensitivity of 87%, a specificity of 100%, and an accuracy of 89%. 51,52 It must be noted that small lesions (less than 5 mm in size) can be difficult to identify with US; this can explain the higher sensitivity of MR reported in some series. 46 US can help show the exact location of the neuroma; thus, it can guide surgery to the appropriate intermetatarsal space. 51 In a postoperative setting, US is able to detect recurrences. 53 CONCLUSION
Fig 7. Nerve trauma. A longitudinal 10 to 13 MHz US image shows a traumatic neuroma (open arrow) within the substance of the ulnar nerve (arrowheads) in the forearm of a patient with partial transection of the nerve by a penetrating wound. The neuroma develops from the resected fascicles as a hypoechoic irregular mass contained within the nerve sheath.
Although the application of US is limited by its inherent operator dependence and a relatively long skill-development learning curve, clinical studies are showing that US is accurate and cost-effective for diagnosing a large spectrum of nerve abnormalities. In our opinion, US can be the first-line approach to patients with suspected lesions of the peripheral nervous system, and can avoid the use of
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MRI in many cases. A careful US approach with accurate, meticulous scanning technique and good knowledge of the course and anatomic relationships of nerves can provide the clinician with precise information regarding the involved nerve and the site and nature of a disease process. This
information facilitates the choice of appropriate treatment. With continued experience and research, newer applications for nerve US will likely become established, further advancing the role of this technique in the evaluation of the peripheral nervous system.
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ping of the small saphenous vein. Muscle Nerve 22:1724-1726, 1999 46. Redd RA, Peters VJ, Emery SF, et al: Morton neuroma: Sonographic evaluation. Radiology 171:415-417, 1989 47. Shapiro PP, Shapiro SL: Sonographic evaluation of interdigital neuromas. Foot Ankle Int 16:604-606, 1995 48. Oliver TB, Beggs I: Ultrasound in the assessment of metatarsalgia: A surgical and histologic correlation. Clin Radiol 53:287-289, 1998 49. Sobiesk GA, Wertheimer SJ, Schulz R, et al: Sonographic evaluation of interdigital neuromas. J Foot Ankle Surg 36:364366, 1997 50. Read JW, Noakes JB, Kerr D, et al: Morton's metatarsalgia: Sonographic findings and correlated histopathology. Foot Ankle Int 20:153-161, 1999 51. Kaminski S, Griffin L, Milsap J: Is ultrasonography a reliable way to confirm the diagnosis of Morton's neuroma? Orthopedics 20:37-39, 1997 52. Zanetti M, Ledermann T, Zollinger H et al: Efficacy of MR imaging in patients suspected of having Morton's neuroma. Am J Roentgenol 168:529-532, 1997 53. Levine SE, Myerson MS, Shapiro PP, et al: Ultrasonographic diagnosis of recurrence after excision of an interdigital neuroma. Foot Ankle Int 19:79-84, 1998