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An Illustrated Tutorial of Musculoskeletal Sonography

Part 2, Upper Extremity

¹ All authors: Department of Radiology, The University of Michigan Medical Center, 1500 E. Medical Center Dr., TC 2910, Ann Arbor, MI 48109-0326.

Received December 8, 1999; accepted after revision February 10, 2000.

 
Address correspondence to J. Lin.

Introduction

Top Introduction Shoulder Elbow Hand and Wrist References

 
Sonography is a useful technique for the assessment of many conditions that can affect the upper extremity because of the superficial nature of most structures in this anatomic region. As technical advances continue to improve image quality, the role for, sonography in the diagnosis of musculoskeletal disorders will grow. Examination of the rotator cuff tendons and evaluation for ganglion cysts of the hand and wrist are common indications for sonography; other applications also continue to gain popularity.

Shoulder

Top Introduction Shoulder Elbow Hand and Wrist References

 
Assessment of the integrity of the rotator cuff tendons is the primary indication for shoulder sonography. Most commonly, the supraspinatus tendon is affected, in isolation or in combination with other tendons. A disruption of the normal fibrillar pattern results in a focal hypoechoic or anechoic defect [1].

A full-thickness tear is diagnosed when the disruption extends from the articular to the bursal surface of the tendon (Fig. 1A,1B,1C). Secondary signs of a full-thickness tear include volume loss with associated flattening or concavity of the echogenic subdeltoid bursal fat (often accentuated with compression), substantial subdeltoid bursal fluid, and cortical irregularity of the humeral tuberosity adjacent to the tear [2,3,4] (Fig. 2A,2B).

View larger version (170K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Rotator cuff tear and normal anatomy. Longitudinal (A) and transverse (B) sonograms of 64-year-old man reveal massive, complete full-thickness tear of supraspinatus tendon with large defect extending from articular to bursal surface (double arrow). Note marked retraction (arrow) of torn proximal tendon end and debris (arrowheads) present within defect. H = humeral head, D = deltoid muscle, m = medial, l = lateral, a = anterior, p = posterior.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Rotator cuff tear and normal anatomy. Longitudinal (A) and transverse (B) sonograms of 64-year-old man reveal massive, complete full-thickness tear of supraspinatus tendon with large defect extending from articular to bursal surface (double arrow). Note marked retraction (arrow) of torn proximal tendon end and debris (arrowheads) present within defect. H = humeral head, D = deltoid muscle, m = medial, l = lateral, a = anterior, p = posterior.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —Rotator cuff tear and normal anatomy. Longitudinal sonogram of healthy 28-year-old woman shows normal supraspinatus tendon (arrowheads). G = greater tuberosity, l = lateral, m = medial.

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —54-year-old woman with rotator cuff tear. Longitudinal (A) and transverse (B) sonograms of supraspinatus tendon reveal full-thickness tear, confirmed at surgery. Several secondary signs of full-thickness rotator cuff tear are present including cortical irregularity (solid arrow) of tuberosity adjacent to tendon tear, volume loss (double arrow), subacromial—subdeltoid bursal contour deformity and flattening (open arrows), and subdeltoid bursal distention (arrowhead). l = lateral, m = medial, a = anterior, p = posterior.

View larger version (110K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —54-year-old woman with rotator cuff tear. Longitudinal (A) and transverse (B) sonograms of supraspinatus tendon reveal full-thickness tear, confirmed at surgery. Several secondary signs of full-thickness rotator cuff tear are present including cortical irregularity (solid arrow) of tuberosity adjacent to tendon tear, volume loss (double arrow), subacromial—subdeltoid bursal contour deformity and flattening (open arrows), and subdeltoid bursal distention (arrowhead). l = lateral, m = medial, a = anterior, p = posterior.

A retracted tear results in a large hypoechoic to anechoic fluid-filled space that may show echogenic debris (Fig. 1A,1B,1C). The deltoid muscle may closely approximate the humeral head in the space normally occupied by the rotator cuff tendons (Fig. 3).

View larger version (114K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —80-year-old woman with rotator cuff tear. Longitudinal sonogram shows chronic full-thickness tear of retracted supraspinatus tendon (solid arrows). Note deltoid muscle (D) is adjacent to humeral head (H) within space (between open arrows and arrowheads) normally occupied by distal supraspinatus tendon. l = lateral, m = medial.

Sonographic findings of a partial-thickness tear include a focal hypoechoic defect reaching either the bursal or the articular surface, but not both, similar to criteria for MR imaging examinations (Fig. 4A,4B). Typically, no significant volume loss or subdeltoid contour abnormality is seen [5].

View larger version (100K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —67-year-old man with partial-thickness rotator cuff tear. Longitudinal (A) and transverse (B) sonograms of supraspinatus tendon show discrete bursal surface defect (black arrows) representing partial-thickness tear with intact articular surface fibers present (white arrows). l = lateral, m = medial, a = anterior, p = posterior.

View larger version (102K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —67-year-old man with partial-thickness rotator cuff tear. Longitudinal (A) and transverse (B) sonograms of supraspinatus tendon show discrete bursal surface defect (black arrows) representing partial-thickness tear with intact articular surface fibers present (white arrows). l = lateral, m = medial, a = anterior, p = posterior.

Tendinosis is considered mucoid degeneration without significant inflammation and can be associated with a painful shoulder. Findings include heterogeneity and thickening of the tendon without discrete defects (Fig. 5).

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —51-year-old man with supraspinatus tendinosis. Longitudinal sonogram of supraspinatus tendon shows diffuse thickening and heterogeneity (white arrows) without discrete defect, consistent with diffuse tendinosis. Note small region of relatively spared normal fibrillar pattern of tendon (black arrows). m = medial, l = lateral.

Calcium hydroxyapatite deposition within the rotator cuff tendons and adjacent bursa is a cause of pain that can simulate symptoms of a rotator cuff tear [6]. Calcifications appear as echogenic foci that typically shadow (Fig. 6), although small calcifications may not show shadowing.

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6. —37-year-old woman with calcific tendinitis. Longitudinal sonogram of supraspinatus tendon reveals large irregular hyperechoic foci (black arrows) with associated distal shadowing (white arrows), along with several smaller lesions, representing intrasubstance calcifications. Tendon is also focally thickened. m = medial, l = lateral.

Fluid surrounding the biceps tendon may indicate simple joint effusion or biceps tenosynovitis, especially when power Doppler sonography shows increased flow (Fig. 7A,7B). Loose bodies in the shoulder joint may travel into the dependent bicipital sheath when an effusion is present (Fig. 8). The long head of the biceps tendon can be displaced from the bicipital groove, usually in a medical direction (Fig. 9). The tendon may be subluxed so that it is partially displaced over the lesser tuberosity or fully dislocated, often with an associated tear of the subscapularis tendon [7]. Rupture of the long head of the biceps tendons can also occur, resulting in discontinuity of the tendon and associated hematoma [8] (Fig. 10A,10B,10C).

View larger version (162K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7A. —72-year-old woman with biceps tenosynovitis. Transverse sonogram of anterior shoulder shows circumferential hypoechoic fluid (black arrows) surrounding slightly thickened and heterogeneous long head of biceps tendon (white arrows). L = lesser tuberosity, G = greater tuberosity.

View larger version (94K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7B. —72-year-old woman with biceps tenosynovitis. Transverse sonogram with power Doppler sonography reveals increased flow in peripheral ring pattern representing inflammation of bicipital tendon sheath synovium.

View larger version (189K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8. —66-year-old man with left glenohumeral joint loose bodies. Transverse sonogram of anterior shoulder reveals several small echogenic foci (arrowheads) medial to intraarticular portion of biceps tendon (arrows), floating within joint effusion. Echogenic foci were mobile on real-time dynamic imaging, confirming presence of loose bodies.

View larger version (129K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 9. —42-year-old man with pain and weakness of left shoulder. Transverse sonogram of anterior left shoulder shows dislocation of long head of biceps tendon (arrows) medially out of bicipital groove (arrowheads). Subscapularis tendon was torn on sonographic examination. Findings were confirmed at surgery. L = lesser tuberosity.

View larger version (142K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 10A. —68-year-old man with ruptured biceps tendon and hematoma. Longitudinal sonograms of long head of biceps tendon show completely ruptured and retracted tendon (white arrows) with massive fluid collection slightly more distally, representing chronic hematoma (black arrows). Note frayed end of residual tendon (arrowheads). Image in B was obtained just distal to A. p = proximal, d = distal.

View larger version (87K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 10B. —68-year-old man with ruptured biceps tendon and hematoma. Longitudinal sonograms of long head of biceps tendon show completely ruptured and retracted tendon (white arrows) with massive fluid collection slightly more distally, representing chronic hematoma (black arrows). Note frayed end of residual tendon (arrowheads). Image in B was obtained just distal to A. p = proximal, d = distal.

View larger version (100K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 10C. —68-year-old man with ruptured biceps tendon and hematoma. Transverse sonogram shows biceps tendon (small arrow) surrounded by massive liquefied hematoma (large arrows).

Ganglion cysts commonly occur within the suprascapular or spinoglenoid notch, or both, and may cause symptoms by exhibiting a mass effect on adjacent structures. Compression of the suprascapular nerve may cause supraspinatus and infraspinatus muscle atrophy. Ganglion cysts appear as well-defined, round or lobulated, anechoic lesions, and may show posterior acoustic enhancement [9] (Fig. 11).

View larger version (146K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 11. —27-year-old man with spinoglenoid notch ganglion cyst. Longitudinal sonogram of posterior shoulder reveals cystic lesion (black arrows) in spinoglenoid notch region consistent with ganglion cyst. Note posterior scapular cortex (arrowheads) immediately beneath scapular spine and humeral head cortex (white arrows).

Patients are often referred for sonography to exclude a rotator cuff tear after a traumatic episode and normal findings on radiologic examination. The tomographic nature of sonography allows imaging in multiple planes to optimally reveal a subtle cortical disruption representing a minimally displaced fracture, most commonly involving the greater tuberosity [10] (Fig. 12A,12B). Direct correlation to patient symptomatology with transducer pressure is helpful. A Hill-Sachs lesion can be evaluated with sonography in the setting of anterior shoulder dislocation (Fig. 13).

View larger version (129K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 12A. —36-year-old man with occult greater tuberosity fracture after trauma. Longitudinal (A) and transverse (B) sonograms of right shoulder reveal cortical disruption of greater tuberosity (arrows) at supraspinatus insertion. Fracture was not identified on radiographs obtained a week before sonographic examination. l = lateral, m = medial, a = anterior, p = posterior.

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 12B. —36-year-old man with occult greater tuberosity fracture after trauma. Longitudinal (A) and transverse (B) sonograms of right shoulder reveal cortical disruption of greater tuberosity (arrows) at supraspinatus insertion. Fracture was not identified on radiographs obtained a week before sonographic examination. l = lateral, m = medial, a = anterior, p = posterior.

View larger version (129K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 13. —65-year-old man with history of left anterior shoulder dislocation. Longitudinal sonogram of posterior shoulder shows notched defect present in posterolateral aspect of humeral head (H) consistent with Hill-Sachs lesion (arrowheads). Infraspinatus tendon was intact. m = medial, l = lateral.

Elbow

Top Introduction Shoulder Elbow Hand and Wrist References

 
Sonography is sensitive for the detection of a joint effusion in the elbow. The joint capsule will be distended by hypoechoic to anechoic fluid displacing the fat pads, seen best in the posterior recess with the elbow flexed (Fig. 14). When there is clinical concern for septic arthritis, sonographically guided aspiration of the joint fluid can be performed [1].

View larger version (157K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 14. —76-year-old man with elbow joint effusion. Transverse sonogram of posterior elbow held in flexed position shows large amount of fluid present in olecranon fossa, representing joint effusion (asterisk). Sonographically guided aspiration of fluid revealed infection consistent with septic arthritis. Note posterior humeral cortex of posterior fossa (arrows). l = lateral, m = medial.

Inflammation of the olecranon bursa is a common condition that can be confused with other sources of elbow pain. Characteristic findings of olecranon bursitis include hypoechoic distention of the olecranon bursa with increased power Doppler sonography flow, typically in a rimlike fashion (Fig. 15A,15B).

View larger version (135K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 15A. —47-year-old man with right elbow olecranon bursitis. Longitudinal sonogram of elbow superficial to olecranon process (O) shows marked thickening of soft tissues with irregular anechoic fluid collection (arrows) representing distended olecranon bursa. Note dorsal cortex of olecranon (arrowheads). p = proximal, d = distal.

View larger version (129K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 15B. —47-year-old man with right elbow olecranon bursitis. Longitudinal sonogram with power Doppler sonography shows increased flow in synovium around periphery, consistent with olecranon (O). Arrows indicate bursal fluid collection; arrowheads indicate dorsal cortex of olecranon.

The distal triceps tendon insertion onto the posterior olecranonis is well visualized with sonography; however, the distal biceps tendon insertion onto the radial tuberosity is more difficult to consistently visualize [11]. Directed inspection of these structures can reveal injuries ranging from strains to complete rupture (Fig. 16A,16B).

View larger version (155K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 16A. —20-year-old woman with partial triceps muscle tear. Longitudinal (A) and transverse (B) sonograms of distal triceps muscle near musculotendinous junction show discrete defect involving long head of triceps muscle, representing tear (arrows). p = proximal, d = distal, m = medial, l = lateral.

View larger version (119K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 16B. —20-year-old woman with partial triceps muscle tear. Longitudinal (A) and transverse (B) sonograms of distal triceps muscle near musclotendinous junction show discrete defect involving long head of triceps muscle, representing tear (arrows). p = proximal, d = distal, m = medial, l = lateral.

With epicondylitis, there is thickening and hypoechogenicity of the tendon at the attachment on the epicondyle [1]. Calcification within the tendon can indicate chronic injury and should be correlated with radiologic findings. Tenderness with transducer pressure is a helpful secondary finding. Integrity of collateral ligaments in the elbow, particularly the ulnar collateral ligament, is also accessible to sonographic examination [1] (Fig. 17).

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 17. —24-year-old man with ulnar collateral ligament tear. Longitudinal split-screen image compares abnormal, torn ulnar collateral ligament on left with that of normal, intact ulnar collateral ligament (black arrows) on right. Heterogeneous, relatively hypoechoic material (white arrows) is in expected location of left ulnar collateral ligament and represents debris and hemorrhage. Note medial epicondyle (arrowheads) of humerus (H) and medial proximal ulna (U).

Enlargement of the lymph nodes can be revealed sonographically. Cat-scratch disease classically involves the medial epitrochlear lymph nodes of the elbow after a superficial wound inflicted by a cat's claw (Fig. 18). Reactive lymph nodes maintain a kidney bean shape with a typical echogenic central region related to multiple interfaces.

View larger version (151K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 18. —73-year-old man with enlarged epitrochlear lymph nodes. Longitudinal sonogram of medial elbow shows several ovoid masses representing enlarged epitrochlear lymph nodes (arrows) from nonspecific cause. Sonographically guided core biopsy was performed that did not reveal malignancy or infection. p = proximal, d = distal.

The ulnar nerve is normally positioned in the cubital tunnel along the posteromedial aspect of the distal humerus, in a groove adjacent to the medial epicondyle. Cubital tunnel syndrome is a result of inflammation of the ulnar nerve manifested by an enlarged, hypoechoic appearance on sonography. Dynamic imaging can reveal intermittent subluxation of the ulnar nerve, a cause of ulnar neuritis [12].

Hand and Wrist

Top Introduction Shoulder Elbow Hand and Wrist References

 
Ganglion cysts represent the most common soft-tissue mass in the hand and wrist and are generally attached to tendon sheaths, muscles, or cartilage. Unlike synovial cysts, ganglia do not have a synovial lining and infrequently communicate with a joint. Sonography reveals a hypoechoic to anechoic well-defined structure with posterior acoustic enhancement consistent with a cystic lesion [13] (Fig. 19).

View larger version (135K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 19. —48-year-old woman with nontender palpable mass involving snuff box region of her hand. Longitudinal sonogram of thumb revealed superficial simple cystic lesion (arrows) adjacent to extensor pollucis longus tendon (arrowheads) representing ganglion cyst. p = proximal, d = distal.

Tenosynovitis appears as tendon sheath distention from fluid and thickened synovium. Increased flow on power Doppler sonography indicates synovial inflammation (Fig. 20A,20B). Coexisting tendinosis or tendon tear may be present.

View larger version (145K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 20A. —28-year-old woman with systemic lupus erythematosis and swollen, painful left index finger. Transverse sonogram of flexor compartment of index finger adjacent to middle phalynx cortex (white arrows) shows hypoechoic distention of tendon sheath (black arrows) and slight heterogeneity of flexor tendon (arrowheads).

View larger version (73K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 20B. —28-year-old woman with systemic lupus erythematosis and swollen, painful left index finger. Transverse power Doppler sonogram reveals peripheral pattern of increased flow consistent with tenosynovitis.

Carpal tunnel syndrome is a peripheral neuropathy frequently related to occupational causes. Compression of the median nerve may result in neuropathy with pain and paresthesias in a typical distribution. Sonographically, carpal tunnel syndrome appears as enlargement and hypo-echogenicity of the median nerve [14] (Fig. 21).

View larger version (111K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 21. —32-year-old woman with carpal tunnel syndrome. Transverse sonogram of left wrist reveals enlarged cross-sectional area of median nerve (black arrows), consistent with diagnosis of carpal tunnel syndrome. Findings were confirmed with electromyography. Note flexor tendons (white arrows). r = radial, u = ulnar.

References

Top Introduction Shoulder Elbow Hand and Wrist References

 

1. Jacobson JA, van Holsbeeck MT. Musculoskeletal ultrasonography. Orthop Clin North Am 1998;29:135 -167[Medline]
2. Wiener SN, Seitz WH. Sonography of the shoulder in patients with tears of the rotator cuff: accuracy and value of selecting surgical options. AJR 1993;160:103 -107[Abstract/Free Full Text]
3. Hollister MS, Mack LA, Patten RM, Winter TC, Matsen FA, Veith RR. Association of sonographically detected subacromial/subdeltoid bursal effusion and intraarticular fluid with rotator cuff tear. AJR 1995;165:605 -608[Abstract/Free Full Text]
4. Wohlwend JR, van Holsbeeck M, Craig J, et al. The association between irregular greater tuberosities and rotator cuff tears: a sonographic study. AJR 1998;171:229 -233[Abstract/Free Full Text]
5. van Holsbeeck MT, Kolowich PA, Eyler WR, et al. US depiction of partial-thickness tear of the rotator cuff. Radiology 1995;197:443 -446[Abstract/Free Full Text]
6. Farin PU, Jaroma K. Sonographic findings of rotator cuff calcifications. J Ultrasound Med 1995; 14:7 -14[Abstract]
7. Farin PU, Jaroma H, Harju A, Soimakallio S. Medial displacement of the biceps brachii tendon: evaluation with dynamic sonography during maximal external shoulder rotation. Radiology 1995;195:845 -848[Abstract/Free Full Text]
8. Ptasznik R, Hennessy O. Abnormalities of the biceps tendon of the shoulder: sonographic findings. AJR 1995;164:409 -414[Abstract/Free Full Text]
9. Hashimoto BE, Hayes AS, Ager JD. Sonographic diagnosis and treatment of ganglion cysts causing suprascapular nerve entrapment. J Ultrasound Med 1994;13:671 -674[Abstract]
10. Patten RM, Mack LA, Wang KY, Lingel J. Nondisplaced fractures of the greater tuberosity of the humerus: sonographic detection. Radiology 1992;182:201 -204[Abstract/Free Full Text]
11. Lozano V, Alonso P. Sonographic detection of the distal biceps tendon rupture. J Ultrasound Med 1995;14:389 -391[Medline]
12. Lin J, Fessell DP, Jacobson JA, Weadock WJ, Hayes CW. An illustrated tutorial of musculoskeletal sonography. 1. Introduction and general principles. AJR 2000;175:637 -645[Free Full Text]
13. Bianchi S, Abdelwahab IF, Zwass A, Giacomello P. Ultrasonographic evaluation of wrist ganglia. Skeletal Radiol 1994;23:201 -203[Medline]
14. Duncun I, Sullivan P, Lomas F. Sonography in the diagnosis of carpal tunnel syndrome. AJR 1999;173:681 -684[Abstract/Free Full Text]

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This Article Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lin, J. Articles by Hayes, C. W. Search for Related Content PubMed PubMed Citation Articles by Lin, J. Articles by Hayes, C. W. Social Bookmarking                      What's this?