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ULTRASOUND N February 2005 N Volume 13 N Number 1 Ultrasonography of the Shoulder D. P. O’Regan, A. K. Lim & A. W. M. Mitchell Imaging Sciences Department, Hammersmith Hospital, London, UK Introduction Examination of the shoulder with ultrasound has become a widely accepted method of evaluating a number of musculoskeletal pathologies. The continuing advancements made in imaging technology have allowed ultrasound to develop into a powerful diagnostic tool. Ultrasound has the advantage of producing high-resolution dynamic images of the shoulder, as well as allowing the operator to perform image-guided interventions, such as cyst aspiration or steroid injections. Its main role has continued to be in diagnosing partial and fullthickness rotator cuff injuries, and it allows the assessment of size, location and extension of tears. It has good correlation to intra-operative findings1 and compares favourably to MRI, particularly in the diagnosis of partial rotator cuff tears.2 In experienced hands it provides a rapid and cost-effective evaluation of the painful shoulder.3 Ultrasound also provides information about intra-articular abnormalities, such as labral tears, loose bodies and synovial disease, as well as evaluating joint effusions and acromio-clavicular joint arthropathies.4 In this article, we provide a detailed guide on how to perform a standard ultrasound examination of the shoulder with illustrations of patient positioning, and examples of the normal sonographic appearances of the rotator cuff and associated structures. Some important diagnostic pitfalls that may be encountered will be discussed. Rotator Cuff Anatomy The rotator cuff is a complex of four muscles that arise from the scapula and whose tendons blend with the joint capsule as they insert onto the humeral tubercles (Fig. 1). Supraspinatus is clinically the most important rotator cuff tendon as it is usually involved, either alone or in combination with other cuff tendons, in the great majority of tears. The muscle arises from the supraspinous fossa of the scapula and passes inferior to the acromion process. It follows the curvature of the superior humeral head and its fibres insert onto the superior facet of the greater tubercle of the humerus. The subacromial sub-deltoid bursa lies between the rotator cuff and the subacromial arch, and may contain a thin layer of fluid in asymptomatic individuals.5 Thus, the supraspinatus muscle has a deep articular surface and a superficial bursal surface. The overlying deltoid muscle is characteristically less echogenic than the underlying supraspinatus tendon. Infraspinatus and teres minor arise from the infraspinous fossa and lateral border of the scapula, respectively, and insert onto the middle and inferior facets of the greater tubercle. The subscapularis muscle arises from the costal surface of the scapula and its tendon inserts independently of the other rotator cuff muscles onto the lesser tubercle. The long head of the biceps tendon traverses the rotator cuff interval, which separates the supraspinatus and subscapularis tendons, and is held in place by the coracohumeral ligament and transverse humeral ligament. The shallow glenoid fossa Correspondence: Declan O’Regan, Imaging Sciences Department, Hammersmith Hospital, London W12 0HS, UK, [email protected] ß British Medical Ultrasound Society 2005 48 Figure 1. The muscles of the rotator cuff seen posteriorly (subscapularis not shown). Reproduced with permission from Gray’s Anatomy for Students, Churchill Livingstone 2004. is enlarged by the cartilaginous labrum. The head of the humerus is kept within the centre of the labrum by both static and dynamic stabilizers. The superior, middle and inferior glenohumeral ligaments, and the joint capsule provide static stabilization. Dynamic stability is achieved by the co-ordinated actions of the rotator cuff muscles with biceps and deltoid having an accessory role. The rotator cuff has three principle actions: N N N it rotates the humerus with respect to the scapula; it compresses the humeral head into the glenoid fossa; it provides muscular stability during shoulder movements.6 Ultrasound Equipment Transducers with frequencies in the range from 8 to 15 MHz have become standard equipment on modern machines. In larger patients, a lower frequency probe may sometimes be necessary (5–7.5 MHz) for adequate penetration. Small footprint transducers are also now available, which improve skin contact and reduces anisotropy. The availability of extended field-of-view or panoramic imaging also helps to demonstrate whole segments of tendons to rival the coverage achieved with MR imaging. Power or colour Doppler is standard on most equipment, and is helpful when evaluating the presence of inflammatory changes. Real time compound imaging is available on a number of machines, and this significantly reduces the intrinsic artefacts and noise of conventional sonography, thus improving image quality (Fig. 2).7 Some machines also have post-processing image algorithms, such as XRES (Philips, Holland), which may improve visualization of tissue textures and margins. The image quality can also be improved by increasing the number of focal zones, although this leads to a reduction in frame DOI: 10.1179/174313405X27481 ULTRASOUND N February 2005 N Volume 13 N Number 1 (a) Figure 4. Longitudinal section of the biceps tendon acquired with the patient’s hand supinated and resting on their knee. The lamellar structure of the tendon (asterisk) can be readily appreciated. It is enclosed by synovium and small joint effusions may be apparent at the level of its musculo-tendinous junction. rate. Two or three focal zones are typically used in standard practice. The ultrasound images is this article were acquired from a normal volunteer with a Philips HDI 5000 ultrasound machine using a 12 MHz linear probe, using SonoCT compound imaging with two focal zones. (b) Examination Technique Figure 2. (a) The upper image of supraspinatus was acquired with compound imaging in which the ultrasound beam is steered in multiple offaxis lines-of-sight and rendered into a real time image. It provides improved image contrast and interface definition compared to the conventional image below (b). It is important that both the patient and operator are positioned correctly to allow optimal imaging of the rotator cuff. Typically, the patient is seated on a backless chair or stool, which allows Figure 3. The patient places their supinated hand over their knee and the probe is positioned anterolaterally to follow the course of the biceps tendon as it passes through the rotator cuff interval. Figure 5. The patient hyper extends and internally rotates their shoulder to reveal the supraspinatus tendon from under the acromion process. 49 ULTRASOUND N February 2005 N Volume 13 N Number 1 Figure 6. Long axis of the supraspinatus tendon with the arm in hyperextension and internal rotation. Supraspinatus curves over the head of the humerus to insert onto the greater tubercle (arrowheads). The tendon is hyper-echoic compared with the overlying deltoid muscle (asterisk). No fluid is visible in the intervening sub-acromial sub-deltoid bursa (arrows). Figure 7. The patient places their hand over their opposite shoulder to bring it into internal rotation and flexion. The probe is placed to view the infraspinatus tendon near its attachment. Figure 8. Infraspinatus (asterisk) in its long axis as its fibres converge onto the middle facet on the greater tubercle between supraspinatus and teres minor. Figure 9. The patient turns their shoulder into external rotation to view subscapularis. Figure 10. The biceps tendon (arrowhead) traverses the rotator cuff interval along the border of subscapularis (asterisk). 50 the operator convenient access to the desired imaging planes. This position also permits the patient to freely move their arm into a favourable position for imaging a particular tendon and facilitates shoulder movement during dynamic sonography. It is important that the patient should be allowed to move their shoulder actively to avoid causing unnecessary discomfort. Most operators find the examination is most comfortably ULTRASOUND N February 2005 N Volume 13 N Number 1 performed from behind the patient, although others prefer to scan while facing the patient. To begin with, the patient is asked to place their supinated hand over their knee (Fig. 3). The probe is placed over the anterolateral aspect of the humeral neck in the axial plane, where the biceps tendon can be readily identified lying in the intertubercular groove. Its proximal course through the rotator cuff interval can be demonstrated as it passes between the supraspinatus and subscapularis, and deep to the coracohumeral ligament. The probe may then be rotated to view the biceps tendon in its long axis (Fig. 4). The tendon is enclosed by synovium and the musculotendinous junction is the most dependent part of the joint, where small effusions may only be apparent.8 The patient is then asked to place their hand behind their back over their buttock, as though in their back trouser pocket (Fig. 5). This puts the shoulder joint into hyperextension and internal rotation allowing the supraspinatus tendon to be better demonstrated. The supraspinatus muscle runs in a coronal oblique plane under the acromion process, and may be visualized in short and long axis planes (Fig. 6). The fibrillar structure of the tendon may be appreciated as it passes under the deltoid muscle and over the humeral head. Supraspinatus has a smooth fibrocartilaginous insertion on the greater tubercle of the humerus, which typically appears hypo-echoic compared with the tendon itself. The sub-acromial sub-deltoid bursa should have no more than a trace of fluid within it. The other rotator cuff muscles are then examined in turn. First, the patient places their arm across their chest with their shoulder in flexion and internal rotation to reveal the infraspinatus and teres minor tendons (Figs 7 and 8). Orientation may be gained by following the tendons to their insertion where, in the short axis plane, the anterior portion of the cuff insertion is formed by supraspinatus and the posterior portion by infraspinatus and teres minor. Lastly, subscapularis is shown to best advantage by asking the patient to bring their arm by their side and turn their shoulder into external rotation (Figs 9 and 10). Dynamic imaging to test for impingement may be performed by placing the probe both coronally and sagittally lateral to the acromion process. The patient is asked to abduct and adduct their arm to assess for the smooth movement of supraspinatus under the acromion process. The examination may be completed by visualizing the non-tendinous structures of the shoulder. In particular the acromio-clavicular joint may be readily examined for arthropathy, and the glenoid labrum evaluated for labral cysts and tears, although these are more reliably assessed with MRI. Synovitis may also be seen as thickening of the joint capsule with hyperaemia on Doppler imaging. (a) (b) Figure 11. (a) Transverse section of the biceps tendon as it lies in the intertubercular groove (arrows). The image was acquired with the probe perpendicular to the tendon, while (b) was acquired at a shallower angle of insonation. This demonstrates the phenomenon of anisotropy in tendinous structures, which may be mistaken for a pathological defect. Pitfalls Some important pitfalls that may be encountered are either due to artefacts of the ultrasound technique or to misinterpretation of the complex anatomy of the rotator cuff and surrounding structures. The echogenicity of tendons is highly angle dependent, a characteristic called anisotropy. The lamellated structure of the tendon causes it to have maximum echogenicity when insonated perpendicularly, and it becomes hypo-echoic at more shallow angles (Fig. 11).9 This reduction in tendon reflectivity may be mistaken for a tear. This phenomenon can be readily observed by changing the angle of insonation of the probe in real time. The rotator cuff muscles have a multipennate structure and coalesce onto the joint capsule. The interdigitating fibres produce alternating bands of reflectivity within the tendons near their insertion and this heterogeneity must not be mistaken for pathology (Fig. 12).10 Figure 12. The tendinous interdigitations around the insertion of supraspinatus should not be mistaken for partial tears. The rotator cuff interval may also give the impression of a tendinous defect, while an oblique view of the biceps tendon may mimic the appearance of a longitudinal tear of the 51 ULTRASOUND N February 2005 N Volume 13 N Number 1 adjacent supraspinatus. However, these appearances may be readily resolved by turning the probe to appreciate the tendon in its long axis and its relationship to the rotator cuff interval. 2. Teefey SA, Rubin DA, Middleton WD, Hildebolt CF, Leibold RA, Yamaguchi K. Detection and quantification of rotator cuff tears. Comparison of ultrasonographic, magnetic resonance imaging, and arthroscopic findings in seventy-one consecutive cases. J Bone Jt Surg Am 2004;86-A:708–716. 3. Dinnes J, Loveman E, McIntyre L, Waugh N. The effectiveness of diagnostic tests for the assessment of shoulder pain due to soft tissue disorders: a systematic review. Hlth Technol Assess 2003;7(29):iii,1–166. 4. Peetrons P, Rasmussen OS, Creteur V, Chhem RK. Ultrasound of the shoulder joint: non ‘rotator cuff’ lesions. Eur J Ultrasound 2001;14:11–19. 5. Schmidt WA, Schmidt H, Schicke B, Gromnica-Ihle E. Standard reference values for musculoskeletal ultrasonography. Ann Rheum Dis 2004;63:988–994. 6. Hess SA. Functional stability of the glenohumeral joint. Man Ther 2000;5(2):63–71. 7. De Candia A, Doratiotto S, Paschina E, Segatto E, Pelizzo F, Bazzocchi M. Real-time compound sonography of the rotator-cuff: evaluation of artefact reduction and image definition. Radiol Med (Torino) 2003;105(4):308–314. 8. Allen GM, Wildon DJ. Ultrasound of the shoulder. Eur J Ultrasound 2001;14:3–9. 9. Crass JR, van de Vegte GL, Harkavy LA. Tendon echogenicity: ex vivo study. Radiology 1988;167:499–501. 10. Thain LM, Adler RS. Sonography of the rotator cuff and biceps tendon: technique, normal anatomy, and pathology. J Clin Ultrasound 1999;27(8):446–458. Conclusions Shoulder ultrasound has matured into an accurate and costeffective technique for non-invasive imaging of the rotator cuff and surrounding structures. It has a comparable accuracy with MRI for identifying cuff tears and has the advantage of providing a dynamic assessment of muscle impingement. It requires a sound knowledge of ultrasound techniques and musculoskeletal anatomy, as well as familiarity with the common imaging pitfalls. A period of formal training and continuing audit is recommended to ensure operator accuracy. References 1. 52 Zehetgruber H, Lang T, Wurnig C. Distinction between supraspinatus, infraspinatus and subscapularis tendon tears with ultrasound in 332 surgically confirmed cases. Ultrasound Med Biol 2002;28:711–717.