MRI of the Sacroiliac Joints in Patients with Moderate to Severe Ankylosing Spondylitis

MRI of Sacroiliac Joints in Patients with nkylosing Spondylitis Musculoskeletal Imaging Original Research M E D E N T U R I L I M G I N G JR 2006; 187:1420 1426 0361 803X/06/1876 1420 merican Roentgen Ray Society Y O Miriam. Bredella 1,2 Lynne S. Steinbach 1 Stephanie Morgan 3 Michael Ward 4 John. Davis 3 F Bredella M, Steinbach LS, Morgan S, Ward M, Davis J Keywords: ankylosing spondylitis, bone, joint, MRI, musculoskeletal imaging, sacroiliac joints, sacroiliitis DOI:10.2214/JR.05.1423 Received ugust 15, 2005; accepted after revision October 21, 2005. 1 Department of Radiology, University of alifornia, San Francisco, San Francisco,. 2 Present address: Department of Radiology, Massachusetts General Hospital, 55 Fruit St., Yawkey Bldg., 6400 (6E), Boston, M 02114. ddress correspondence to M.. Bredella (mbredella@partners.org). 3 Department of Internal Medicine, Division of Rheumatology, University of alifornia, San Francisco, San Francisco,. 4 National Institute of rthritis and Musculoskeletal Skin Diseases, National Institutes of Health, Bethesda, MD. MRI of the Sacroiliac Joints in Patients with Moderate to Severe nkylosing Spondylitis OBJETIVE. The objectives of our study were to evaluate whether MRI findings of the sacroiliac joints are able to distinguish between active and inactive disease in patients with established ankylosing spondylitis and to determine whether these findings correlate with markers of clinical activity, disease duration, severity, and degree of radiographic damage. MTERILS ND METHODS. Eighteen patients with symptomatic moderate to severe ankylosing spondylitis were evaluated. MRI of the sacroiliac joint (1.5 T) was performed using fat-saturated T2-weighted, T1-weighted, STIR, and fat-saturated contrast-enhanced T1- weighted sequences. The sacroiliac joints were evaluated by two radiologists for enhancement, subchondral bone marrow edema, erosions, and subchondral fatty marrow infiltration. Findings on MRI were analyzed for correlation with multiple clinical characteristics and measures of disease activity, including radiographic scoring. RESULTS. In 17 patients, MRI showed abnormal findings of the sacroiliac joint. Ten patients showed active disease on MRI as measured by abnormal enhancement and subchondral bone marrow edema. Disease activity detected using MRI correlated in a positive fashion with only -reactive protein (RP) level. There was no correlation with the other measures of disease activity or with disease duration. In 14 patients, fatty subchondral bone marrow was detected on MRI. These changes were seen in patients with active and chronic disease and correlated with higher radiographic scores but not with disease duration or markers of disease activity. ONLUSION. ontrast-enhanced MRI of the sacroiliac joint is sensitive in depicting sacroiliitis in patients with established ankylosing spondylitis. Subchondral edema and enhancement correlate with high RP levels. Subchondral fatty bone marrow changes were seen in both active and chronic sacroiliitis and are correlated with higher radiographic scores; these changes may be a marker of more advanced disease. nvolvement of the sacroiliac joints I is a hallmark of ankylosing spondylitis [1 4]. The definite diagnosis of ankylosing spondylitis requires radiographic evidence of sacroiliitis, which is defined as erosions, subchondral sclerosis, and irregular joint spaces, and clinical features, including inflammatory back pain [1]. onventional radiographs remain the most widely accepted and available screening method for ankylosing spondylitis; however, radiographs often show normal findings during the early stages of the disease, and several years may be required for sacroiliitis to become apparent on radiography [3 6]. MRI of the sacroiliac joints has been shown to be superior to radiography in depicting sacroiliitis, and gadolinium-enhanced MRI has been shown to be useful in the early detection of active sacroiliitis [7, 8]. New treatment options for patients with ankylosing spondylitis require sensitive imaging techniques to not only help diagnose ankylosing spondylitis early, but also determine disease activity and the degree of damage present at diagnosis [9 11]. The purposes of our study were to evaluate MRI of the sacroiliac joint in patients with moderate to severe ankylosing spondylitis and to determine whether MRI findings of enhancement, edema, and fatty marrow changes were correlated with clinical features and measures of disease activity. Materials and Methods Over a 1-year period, MR images and radiographs of the sacroiliac joints of 18 patients with ankylosing spondylitis who had been recruited for two clinical trials were evaluated. Patients had moderate to severe disease activity as defined by the Bath nkylosing Spondylitis Disease ctivity Index (BSDI) score 1420 JR:187, December 2006

MRI of Sacroiliac Joints in Patients with nkylosing Spondylitis TBLE 1: Patient Population haracteristic Value Duration of disease (y) 14 (5, 20) HL B-27 positive, no. (%) of patients 17 (94.4) BSFI score 25.7 (22.5, 63.5) BSDI score 60.2 (44.8, 65.8) Global score Patient 72.3 (40.0, 80.0) Physician 55.5 (48.0, 65.0) Inflammatory back pain score 62.2 (50.5, 93.5) Nocturnal back pain score 71.0 (51.0, 82.5) Total back pain score 71.0 (47.0, 78.0) Erythrocyte sedimentation rate (mm/h) 11 (6, 26) -reactive protein value (mg/l) 1.125 (0.5, 7.3) High -reactive protein value, a no. (%) of patients) 9 (50) BSRI score, no. (%) of patients 2 2 (11.1) 3 8 (44.4) 4 8 (44.4) Subchondral bone marrow edema score, no. (%) of patients 0 8 (44.4) 1 9 (50) 2 1 (5.6) Enhancement score, no. (%) of patients 0 8 (44.4) 1 6 (33.3) 2 3 (16.7) 3 1 (5.6) Fatty subchondral bone marrow change score, no. (%) of patients 0 2 (11.1) 1 6 (33.3) 2 7 (38.9) 3 3 (16.7) Note Unless indicated otherwise, data are medians (25%, 75%). HL = human leukocyte antigen, BSFI = Bath nkylosing Spondylitis Functional Index, BSDI = Bath nkylosing Spondylitis Disease ctivity Index, BSRI = Bath nkylosing Spondylitis Radiology Index. a Normal, < 6 mg/l. of > 40 (range, 0 100) and physician visual analog scale (VS) global score of > 40 (range, 0 100). nother criterion for inclusion in our study was that patients had symptomatic inflammatory lower back pain. Definite ankylosing spondylitis was diagnosed using the modified New York criteria [1]. Radiography Oblique and anteroposterior radiographs of both sacroiliac joints were available for all patients. Radiographs were graded according to the Bath nkylosing Spondylitis Radiology Index (BSRI). Each sacroiliac joint was evaluated retrospectively by two radiologists in consensus who were blinded to laboratory results and clinical status. The sacroiliac joints were evaluated for blurring of joint margins, sclerosis, erosions, and total ankylosis. BSRI score was then assigned for each patient. MRI ll patients underwent MRI of the sacroiliac joints with and without administration of IV gadolinium. MRI (1.5 T; Signa, GE Healthcare) was performed using oblique coronal (parallel to the long axis of the sacrum) and axial fast spin-echo (FSE) T1-weighted sequences (TR/TE, 600/minimum); and STIR (4,000/60), fat-saturated FSE T2-weighted (4,000/50), and fat-saturated contrast-enhanced FSE T1-weighted (600/minimum) sequences. The fat-saturated contrastenhanced T1-weighted images were obtained after IV administration of 0.1 mmol/kg of body weight of gadopentetate dimeglumine. The field of view was 20 cm; slice thickness, 4 mm; and number of excitations, 2. The imaging times were 7 minutes for the STIR sequences, 4 minutes for the fat-saturated FSE T2- weighted sequences, 6 minutes for the FSE T1- weighted sequences, and 6 minutes for the fat-saturated contrast-enhanced FSE T1-weighted sequences. The sacroiliac joints were retrospectively analyzed by the same two radiologists in consensus who were blinded to laboratory results and clinical status. MR images were evaluated at a different time point than the radiographs, and the results of the radiographs were not available at the time of MR interpretation. The sacroiliac joints were evaluated for signal characteristics involving the joint space, surrounding bone, and bone marrow adjacent to the joint on each imaging sequence. Enhancement, subchondral bone marrow edema, cartilage abnormalities, periarticular erosions, subchondral fatty marrow infiltration, and ankylosis were recorded. hronic disease was defined as changes that were low signal on T1- and T2- weighted images, subchondral sclerosis, narrowing of the joint spaces, bone bridging, and ankylosis. Erosions that were high signal on STIR or T2- weighted images, subchondral edema, and enhancement within or adjacent to the sacroiliac joint were considered markers for active inflammatory disease. Findings on MRI of the sacroiliac joint were graded as 1 (mild), 2 (moderate), or 3 (severe). n MRI score was obtained for each patient. MRI was performed within 12 weeks of radiography. nalysis Findings on MRI and radiography were analyzed for correlation with clinical inflammatory markers: -reactive protein (RP), erythrocyte sedimentation rate (ESR), BSDI, Bath nkylosing Spondylitis Functional Index (BSFI), back pain scores (total back pain, nocturnal back pain, inflammatory back pain, and physician and patient global scores), disease duration, and BSRI scores. Laboratory markers were obtained within 1 week of MRI. The ESR (Westergren sedimentation rate test) and RP level were measured using conventional laboratory technology, with normal values being < 10 mm/h and < 6 mg/l, respectively. The Wilcoxon s rank sum test and Jonckheere- Terpstra test were used to compare associations between different radiographic measures. The Jonckheere-Terpstra test is a nonparametric test that accounts for the ordered nature of the radiographic grading categories. Large values of Z on the Jonckheere-Terpstra test indicate an important association between measures. JR:187, December 2006 1421

Results Multiple demographic and disease activity measures are listed in Table 1. The patient population included 14 men and four women with a mean age of 37 years. The mean disease duration was 14 years (range, 2 39 years). Findings for human leukocyte antigen (HL) B-27 were positive in 94.4% of the patients. s expected by the inclusion criterion of definite ankylosing spondylitis by the modified New York criteria, conventional radiographs showed involvement of the sacroiliac joint in all 18 patients. Unilateral involvement was seen in one patient and bilateral involvement was detected in 17 patients. Seven patients were shown to have complete ankylosis of the sacroiliac joint. Moderate findings, corresponding to a BSRI score of 3, were seen in eight patients. One patient had minimal changes of the sacroiliac joint (BSRI score of 2). ll 18 patients except one had abnormal MRI findings of the sacroiliac joint: 16 patients had bilateral involvement and one patient had unilateral involvement. Ten patients showed abnormal enhancement and subchondral bone marrow edema, suggestive of active disease (Figs. 1 and 2). These findings were bilateral in all patients. Seven patients were shown to have ankylosis and subchondral sclerosis of the sacroiliac joint. Two of these Fig. 1 28-year-old man with ankylosing spondylitis for 10 years. Laboratory results and clinical findings were as follows: -reactive protein, 7.3 mg/l; erythrocyte sedimentation rate, 5 mm/h; Bath nkylosing Spondylitis Functional Index (BSFI), 80.0; Bath nkylosing Spondylitis Disease ctivity Index (BSDI), 60.2; inflammatory back pain score, 94; nocturnal back pain score, 83; total back pain score, 82., Radiographs show indistinct sacroiliac joint with erosions. B, oronal T1-weighted MR image shows subchondral fatty marrow changes (arrows). There is irregularity of sacroiliac joint., oronal fat-saturated contrast-enhanced T1-weighted image shows small foci of enhancement at inferior sacroiliac joint (arrows). (Fig. 1 continues on next page) patients with ankylosis showed edema and enhancement on MRI, indicating active disease (Fig. 3). In 16 patients, fatty subchondral bone marrow was seen. These changes were seen in patients with MRI findings suggestive of active disease and in those with MRI findings suggestive of chronic disease. In all patients with MRI findings of enhancement, bone marrow edema was seen on STIR and fat-saturated FSE T2-weighted images. No difference in the severity of edema was detected on STIR images and fatsaturated FSE T2-weighted images; however, edema was slightly better seen on the STIR images than the fat-saturated FSE T2-weighted B 1422 JR:187, December 2006

MRI of Sacroiliac Joints in Patients with nkylosing Spondylitis images (Fig. 1). Four of 10 patients with active disease on MRI showed more extensive enhancement on fat-saturated T1-weighted images compared with the edematous changes seen on STIR or fat-saturated FSE T2-weighted images (Figs. 2 and 3). MRI findings of disease activity correlated only with RP value (Table 2). There was no correlation between MRI findings and ESR, BSRI, BSDI, BSFI, back pain scores, or disease duration. Subchondral fatty changes on MRI correlated with BSRI score but were inversely related to enhancement (Table 3). MRI findings of fatty subchondral bone marrow did not correlate with disease duration or clinical inflammatory markers. Radiographic findings did not correlate with clinical or laboratory markers of disease activity or of disease duration. D Fig. 1 (continued) 28-year-old man with ankylosing spondylitis for 10 years. Laboratory results and clinical findings were as follows: -reactive protein, 7.3 mg/l; erythrocyte sedimentation rate, 5 mm/h; Bath nkylosing Spondylitis Functional Index (BSFI), 80.0; Bath nkylosing Spondylitis Disease ctivity Index (BSDI), 60.2; inflammatory back pain score, 94; nocturnal back pain score, 83; total back pain score, 82. D, oronal STIR image shows focal T2 prolongation at inferior sacroiliac joint (arrows). E, Edema (arrows) is not well visualized on coronal fat-saturated T2-weighted image. Discussion Given the development of new promising treatment options for ankylosing spondylitis, such as tumor necrosis factor alpha, it is important to diagnose ankylosing spondylitis early, detect active sacroiliitis and differentiate it from chronic changes, and monitor for potential changes after therapy [10, 12]. In addition, studies have shown a lack of correlation between clinical signs of disease activity and conventional laboratory markers of disease activity such as RP levels and ESR [13]. Imaging findings play an important role in the diagnosis of sacroiliitis in patients with ankylosing spondylitis, and MRI of the sacroiliac joint has been shown to be able to reveal the anatomy and degree of inflammation without the use of ionizing radiation [6]. lso, MRI has been found to be more sensitive than radiography for detecting sacroiliitis in patients with ankylosing spondylitis, especially in the evaluation of early disease [7, 8, 14 16]. The purpose of our study was to focus on the use of MRI in evaluating disease activity in patients with moderate to severe ankylosing spondylitis and whether it is possible to show active disease in patients with established ankylosing spondylitis. In this select group of patients with moderate to severe ankylosing spondylitis recruited for clinical trials, MRI of the sacroiliac joint was sensitive in depicting sacroiliitis. MRI allowed lesions with higher water content due to inflammatory edema to be differentiated from lesions with reduced water content due to fibrotic tissue or sclerosis. MRI was also able to show inflammatory changes in advanced stages of ankylosing spondylitis, even in patients with ankylosis of the sacroiliac joint. This finding suggests that fusion does not necessarily signal the absence of associated inflammatory activity at the sacroiliac joint and that patients with sacroiliitis need to be treated in the later disease stages. When evaluating the effects of disease-modifying drugs, it may be valuable to follow these different lesions because they may be, in part, reversible. Fat-saturated T2-weighted and STIR sequences were slightly less sensitive than contrast-enhanced T1-weighted sequences for detecting the extent of acute inflammatory changes. lthough all patients with edematous changes on STIR and fat-saturated FSE T2- weighted images also showed abnormal enhancement, we saw more enhancing lesions on the fat-saturated contrast-enhanced T1- weighted images, supporting the use of IV contrast material. The oblique coronal plane was the most useful plane for detecting changes associated with ankylosing spondylitis. MRI findings of disease activity correlated only with RP value. There was no correlation between MRI findings and ESR, BSRI, BSDI, BSFI, back pain scores, or disease duration. These findings are in contrast to the results of a study performed by Jee et al. [2] who found significant correlation with synovial enhancement and ESR value and with the sum of ESR and RP values but not with the RP value alone. E JR:187, December 2006 1423

The observation that some patients had periarticular fat accumulation in the bone marrow has no apparent pathophysiologic explanation. However, this finding seems to reflect a later stage of disease because it was associated with more severe involvement of the sacroiliac joints (ankylosis), as determined using the BSRI score, and was inversely related to enhancement. This suggests a temporal change Fig. 2 34-year-old woman with ankylosing spondylitis for 21 years. Laboratory results and clinical findings were as follows: -reactive protein, 6 mg/l; erythrocyte sedimentation rate, 7 mm/h; Bath nkylosing Spondylitis Functional Index (BSFI), 77.3; Bath nkylosing Spondylitis Disease ctivity Index (BSDI), 75.2; inflammatory back pain score, 100; nocturnal back pain score, 24; total back pain score, 47., Radiograph shows suspicious changes of sacroiliac joint. B, oronal T1-weighted MR image shows normal findings., oronal fat-saturated contrast-enhanced T1-weighted image shows moderate enhancement (arrows). D, oronal STIR image shows mild bilateral inferior edema of sacroiliac joint (arrows). from enhancement to fat as sacroiliac fusion progresses. The observed fat accumulation supports the concept that the disease process in sacroiliitis involves subchondral areas and may be due to an ongoing effect of inflammatory products on local fat metabolism [17, 18]. Our study had several limitations. First is the relatively small number of patients and the retrospective nature of the study. Second is the absence of pathologic tissue confirmation of disease activity. lso, reviewers evaluated the MR examinations and radiographs without knowledge of the laboratory data; however, the reviewers were aware that the patients had been diagnosed with ankylosing spondylitis. In conclusion, contrast-enhanced MRI of the sacroiliac joint is able to depict sacroiliitis in patients with moderate to severe ankylosing B D 1424 JR:187, December 2006

MRI of Sacroiliac Joints in Patients with nkylosing Spondylitis B Fig. 3 43-year-old man with ankylosing spondylitis for 20 years. Laboratory results and clinical findings were as follows: -reactive protein, 17.5 mg/l; erythrocyte sedimentation rate, 34 mm/h; Bath nkylosing Spondylitis Functional Index (BSFI), 42.8; Bath nkylosing Spondylitis Disease ctivity Index (BSDI), 41.8; inflammatory back pain score, 41.5; nocturnal back pain score, 62; total back pain score, 63., Radiograph shows fusion of sacroiliac joint. B, xial T1-weighted MR image shows sclerosis and fusion of sacroiliac joint (arrows)., oronal T1-weighted MR image shows sclerosis and fusion of sacroiliac joint (arrows). D, oronal fat-saturated contrast-enhanced T1-weighted image shows bilateral enhancement of sacroiliac joint (arrows). E, oronal STIR image shows mild subchondral edema (arrows). D E JR:187, December 2006 1425

TBLE 2: ssociation of Disease ctivity Determined Using MRI riteria and linical or Laboratory riteria Laboratory or linical riterion spondylitis. MRI findings suggestive of active disease, such as subchondral edema and enhancement, and MRI findings of fatty bone marrow changes show no correlation with clinical parameters except RP level. This suggests that MRI can reveal changes at a cellular level that are not depicted by clinical parameters. cknowledgment We thank the Rosalind Russell Medical enter for rthritis Research for its support. bnormal Enhancement and Subchondral Bone Marrow Edema bsent on MRI (n = 8) Present on MRI (n = 10) p a RP value 0.55 (0.18, 1.125) 6.4 (0.63, 9.1) 0.04 ESR value 12.5 (6, 25.5) 9.5 (6, 34) 0.83 BSFI score 36 (15.2, 79.8) 41.2 (22.7, 63.5) 0.48 BSDI score 61.2 (44.8, 69.8) 59.1 (41.8, 65.8) 0.67 Disease duration 14 (12, 18.5) 12.5 (4, 20) 0.58 Inflammatory back pain score 62.2 (57, 76.9) 72.1 (42, 94) 0.97 Nocturnal back pain score 71 (67.7, 77.7) 68.5 (32, 83) 0.70 Total back pain score 75 (53, 78) 60.5 (47, 77) 0.37 Global score Patient 72.2 (54, 79) 64.5 (40, 80) 0.90 Physician 68 (49.7, 82.5) 51.5 (48, 56) 0.11 Note Excluding p values, data are medians (25%, 75%). RP = -reactive protein, ESR = erythrocyte sedimentation rate, BSFI = Bath nkylosing Spondylitis Functional Index, BSDI = Bath nkylosing Spondylitis Disease ctivity Index. a Based on Wilcoxon s rank sum tests. TBLE 3: ssociations mong Radiographic Measures (BSRI Score) by Jonckheere-Terpstra Test for Trend Radiographic Measure MRI Finding Z p a BSRI score Subchondral bone marrow edema 1.4 0.16 BSRI score Enhancement 1.3 0.18 BSRI score Fatty subchondral bone marrow change 2.0 0.05 Subchondral bone marrow edema Enhancement 4.1 < 0.0001 Subchondral bone marrow edema Fatty subchondral bone marrow change 0.0 1.0 Enhancement Fatty subchondral bone marrow change 0.3 0.77 Note MRI findings of subchondral bone marrow edema strongly correlate with abnormal enhancement. Fatty subchondral bone marrow changes on MRI show an inverse correlation with subchondral bone marrow edema or abnormal enhancement. Fatty changes on MRI correlate with the BSRI score. 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