Early Rheumatoid Arthritis: AReview of MRI and Sonographic Findings

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1 outry et al. MRI and Sonography of Rheumatoid rthritis Musculoskeletal Imaging Pictorial Essay Nathalie outry 1 Mélanie Morel 1 René-Marc Flipo 2 Xavier Demondion 1,3 nne Cotten 1 outry N, Morel M, Flipo RM, Demondion X, Cotten Keywords: extremities, hand, MRI, musculoskeletal imaging, power Doppler sonography, rheumatoid arthritis, sonography, wrist DOI: /JR Received January 24, 2007; accepted after revision June 19, Department of Musculoskeletal Radiology, Centre Hospitalier Universitaire de Lille and Hôpital Roger Salengro, CHRU de Lille, lvd. du Pr. J Leclercq, Lille, France. ddress correspondence to N. outry (nboutry@chru-lille.fr). 2 Department of Rheumatology, Centre Hospitalier Universitaire de Lille and Hôpital Roger Salengro, Lille, France. 3 Department of natomy, Centre Hospitalier Universitaire de Lille and Hôpital Roger Salengro, Lille, France. JR 2007; 189: X/07/ merican Roentgen Ray Society Early Rheumatoid rthritis: Review of MRI and Sonographic Findings OJECTIVE. The introduction of anti tumor necrosis factor α agents has opened new prospects in therapeutic management of patients with early rheumatoid arthritis, thereby creating new demands on radiologists to identify patients with aggressive disease at an early stage. s a result, imaging techniques such as MRI and sonography have developed during the past few years. CONCLUSION. This article illustrates the imaging findings that may be encountered with these techniques in patients with early rheumatoid arthritis. heumatoid arthritis is characterized R by proliferative, hypervascularized synovitis, resulting in bone erosion, cartilage damage, joint destruction, and long-term disability. Diagnosis is based on clinical, laboratory, and radiographic findings. Conventional radiography has been the mainstay for diagnosis of joint damage and subsequent follow-up. Radiography can provide only indirect information on synovial inflammation, however, and the technique is insensitive to early bone damage. Until recently, the absence of effective treatment to prevent joint destruction has limited the need for more sensitive imaging techniques. This situation changed after the development of new therapeutics for rheumatoid arthritis, such as the anti tumor necrosis factor (TNF) α agents. vailability of these powerful and expensive drugs has created new demands on radiologists to identify patients with aggressive rheumatoid arthritis at an early stage to affect the therapeutic management of these patients. MRI and sonography can be useful tools in evaluating patients with early rheumatoid arthritis. oth imaging techniques can detect preerosive synovitis. They can also identify early bone damage before it becomes apparent on radiography. Furthermore, MRI can be used to predict future bone damage. ecause MRI and sonography are rapidly becoming imaging techniques for the evaluation of patients with early rheumatoid arthritis, the purpose of this article is to illustrate how these techniques can be used in diagnosing early stage rheumatoid arthritis, monitoring disease activity, and differentiating early rheumatoid arthritis from other inflammatory arthritides in some patients. Positive Diagnosis of Early Rheumatoid rthritis The wrist and the metacarpophalangeal (MCP) and metatarsophalangeal (MTP) joints are among the first areas to be affected in rheumatoid arthritis. The most symptomatic extremity, the dominant extremity, or both may be studied with MRI and sonography. bnormalities in early rheumatoid arthritis include synovitis, tenosynovitis, bone erosions, bone marrow edema, and bursitis. Synovitis Proliferative synovitis (i.e., rheumatoid pannus) is the earliest pathologic abnormality in rheumatoid arthritis, and it is secondarily responsible for bone and cartilage damage. It is usually, but not exclusively, bilateral. MRI reveals proliferative synovitis as thickening of the synovial membrane that appears as quick enhancement after the administration of gadolinium [1]. This is well shown on fat-suppressed gadolinium-enhanced T1-weighted images (Fig. 1). Sonography shows abnormal hypoechoic (relative to subdermal fat) intraarticular tissue that is poorly compressible and that exhibits Doppler signal with color or power Doppler imaging [2] (Fig. 2). small amount of fluid may be associated with synovitis. This fluid shows high signal intensity on T2-weighted MR images and low signal intensity on fat-suppressed gadoliniumenhanced T1-weighted MR images. The fluid appears anechoic on sonography, with no evidence of flow on Doppler imaging, and can be expelled from the region by compression with the sonographic transducer. oth MRI and 1502 JR:189, December 2007

2 MRI and Sonography of Rheumatoid rthritis sonography are more sensitive than clinical assessment for detecting synovial inflammation [3], and they help distinguish between patients with polyarthritis and those with oligoarthritis. Conventional radiography, on the other hand, is not helpful in the diagnosis of synovitis unless there is fusiform soft-tissue swelling at the joints. This swelling is well seen at the proximal interphalangeal joints and, to a lesser extent, at the MCP joints. Tenosynovitis Tenosynovitis is a common finding in patients with early rheumatoid arthritis. lthough any tendon may be affected, the flexor digitorum, extensor digitorum, and extensor carpi ulnaris are frequently involved [4]. Tenosynovitis is usually, but not exclusively, bilateral. MRI reveals thickening of the synovial sheath with marked enhancement on fat-suppressed gadolinium-enhanced T1-weighted images [4] (Fig. 3). Sonography shows similar findings: hypoechoic thickening of the synovial sheath with hyperemia on Doppler imaging [2] (Fig. 3). small amount of fluid may be associated with tenosynovitis. In some patients with early rheumatoid arthritis, affected tendons may appear heterogeneous (suggesting incipient tendinitis) on both imaging techniques. These tendinous changes are seen best on sonography (Fig. 3). oth MRI and sonography outperform conventional radiography in detecting tenosynovitis. one Erosions one erosions result from proliferative synovitis. They are less frequently bilateral than synovitis or tenosynovitis. The capitate, triquetrum, and lunate bones (Fig. 4); the radial aspect of the second and third metacarpal bones (Fig. 4); and the lateral aspect of the fifth metatarsal bone (Fig. 4C) are more frequently involved with bone erosions [4, 5]. On MRI, bone erosions appear as sharply marginated areas of trabecular bone loss with a cortical defect [1], often associated with synovitis. These erosions are well seen after IV gadolinium injection, especially with thin-partition 3D gradient-echo sequences [4] (Fig. 4). On sonography, bone erosions are seen as intraarticular discontinuities of the bone surface that are visible in two perpendicular planes [2]. They are best detected at the ulnar styloid process (Fig. 5), the radial aspect of the second MCP joint, the ulnar aspect of the fifth MCP joint, and the lateral aspect of the fifth MTP joint [4] (Fig. 5). High signal on Doppler imaging suggests the presence of proliferative, hypervascularized pannus tissue in the erosion [2] (Fig. 5C). Compared with MRI, however, sonography is limited in the evaluation of the other MCP and MTP joints because of limitations of probe positioning, even with a hockey stick transducer and the carpal bones. MRI is more sensitive than conventional radiography for diagnosing bone erosions [6]. The same is true of sonography for the MCP and MTP joints [7, 8]. one Marrow Edema one marrow edema may precede the development of bone erosions and can be used to predict medium-term functional disability [9]. It is detectable with STIR T2-weighted or fat-suppressed T2-weighted MRI sequences (Fig. 6). one marrow edema appears as a lesion with ill-defined margins and high signal intensity [1], typically located at the insertion of the synovial membrane. It can occur alone, or it may surround bone erosions [1]. In contrast to MRI, sonography provides no information on bone marrow edema. ursitis ursitis is a common finding in patients with early rheumatoid arthritis and may be asymptomatic. It is located between or beneath the metatarsal heads [4]. Intermetatarsal and submetatarsal bursitis show significant enhancement on MRI after IV gadolinium injection due to inflammation (Fig. 7). On sonography, intermetatarsal and submetatarsal bursitis appear as heterogeneous (hypo- and hyperechoic) collections that can be well- or ill-defined (Fig. 8). Significant hyperemia of the synovial lining is usually seen on Doppler sonography (Fig. 8). Intermetatarsal bursitis is more frequent in the second and third web spaces [4], where it may be difficult to differentiate from Morton s neuroma. However, location at the plantar aspect of the foot on MRI and identification of the entering and exiting nerve on sonography are more suggestive of interdigital nerve entrapment. Disease ctivity and Damage Monitoring MRI and sonography are both useful in assessing early rheumatoid arthritis activity. Modern drug therapies have reportedly decreased synovial proliferation and bone marrow edema and prevented the development of bone erosions. MRI and sonography can both quantify synovial inflammation. Treatment response can be identified on MRI as a reduction in synovial volume and a decrease in the rate of synovial enhancement [10, 11] (Fig. 9). Similarly, sonography shows a decrease in synovial thickness and disappearance of the Doppler signal in patients who respond to treatment [12]. Microbubble sonographic contrast agents may also improve the detection of synovial vascularization, which is a marker of disease activity [13], but they are not widely used in daily practice. More recently, methods of semiquantitative scoring of early rheumatoid arthritis changes (i.e., synovitis, bone erosions, and bone edema) at the wrist and MCP joints have been developed and standardized on MRI by the OMERCT (Outcome Measures in Rheumatology Clinical Trials) [1] and EULR (European League gainst Rheumatism) [1] groups. These scoring systems may also be useful in assessing rheumatoid arthritis activity and bone damage. Differential Diagnosis Diagnosis of early rheumatoid arthritis is often based primarily on inflammatory polyarthralgia of the hands. Clinicians sometimes struggle to differentiate early rheumatoid arthritis from psoriatic arthritis or systemic lupus erythematosus, especially when conventional radiography shows no abnormality. In patients with psoriatic arthritis, MRI may show extensive signal intensity changes in the bone marrow on STIR T2-weighted, fat-suppressed T2-weighted, or fat-suppressed gadolinium-enhanced T1-weighted sequences [14]. These changes may sometimes be seen in the soft tissues as well [14]. one marrow changes due to psoriatic arthritis do not remain localized in the joint capsule (in contrast to those due to early rheumatoid arthritis) and can extend far beyond the joint capsule, probably related to inflammatory enthesitis (Fig. 10). Sonography cannot detect bone marrow changes, but it may exhibit signs of peripheral enthesitis affecting the lower limbs (especially the chilles tendon and the plantar fascia) (Fig. 10) and, in some cases, the fingers (Fig. 10C). Enthesitis appears as a hypoechoic thickening of the enthesis, associated with hyperemia on Doppler imaging (Fig. 10C). In patients with systemic lupus erythematosus, MRI may show abnormalities similar to those of patients with early rheumatoid arthritis (e.g., synovitis, tenosynovitis, and bone erosions), and it might be impossible to differentiate patients with early rheumatoid arthritis from those with systemic lupus erythematosus on MRI [15] (Fig. 11). JR:189, December

3 outry et al. Conclusion MRI and sonography have opened new horizons in the detection of early joint damage, assessment of synovial inflammation, and therapeutic management of patients with rheumatoid arthritis. Radiologists should be familiar with the MRI and sonographic appearances of early rheumatoid arthritis in the small synovial joints of the appendicular skeleton. It is still too early to indicate with certainty the role of imaging in treatment decisions. No strategy has yet been proposed in the literature. However, sonography is a quick and inexpensive way to detect synovitis, whereas MRI allows a more global approach to the small synovial joints of the appendicular skeleton. References 1. Ostergaard M, Peterfy C, Conaghan P, et al. OMER- CT Rheumatoid rthritis Magnetic Resonance Imaging Studies. Core set of MRI acquisitions, joint pathology definitions, and the OMERCT R-MRI scoring system. J Rheumatol 2003; 30: [Erratum in J Rheumatol 2004; 31:198] 2. Wakefield RJ, alint PV, Szkudlarek M, et al. Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 2005; 32: ackhaus M, Kamradt T, Sandrock D, et al. rthritis of the finger joints: a comprehensive approach comparing conventional radiography, scintigraphy, ultrasound, and contrast-enhanced magnetic resonance imaging. rthritis Rheum 1999; 42: outry N, Larde, Lapegue F, Solau-Gervais E, Flipo RM, Cotten. Magnetic resonance imaging appearance of the hands and feet in patients with early rheumatoid arthritis. J Rheumatol 2003; 30: McQueen FM, Stewart N, Crabbe J, et al. Magnetic resonance imaging of the wrist in early rheumatoid arthritis reveals a high prevalence of erosion at four months after symptom onset. nn Rheum Dis 1998; 57: Foley-Nolan D, Stack JP, Ryan M, et al. Magnetic resonance imaging in the assessment of rheumatoid arthritis: a comparison with plain film radiographs. r J Rheumatol 1991; 30: Wakefield RJ, Gibbon WW, Conaghan PG, et al. The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: a comparison with conventional radiography. rthritis Rheum 2000; 43: Szkudlarek M, Narvestad E, Klarlund M, et al. Ultrasonography of the metatarsophalangeal joints in rheumatoid arthritis: comparison with magnetic resonance imaging, conventional radiography, and clinical examination. rthritis Rheum 2004; 50: enton N, Stewart N, Crabbe J, et al. MRI of the wrist in early rheumatoid arthritis can be used to predict functional outcome at 6 years. nn Rheum Dis 2004; 63: Jevtic V, Watt I, Rozman, et al. Contrast-enhanced Gd-DTP magnetic resonance imaging in the evaluation of rheumatoid arthritis during a clinical trial with DMRDs: a prospective two-year follow-up study on hand joints in 31 patients. Clin Exp Rheumatol 1997; 15: Ostergaard M, Hansen M, Stoltenberg M, et al. Magnetic resonance imaging determined synovial membrane volume as a marker of disease activity and a predictor of progressive joint destruction in the wrists of patients with rheumatoid arthritis. rthritis Rheum 1999; 42: Ribbens C, ndre, Marcelis S, et al. Rheumatoid hand joint synovitis: gray-scale and power Doppler US quantifications following anti-tumor necrosis factor-alpha treatment: pilot study. Radiology 2003; 229: Klauser, Frauscher F, Schirmer M, et al. The value of contrast-enhanced color Doppler ultrasound in the detection of vascularization of finger joints in patients with rheumatoid arthritis. rthritis Rheum 2002; 46: Jevtic V, Watt I, Rozman, et al. Distinctive radiological features of small hand joints in rheumatoid arthritis and seronegative spondyloarthritis demonstrated by contrast-enhanced (Gd- DTP) magnetic resonance imaging. Skeletal Radiol 1995; 24: outry N, Hachulla E, Flipo RM, Cortet, Cotten. MR imaging findings in hands in early rheumatoid arthritis: comparison with those in systemic lupus erythematosus and primary Sjögren syndrome. Radiology 2005; 236: Fig year-old woman with early rheumatoid arthritis and synovitis. and, Transverse fat-suppressed gadolinium-enhanced T1-weighted spin-echo MR images show bilateral synovitis (arrows) in wrist () and metatarsophalangeal joints (). Note also bone marrow signal intensity changes (asterisks, ), which precede frank bone erosions, and flexor digitorum tenosynovitis (arrowhead, ) JR:189, December 2007

4 MRI and Sonography of Rheumatoid rthritis Fig year-old man with early rheumatoid arthritis and synovitis. Dorsal longitudinal color sonogram of wrist reveals hypoechoic distention of both radiocarpal (single asterisk) and midcarpal (double asterisks) synovial recesses. High signal in synovium on power Doppler imaging indicates hyperemia. R = radius, L = lunate, C = capitate. Fig year-old woman with early rheumatoid arthritis and tenosynovitis. R = radius, U = ulna, t = tendon., Transverse fat-suppressed gadolinium-enhanced T1-weighted spin-echo MR image shows significant enhancement (arrows) around extensor carpi ulnaris tendon that represents tenosynovitis. Note also mild enhancement in distal radioulnar joint, which is suggestive of synovitis., Dorsal transverse sonogram of wrist shows hypoechoic thickening (asterisks) and hyperemia around extensor carpi ulnaris tendon on power Doppler imaging, representing tenosynovitis. Note also heterogeneous appearance of tendon on sonography. JR:189, December

5 outry et al. C Fig year-old woman with early rheumatoid arthritis and bone erosions., Transverse fat-suppressed gadolinium-enhanced 3D gradient-echo MR image reveals carpal bone erosions (capitate, triquetrum, pisiform) (arrows). Synovitis in carpal joints and flexor and extensor tenosynovitis are also evident. (Reprinted with permission from outry N, Larde, Lapegue F, Solau-Gervais E, Flipo RM, Cotten. Magnetic resonance imaging appearance of the hands and feet in patients with early rheumatoid arthritis. J Rheumatol 2003; 30: [4]), Transverse fat-suppressed gadolinium-enhanced 3D gradient-echo MR image shows bone erosion on radial aspect of third metacarpal bone (arrowhead). Note also presence of significant bilateral synovitis in second and third metacarpophalangeal joints and flexor digitorum tenosynovitis (arrows). C, Transverse fat-suppressed gadolinium-enhanced 3D gradient-echo MR image exhibits bone erosion on lateral aspect of fifth metatarsal bone (arrowhead), which is associated with synovitis. Note also presence of inflammatory bursitis beneath fifth metatarsal bone (asterisk). (Reprinted with permission from outry N, Larde, Lapegue F, Solau-Gervais E, Flipo RM, Cotten. Magnetic resonance imaging appearance of the hands and feet in patients with early rheumatoid arthritis. J Rheumatol 2003; 30: [4]) 1506 JR:189, December 2007

6 MRI and Sonography of Rheumatoid rthritis Fig year-old woman with rheumatoid arthritis and bone erosions., Transverse sonogram of wrist exhibits bone erosion of ulnar styloid process (arrow). Latter is related to hypoechoic thickening around extensor carpi ulnaris tendon, representing tenosynovitis (asterisks). U = ulna, t = tendon., Coronal sonogram of forefoot shows bone erosion (arrow) on lateral aspect of fifth metatarsal bone (M5) associated with synovitis (asterisks). C, Coronal sonogram of hand shows hypervascular pannus filling bone erosion (arrows) on radial aspect of second metacarpal bone (M2) on power Doppler imaging. Note also hyperemia in articular space. C JR:189, December

7 outry et al. Fig year-old man with early rheumatoid arthritis and bone marrow edema. Coronal STIR T2-weighted MR image reveals bone marrow edema in second metacarpal bone (asterisk). Note also fluid in articular space. Fig year-old man with early rheumatoid arthritis and bursitis. Longitudinal sonogram of web space reveals intermetatarsal bursitis (asterisks) as well-defined heterogeneous collection with synovial hyperemia on power Doppler imaging. (Courtesy of Morvan G, Paris, France) Fig year-old man with early rheumatoid arthritis and bursitis. Transverse fatsuppressed gadolinium-enhanced 3D gradient-echo MR image shows submetatarsal (asterisk) and intermetatarsal (boxes) bursitis. Note also presence of bone erosion (arrow) associated with synovitis in third metatarsophalangeal joint. Signal Intensity of Synovium S max S 3 S 2 S 1 0 t 0 t 1 t 2 Fig. 9 Monitoring early rheumatoid arthritis activity. Schematic of quantitative evaluation of rate of synovial enhancement before (solid line) and after (dotted line) effective treatment. Data were derived from contrast-enhanced dynamic MRI scans. Synovial enhancement is defined as SI t SI 0 / Δ t, where SI t is signal intensity obtained t seconds after contrast injection, SI 0 is signal intensity obtained in first unenhanced image, and Δ t is time taken to reach peak enhancement over initial linear phase (dotted area). fter treatment, synovitis and therefore synovial enhancement are reduced. t 3 Time (s) t 4 t 5 t JR:189, December 2007

8 MRI and Sonography of Rheumatoid rthritis Fig year-old man with psoriatic arthritis., Coronal fat-suppressed T2-weighted MR image shows edematous signal intensity changes (asterisks) in bone marrow of first phalanx. Note also similar findings along collateral ligaments (arrows) of adjacent proximal interphalangeal joint., Longitudinal sonogram of foot using extended field of view reveals enthesitis of plantar fascia. Note significant hypoechoic thickening of fascia origin (double arrow); also note bone erosions and spurs (arrowheads). More distally, plantar fascia shows normal sonographic appearance (arrows). C = calcaneus. C, Coronal color sonogram of hand shows enthesitis of radial collateral ligament as hypoechoic thickening of ligament with mild hyperemia on power Doppler imaging. For comparison, note normal fibrillar hyperechoic appearance of radial collateral ligament on normal side (arrows). P1 = proximal phalanx, P2 = middle phalanx. C Fig year-old woman with systemic lupus erythematosus. Transverse fatsuppressed gadolinium-enhanced T1-weighted spin-echo MR image shows bilateral synovitis in metacarpophalangeal joints and tenosynovitis (arrows) in flexor and extensor digitorum, as well as bone erosion on radial aspect of second metacarpal bone (arrowhead). MRI findings are similar to those of early rheumatoid arthritis. JR:189, December