International Journal of Rheumatic Diseases 2014; 17: 709–713

EDITORIAL

Ultrasound in Rheumatology Ultrasound has changed the diagnostic approach in daily rheumatology practice within the last years. It helps provide clearly distinct findings and assists clinical examination. Technology has considerably improved. It allows generating excellent images of anatomical structures with a resolution of up to 0.1 mm. Furthermore, when ultrasound is done in the context of a clinical examination, dynamic imaging provides further information. Ultrasound does not replace clinical examination. Instead it helps to even improve clinical skills as findings are becoming much clearer. Ultrasound is well tolerated by patients without any side effects. While performing ultrasound, findings can readily be explained to the patient. Time is needed for learning ultrasound. However, time consumption is moderate if an experienced sonographer performs ultrasound exclusively for addressing specific questions that cannot be answered only by history and clinical examination alone. To date, ultrasound can provide a plethora of different findings for even more indications. This brief overview provides lists of the most important findings and indications for ultrasound in rheumatology practice.











Doppler signals cover more than 50% of the synovium.6 A drawback of this grading system is that the majority of inflamed joints present with grade 2. Future scoring systems may rely just on the ratio of the synovium covered by color. Tenosynovitis is characterized by hypoechoic or anechoic thickened tissue in the tendon sheath (Fig. 1) that may exhibit Doppler signals.1 Paratenonitis describes inflamed peritendinous tissue of tendons without a tendon sheath such as the Achilles tendons or the extensor digitorum tendons at the level of the metacarpophalangeal (MCP) joints. Tendon damage may be graded just as partial or total tear.7 This may occur due to inflammation or trauma. Tendons commonly involved are the tendons of the rotator cuff, the long biceps tendon, digital extensor tendons or Achilles tendons. Bursitis is represented by an abnormal fluid collection or abnormal tissue in bursae such as subdeltoid bursae (Fig. 3) or Baker’s cysts. Foreign bodies can be well seen, as well as needles (Fig. 3). Therefore, ultrasound is very helpful in guiding injections and aspirations.8

PATHOLOGIES SEEN BY ULTRASOUND The following abnormalities can be seen by ultrasound. • Effusion is anechoic (black), compressible and displaceable, and it does not exhibit any Doppler signals.1 • Synovitis is hypoechoic (gray), poorly compressible and not displaceable (Fig. 1). It may exhibit Doppler signals depending on the inflammatory activity of the joint (Fig. 2). Synovitis may be graded as mild (only found in recesses; grade 1), moderate (capsule parallel to bone or straight; grade 2) or severe (2 – 4 capsule convex; grade 3). This applies to small joints2 as well as to large joints in RA and in spondyloarthritides.5 Vascularity may be graded as mild (grade 1) if up to three signals are seen in one plane, as moderate (grade 2) if confluent or more than three signals are seen in the synovium and as severe (grade 3) if

Figure 1 Volar longitudinal view of a metacarpophalangeal 2 joint of a patient with concomitant rheumatoid arthritis and osteoarthritis with flexor tendon tenosynovitis*, synovitis seen in the proximal recess of the joint** and an osteophyte***.

© 2014 Asia Pacific League of Associations for Rheumatology and Wiley Publishing Asia Pty Ltd

Editorial

Figure 2 Lateral longitudinal view of a metacarpophalangeal 2 joint of a patient with crystal disease (hydroxy-apatite) with intra-articular crystal deposits*, erosion** and abnormal Doppler signals ***indicating hyperperfusion grade 2 due to active inflammatory synovitis.

Figure 3 Anterior transverse view of the right arm below the shoulder showing a subdeltoid bursitis* with a needle** coming from lateral and minor tenosynovitis of the biceps tendon***.

• Enthesitis is characterized by an decreased echogenicity and increased thickness of the inserting tendon, erosions of the underlying bones, bony spurs, calcifications and increased vascularity9 (Fig. 4). • Compressed nerves become edematous. Thus they are hypoechoic and enlarged. Furthermore, ultrasound may detect the reason for compression, for example tenosynovitis or synovitis, as a cause of carpal tunnel syndrome. • Erosions are discontinuities of the bone surface (Figs 3,4) that can be displayed in two planes.1 In rheumatoid arthritis (RA) erosions localize intra-articularly. They may also occur outside the joint in

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Figure 4 Enthesitis of the insertion of the Achilles tendon. The Achilles tendon is hypoechoic, thickened, heterogeneous and exhibits increased vascularity*. The region of the retrocalcaneal bursa also shows increased vascularity**. The surface of the calcaneus is irregular with a small erosion***.

gout or at entheses, particularly in spondyloarthritis (Fig. 4). They are typically U-shaped and irregular in RA. In psoriatic arthritis, often very small erosions are present together with small osteophytes. Physiological cortical breaks may occur for instance due to small feeding vessels of the bones. Their shape is more regular and their diameter is usually < 1 mm. Single physiological cortical breaks of a diameter below 4 mm may occur at the lateral side of the humeral head below the rotator cuff. Ultrasound is more sensitive than conventional radiography of hands and feet, in particular for detecting erosions at the MCP2, MCP5, metatarsophalangeal (MTP)1 and MTP5 joints. • Elastography is an evolving ultrasound technique for evaluating the stiffness of a tendon. The stiffness decreases with inflammation.10 • Osteophytes are bony spurs adjacent to the joint space (Fig. 1). Ultrasound is more sensitive than conventional X-ray for detecting osteophytes, particularly at MCP joints.2 • Crystal depositions are well seen by ultrasound. In gout tophi appear as intra- or extra-articular circumscribed, inhomogeneous, hyperechoic aggregation. This aggregation may be surrounded by a small anechoic rim. It may generate posterior acoustic shadows. Gout tophi exhibit a typical snow-storm like appearance. Furthermore, urate crystals may distribute on the cartilage leading to an abnormal hyperechoic band over the superficial margin of the articular hyaline cartilage, independent of the angle of insonation. These bands are often slightly irregular. The band is usually as thick as the echoes resulting from the bone surface.

International Journal of Rheumatic Diseases 2014; 17: 709–713

Editorial

Therefore this is called ‘double contour sign’. Aggregates, small hyperechoic foci that maintain their high degree of reflectivity even when the gain setting is minimized or the insonation angle is changed are less specific for gout.3 Chondrocalcinosis and hydroxyapatite crystal arthritis lead to slightly more condense aggregates (Fig. 2). Crystal deposits in chondrocalcinosis localize particularly within the fibrocartilage and the hydrocartilage, but less commonly on the cartilage. In most cases chondrocalcinosis can be well distinguished from gout by ultrasound. • Furthermore, ultrasound is a valuable tool also for extra-articular manifestations of rheumatic diseases, including connective tissue diseases and vasculitides. Ultrasound does not need to be performed in every patient with a suspected or established rheumatic disease. However, it should be used in unclear situations in order to make further diagnostic or therapeutic decisions. Below, the main indications for ultrasound in rheumatology are listed.

INDICATIONS FOR ULTRASOUND IN RHEUMATOLOGY • In RA clinical examination may reveal ambivalent findings. This may be particularly the case in MTP joints, ankle joints, hips and shoulders, but also in diffusely swollen wrists and fingers. Both the presence of intra-articular power Doppler signals and the detection of extensor carpi ulnaris tenosynovitis are predictors of erosive disease. In case of early arthritis with clinically definite synovitis, ultrasound might be only performed at MCP2, MCP5 and MTP5 joints for detecting erosions in radiographically negative cases. • Sometimes it is difficult to clinically distinguish osteoarthritis of MCP and proximal interphalangeal (PIP) joints from RA. Ultrasound provides important information by evaluating the bone surface in order to decide whether erosions of osteophytes prevail. • In spondyloarthritides ultrasound is particularly valuable for detecting enthesitis, including plantar fasciitis. In psoriatic arthritis synovitis may reveal only minor articular swelling but intense hypervascularity. In dactylitis often both tendons and joints are inflamed. • In suspected infectious, reactive arthritis or crystal arthritis ultrasound helps detect areas of fluid that can be aspirated for further investigation.

International Journal of Rheumatic Diseases 2014; 17: 709–713

• Ultrasound-assisted needle guidance allows injecting or aspirating areas with small amounts of fluid. It is particularly helpful in shoulder joints, subdeltoid bursitis, tenosynovitis and hip joints. It may be done in all anatomical regions. • A clinically suspected diagnosis of gout can be confirmed sonographically, particularly if it is not possible to aspirate fluid for polarization microscopy. Ultrasound can detect smaller urate deposits compared to dual-energy computed tomography.4 Ultrasound is particularly helpful in distinguishing RA or osteoarthritis from gout or chondrocalcinosis. • Fibromyalgia is an important differential diagnosis. It needs to be distinguished from inflammatory disease. Ultrasound allows clear distinguishing of inflamed from non-inflamed joints, tendons and entheses. This is also helpful, particularly in patients with co-existence of an inflammatory rheumatic disease and pain syndrome. • The rheumatologist needs to distinguish traumatic from inflammatory lesions. A patient with an established inflammatory articular disease who is in remission may suddenly experience, for instance, shoulder pain due to a rotator cuff tear or pain of the forefoot due to a march fracture. Ultrasound can delineate tendon and ligament tears. It is equally sensitive for detecting march fractures as magnetic resonance imaging and more sensitive than conventional radiography. • Soft tissue masses may be related to rheumatic diseases such as rheumatic nodules that appear hypoechoic with a clearly delineated margin or gout tophi. Other masses like ganglia that appear anechoic without perfusion, or anechoic or hypoechoic hematomas, may not be directly related to a rheumatic disease. • Ultrasound has shown to be very sensitive and specific in the diagnosis of large-vessel vasculitis such as giant cell arteritis and Takayasu’s arteritis. A typical homogeneous wall swelling is characteristic. Specialized centers have replaced temporal artery biopsy in case typical clinical and ultrasound features of giant cell arteritis are present. The patients are then examined clinically and with ultrasound by an experienced rheumatologist. Ultrasound is also particularly helpful for large extra-cranial arteries in which histology is even more difficult to achieve. Fast-track clinics are increasingly offered by rheumatologists. Physicians may send patients to them with suspected giant cell arteritis within 24 h.15

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• About two-third of patients with Sj€ ogren’s syndrome exhibit irregular submandibular and parotid glands with multiple hypoechoic foci. The submandibular glands often become atrophic with a sagittal diameter of < 8 mm. The parotid glands may become enlarged.16 • In systemic lupus erythematosus, tenosynovitis is more common than in RA. Ultrasound can detect pleural and pericardial effusions as well as pathology in renal involvement. • Antiphospholipid syndrome is characterized by thromboses that need to be differentiated from ruptured Baker’s cysts in acutely swollen legs. • Acute polymyositis may result in muscle edema which appears hyperechoic if the probe is perpendicular to the muscle. However, this sign is unspecific. Local myositis and muscular dystrophy provide more specific ultrasound images. Atrophic muscle appears also hyperechoic. Furthermore, ultrasound can detect muscle calcifications and tears. • In systemic sclerosis the skin thickness can be measured using high-frequency ultrasound probes.17 Echocardiography provides information if pulmonary hypertension is present. In case of lung fibrosis, so-called comet tails appear in the lungs. These are reverberation artefacts showing repetitive hyperechoic echoes below the pleura. This finding is sensitive, but not specific for pulmonary fibrosis. • Raynaud phenomenon nearly always appears in systemic sclerosis, often in other connective tissue diseases and less commonly in vasculitides. After warming up the hands, radial, ulnar, palmar and digital arteries are well visible with ultrasound. In healthy persons and in primary Raynaud’s phenomenon these arteries are well perfused. In secondary Raynaud’s phenomenon due to connective disease, anti-phospholipid syndrome or vasculitis, chronic or even acute occlusions can be detected by ultrasound in these arteries.18 In summary, a wide range of indications have appeared recently for the use of ultrasound in rheumatology. Many national and international ultrasound courses enable rheumatologists to gain knowledge and experience. In an increasing number of countries, ultrasound equipment is available in many rheumatology departments. As an increasing number of rheumatologists have gained experience they can teach other colleagues how to use this valuable technique. If ultrasound equipment and experience is provided by the majority of institutions, an increasing number of

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countries is making ultrasound an essential part of rheumatology training. Wolfgang A. SCHMIDT Immanuel Krankenhaus Berlin, Medical Centre for Rheumatology Berlin-Buch, Berlin, Germany Email: [email protected]

REFERENCES 1 Wakefield RJ, Balint PV, Szkudlarek M et al. (2005) Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 32, 2485–7. 2 Hammer HB, Bolton-King P, Bakkeheim V et al. (2011) Examination of intra and interrater reliability with a new ultrasonographic reference atlas for scoring of synovitis in patients with rheumatoid arthritis. Ann Rheum Dis 70, 1995–8. 3 Xiao H, Liu M, Tan L et al. (2014) Value of ultrasonography for diagnosis of synovitis associated with rheumatoid arthritis. Int J Rheum Dis 17, 773–81. 4 Cheung PP, Kong KO, Chew L-C et al. (2014) Achieving consensus in ultrasonography synovitis scoring in rheumatoid arthritis. Int J Rheum Dis 17, 782–87. 5 Sch€afer VS, Fleck M, Kellner H et al. (2013) Evaluation of the novel ultrasound score for large joints in psoriatic arthritis and ankylosing spondylitis: six month experience in daily clinical practice. BMC Musculoskelet Disord 14, 358. 6 Szkudlarek M, Court-Payen M, Jacobsen S, Klarlund M, Thomsen HS, Østergaard M (2003) Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis. Arthritis Rheum 48, 955–62. 7 Bruyn GA, Hanova P, Iagnocco A et al. (2014) Ultrasound definition of tendon damage in patients with rheumatoid arthritis. Results of a OMERACT consensus-based ultrasound score focussing on the diagnostic reliability. Ann Rheum Dis 73, 1929–34. 8 D’Agostino MA, Schmidt WA (2013) Ultrasoundguided injections in rheumatology: actual knowledge on efficacy and procedures. Best Pract Res Clin Rheumatol 27, 283–94. 9 Terslev L, Naredo E, Iagnocco A et al. (2014) Defining enthesitis in spondyloarthritis by ultrasound: results of a Delphi process and of a reliability reading exercise. Arthritis Care Res (Hoboken) 66, 741–8. 10 Porta F, Damjanov N, Galluccio F et al. (2014) Ultrasound elastography is a reproducible and feasible tool for the evaluation of the patellar tendon in healthy subjects. Int J Rheum Dis 17, 768–72. 11 Azami A, Maleki N, Anari H, Iranparvar Alamdari M, Kalantarhormozi M, Tavosi Z (2014) The diagnostic value of ultrasound compared with nerve conduction velocity in carpal tunnel syndrome. 17, 612–20.

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12 Iagnocco A, Conaghan PG, Aegerter P et al. (2012) The reliability of musculoskeletal ultrasound in the detection of cartilage abnormalities at the metacarpo-phalangeal joints. Osteoarthritis Cartilage 20, 1142–6. 13 Filippucci E, Di Geso L, Girolimetti R, Grassi W (2014) Ultrasound in crystal-related arthritis. Clin Exp Rheumatol 32 (Suppl. 80), S42–7. 14 Huppertz A, Hermann KG, Diekhoff T, Wagner M, Hamm B, Schmidt WA (2014) Systemic staging for urate crystal deposits with dual-energy CT and ultrasound in patients with suspected gout. Rheumatol Int 34, 763–71. 15 Schmidt WA (2014) Role of ultrasound in the understanding and management of vasculitis. Ther Adv Musculoskelet Dis 6, 39–47.

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16 Goules AV, Tzioufas AG (2014) Imaging: diagnostic value of ultrasonography in Sj€ ogren’s syndrome. Nat Rev Rheumatol 10, 450–2. 17 Ch’ng SS, Roddy J, Keen HI (2013) A systematic review of ultrasonography as an outcome measure of skin involvement in systemic sclerosis. Int J Rheum Dis 16, 264–72. 18 Schmidt WA, Krause A, Schicke B, Wernicke D (2008) Color Doppler ultrasonography of hand and finger arteries to differentiate primary from secondary forms of Raynaud’s phenomenon. J Rheumatol 35, 1591–8.

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Ultrasound in rheumatology.

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