The accuracy of magnetic resonance imaging of the hands and feet in the diagnosis of early rheumatoid arthritis

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1 Joint Bone Spine 74 (2007) 362e367 Original article The accuracy of magnetic resonance imaging of the hands and feet in the diagnosis of early rheumatoid arthritis Cuneyt Calisir a, *, Ali Ilker Murat Aynaci a, Cengiz Korkmaz b a Department of Radiology, Osmangazi University, Medical Faculty, Eskisehir, Turkey b Department of Rheumatology, Osmangazi University, Medical Faculty, Eskisehir, Turkey Received 21 January 2006; accepted 5 July 2006 Available online 30 May Abstract Objective: To analyze MRI findings of early RA in the hand and foot joints and to determine any discrepancies between MRI findings in the hands and feet. Methods: Twenty one patients who fulfilled the 1987 American College of Rheumatology (ACR) criteria for the diagnosis of RA at the onset underwent MRI of both hands and feet. Results: In 18 out of 21 patients, rheumatoid changes were observed in the hand and foot joints. However, rheumatoid changes were observed only in the hand joints of the three remaining patients. MRI revealed pathologic findings suggested RA in the hands of 21 of 21 patients. In the feet, MRI findings suggested RA in 18 of 21 patients. Bone erosions were seen in the hands of 14 patients (67%). Observers found as many bony changes in the hands as in the foot joints. MRI detected active synovitis in 17 patients (81%) in the hands and in 15 patients (71%) in the feet. MRI findings suggested bone edema in the hand and foot joints in 14 (63%) and 11 patients (52%), respectively. There was no significant difference between the MCP and MTP joints with respect to RA-based changes obtained in the MRI ( p > 0.05). Conclusion: Evidence of foot involvement is a frequent occurrence in early RA. Ó 2007 Elsevier Masson SAS. All rights reserved. Keywords: MRI; RA; Foot joints; Hand joints 1. Introduction Rheumatoid arthritis (RA) is a systemic inflammatory disorder with estimated prevalence of 1% [1]. The chronic, bilateral, and symmetric joint lesions ultimately result in joint destruction and deformity [2]. Diagnosing RA during its early stage is important to the implementation of active and aggressive treatment, which is expected to prevent RA joint damage, thereby reducing functional decline and improving the longterm outcome [3,4]. The diagnosis of rheumatoid arthritis is based primarily on the 1987 revised criteria of the American College of Rheumatology, including clinical, biologic, and * Corresponding author. Tel.: þ /2802; fax: þ address: aynaci@yahoo.com (C. Calisir). radiological findings [5]. Magnetic resonance imaging (MRI) has been established as the most sensitive means for detection of active synovitis and bone erosions in early stage RA [6e8]. The joints of the hands are among the first to be affected by rheumatoid arthritis. Several studies have focused on MRI appearances of the hands [7,9,10]. However, there are only two reports on MRI characteristics of the feet in early RA [11,12]. In these studies, in early RA, MRI showed typical bony changes in hand and foot joints of those patients whose conventional radiographies were normal. In addition, radiography has been found to reveal bony erosions in the foot earlier than in the hand joints [13,14]. This suggests that the feet may be primarily affected by early RA. The study was performed to analyze MRI findings of early RA in hand and foot joints and to determine any discrepancies between MRI findings in the hands and feet X/$ - see front matter Ó 2007 Elsevier Masson SAS. All rights reserved. doi: /j.jbspin

2 C. Calisir et al. / Joint Bone Spine 74 (2007) 362e Methods 2.1. Patients Between 2001 and 2005, 21 patients who fulfilled the diagnosis of RA according to 1987 American College of Rheumatology (ACR) criteria at the onset underwent MRI of their hands and feet. Our institutional review board approved the study protocol, and informed consents were obtained from all patients. The study group consisted of 19 women and 2 men with a mean age of 44.5 years (range 20e65 years). Hand (posteroanterior, oblique) and forefoot (anteroposterior, oblique) radiographs were available in all cases and showed no characteristic erosive changes of RA. MRI of the clinically dominant forefoot and hand was performed. Clinically dominant was defined as the site tenderer to pressure and/or with signs of redness and/or hyperthermia and/or swelling. Joints of the dominant hand and forefoot were evaluated in three separate areas, namely wrist or ankle, metacarpophalangeal joints (MCP) or metatarsophalangeal joints (MTP), and proximal interphalangeal joints (PIP). In all joints investigated, when at least one pathological joint was detected in a determined joint area, the area was noted as abnormal. The mean disease duration was 10 months. Medication at entry included non-steroidal anti-inflammatory drugs and corticosteroids in 15 and 1 patients, respectively. None of the patients had previously received disease modifying antirheumatic drugs (DMARD), and five patients were completely untreated MRI protocol MRI was performed with a 1.5 Tesla superconducting magnet (Vision Plus; Siemens, VB33C, Germany) equipped with a flex collimation coil of receiver property for examination of hand and an extremity collimation coil of receiver and transmitter property for examination of foot. Dominant hand was examined while in the prone position with arm hyper extended. In only one case, MRI of the dominant hand was not performed due to extensive shoulder pain experienced by the patient. Dominant foot was scanned while the patient was placed in the prone position with their feet parallel to the floor to prevent patients from moving and to evaluate three separate areas in the same coronal image. In all patients, coronal images of both hand and foot joints were obtained. Axial and sagittal images were not obtained to keep study time shorter since both hand and foot MRI were studied in most of the cases. The examinations consisted of the following sequences: spin echo T1 (SE T1) (TR/TE 400e500/12 ms), fast spin-echo T2 with fat saturation (FSE T2 FS) (TR/TE 4000e5000/45 ms), spin echo T1 with fat saturation (SE T1 FS) (615e660/12 ms) and after administration of i.v gadolinium diethylenetriaminepentaacetic acid (Gd DTPA; 0.1 mmoles/kg of body weight) (Magnevist, Schering, Berlin), and spin echo T1 with fat saturation (SE T1 FS) (615e660/12 ms). For imaging of hand, slice thickness was set as 3 mm, matrix as pixels, excitation as 1, field of view as 25 cm. For imaging of foot, slice thickness was set as 3 mm, matrix as pixels, excitation as 2, and field of view as 23 cm. In all cases, firstly, foot joints were examined by the sequences of T1, fat saturated T1 and T2. Later, hand joints were evaluated by the same sequences. Also, i.v contrast material was given without altering the position of the patient, and fat saturated T1 was obtained. After contrast enhanced study lasting approximately 1.5 min, position of patient was altered, and foot was examined with the same sequence. The overall examination time was about 17 min Analysis of MR images Two experienced MRI readers who were unaware of the patients identities evaluated MR images independently. Evaluation and scoring of MR images of both hand and foot joints was done separately for each patient. MR images were analyzed for bone erosions, synovitis, bone edema and tenosynovitis. Each variable was scored as absent (0) or present (1). In cases of difference of opinion between the MRI readers, a consensus was achieved. MRI criteria were similar to those described in the literature. A distinctive bone defect with cortical break was defined as bone erosion. Bone edema was defined as a lesion within the trabecular bone, with ill-defined margins and signal characteristics consistent with increased water content. Active synovitis was judged to be positive when an area that shows marked enhancement in the synovial compartment and synovial thickening (greater than the width of the joint capsule) were seen. Tenosynovitis was considered to be present when contrast material enhancement of the tendon sheath was observed. MR images of the same patients presented in a randomized fashion to the MRI readers were interpreted twice, with an interval of 5e11 months (mean 7 months) between the 2 interpretations to determine the intra-observer reliability Statistical analysis All statistical analyses were performed using the SPSS 10.0 software package. For assessment of intra- and inter-observer agreement, Cohen s kappa statistics were employed on all variables (erosion, bone edema, synovitis and tenosynovitis). The kappa statistic was interpreted as follows: 0.0e0.20: poor agreement, 0.21e0.40: fair agreement, 0.41e0.60: moderate agreement, 0.61e0.80: substantial agreement, 0.81e1.00: almost perfect agreement. Differences were considered statistically significant if p values were less than Fisher s chi-square test was used to compare the radiological findings of hand and foot. Values of p < 0.05 were considered to be significant. 3. Results 3.1. Hands MRI revealed pathologic findings suggesting RA in the hands of all patients. Rheumatoid changes were detected on MR images in 147 out of 231 joints. MR imaging detected erosions in 70 joints in 14 patients (67%) (Table 1). Wrist (n ¼ 37) and the MCP joints (n ¼ 29)

3 364 C. Calisir et al. / Joint Bone Spine 74 (2007) 362e367 Table 1 Distribution of MRI findings in 21 patients suffering from RA Number of patients Bone edema Inflammation of synovium Hand Foot were the most frequently involved (Fig. S1; see the supplementary material associated with this article online) (Table 2). In the wrists, most common sites for erosions were capitate (n ¼ 12), lunate (n ¼ 10), scaphoid (n ¼ 8) (Fig. S2a). Bone edema was seen in 14 patients (67%) (Table 1). Bone erosion and bone edema were seen simultaneously in 64 (43%) out of 147 joints. Whereas, bone edema without evidence of a bone erosion was observed in five joints (PIP). Synovial contrast enhancement (active synovitis) was observed in 114 joints in 17 patients (81%) (Table 1). MR images revealed this frequency of involvement: MCP joints were involved 55 times, wrists 48 times (Fig. S2b), and PIP joints 11 times (Table 2). The 2nd (n ¼ 35) MCP joints were the most frequently involved. MR imaging detected tenosynovitis in 12 (57%) out of 21 patients. The most commonly affected site for tendon involvement was flexor digitorum tendon (n ¼ 8). Using clinical examination as a reference, the sensitivity, specificity, accuracy, positive predictive value (ppd) and negative predictive value (npd) of MRI in the detection of rheumatoid changes in the hands of patients with early rheumatoid arthritis respectively were 0.86, 0.90, 0.87, 0.95, and Feet Erosion MRI revealed pathologic findings suggesting RA in the feet of 18 of 21 patients (86%). Rheumatoid changes were seen in 114 out of 231 joints. Observers found erosions in 55 joints in 11 patients (52%) (Table 1). MTP joints (n ¼ 29) and ankle (n ¼ 22) were the most frequently involved (Table 2). In the ankles, talus (n ¼ 12) was the most frequently affected. In the MTP joints, the most common sites for erosions were the medial aspect of the 1st MTP (n ¼ 7), lateral aspect of the 5th MTP (n ¼ 6) and lateral aspect of the 3rd MTP (n ¼ 4) joints (Fig. S3a). However, no significant difference was found between the MTP joints. MR imaging detected bone edema in 11 patients Table 2 Distribution of rheumatoid changes in 231 joints from 21 patients suffering from RA Number of joints affected Bone edema Inflammation of synovium Erosion Wrist 32 (46%) 48 (42%) 37 (53%) MCP 30 (43%) 55 (48%) 29 (41%) Hand PIP 7 (11%) 11 (10%) 4 (6%) Total 69 (100%) 114 (100%) 70 (100%) Ankle 24 (46%) 33 (43%) 29 (53%) MTP 24 (46%) 37 (48%) 22 (40%) Foot PIP 4 (8%) 7 (9%) 4 (7%) Total 52 (100%) 77 (100%) 55 (100%) (52%) (Table 1). Bone erosion and bone edema were seen simultaneously in 48 (42%) out of 114 joints. Four MTP joints showed only bone edema without erosion. Isolated bone erosion was observed in three joints (one ankle, one MTP joint and one PIP joints). Synovial contrast enhancement (active synovitis) was observed in 77 joints in 15 patients (71%) (Table 1). MR images revealed this frequency of involvement: MTP joints were involved 37 times (Fig. S3b), ankle was involved 33 times (Fig. S4), and PIP joints were involved 7 times (Table 2). The 5th (n ¼ 17) MTP joints were the most frequently affected. MR imaging detected tenosynovitis in 8 (40%) out of 20 patients. Flexor digitorum tendons were more frequently involved than the extensor ones. Using clinical examination as a reference, the sensitivity, specificity, accuracy, ppd value and npd value of MRI in the detection of rheumatoid changes in the feet of patients with early rheumatoid arthritis respectively were 0.85, 0.82, 0.84, 0.81, and Hands versus feet In 18 out of 21 patients, rheumatoid changes were observed in the hand and foot joints. However, rheumatoid changes were observed only in the hand joints of the three remaining patients. Six patients had bone erosions in the hands without bony changes in the feet. In four patients, osseous abnormalities were seen only in the foot joints (Fig. S3a). There was no significant difference between the hand and foot joints in term of erosion ( p > 0.05). Four patients had rheumatoid changes in the MCP joints without changes in the MTP joints. Two patients had isolated rheumatoid changes in the MTP joints. There were no significant differences between the MCP and MTP joints in terms of rheumatoid changes ( p > 0.05). In two patients, active synovitis was seen only in the hand joints (Fig. S2b). In another patient, synovitis was diagnosed only in the foot joints. There was no significant difference between hand and foot joints in terms of synovitis Inter- and intra-observer reliabilities Inter-observer reliability values showed good to excellent agreement for variables in the hands (k ¼ 0.79 for synovitis, k ¼ 0.82 for bone edema and k ¼ 0.87 for erosion). Interobserver agreement between the readers was good to excellent with regard to variables in the feet (k ¼ 0.77 for synovitis, k ¼ 0.80 for bone edema, and k ¼ 0.84 for erosion). There was no significant difference between the hands and the feet in terms of kappa values. Intra-observer reliability values showed excellent agreement (k ¼ 0.89 for hands, k ¼ 0.85 for feet, and overall k ¼ 0.87). 4. Discussion Radiography of the hand and wrist is the traditional method used for diagnosing, staging, and following up on patients with

4 C. Calisir et al. / Joint Bone Spine 74 (2007) 362e rheumatoid arthritis. However, several studies have reported that MRI is more sensitive for detecting bone erosions in the early rheumatoid arthritis of the hand and wrist [15e19]. MRI is also documented in the literature as an effective imaging method in determination of inflammation of synovium, osseous and soft tissue abnormalities [7,14,18,20]. It is known that the synovial fluid and synovitis are related to each other especially in the long-term RA cases [21]. In a study by Boutry et al., it was indicated that both synovial thickening and effusion are expressions of the same process in RA [11]. Since rheumatoid pannus is hypervascular, numerous studies have shown that intravenous administration of contrast material with fat suppression techniques allows distinction between synovitis and joint effusion [22e24]. Data from earlier studies [25,26] also suggest that MR image acquisition should be performed quickly after gadolinium contrast injection (6e 11 min) to allow better delineation of synovium from joint effusion. In the present study, we imaged the joints with contrast-enhanced MR imaging with fat suppression. Contrast enhanced studies were completed in 6e7 min, and time intervals stated in the literature related to evaluation of synovitis were used. Thus synovitis could be reliably differentiated from the synovial fluid. Synovitis in RA has been studied by a number of groups using MRI. In these studies, MRI evidence of synovitis has been observed in the majority of early RA patients [27e29]. In this regard, it is predictable that active synovitis was observed in 81% of our series of patients. Erosive bony changes are more characteristic of early RA than of synovitis [17,18]. Conaghan et al. showed that, in early RA, synovitis appears to be the primary abnormality, and bone damage occurs in proportion to the level of synovitis but not in the absence of synovitis [30]. Several studies, however, have suggested that erosions occur in very early RA [31e33]. In Klarlund s study, MR imaging detected bone erosions of the MCP and PIP joints in 50% patients [15]. Boutry et al. reported a higher MR prevalence of bone erosion (80%) on patients who had median disease duration of 12 months [11]. In our study (average disease duration 10 months), we observed that the prevalence of erosion in the hand joints was similar to what was reported in that study. On the other hand, in a recent study in which the MTP joints of patients with early RA in whom findings on MR images of the hands were normal were examined, erosion was observed in only 2 (20%) of the patients, whereas synovitis was observed in all (100%) of the patients [12]. Our results are not in agreement with the results of that study. This difference might be explained by the shorter disease duration of the patients with RA in that study (average duration 9.4 weeks), whereas the present study group was characterized by longer mean disease duration of 10 months. Bone edema is known as a very early marker of inflammation and, in addition to synovitis, as a strong individual predictor of bone erosion [32,34]. STIR and T2 weighted sequences are well known for sensitive in detecting bone edema. Because STIR or T2-weighted sequences were not used by Boutry et al., detection of the early arthritis marker bone edema failed in that study [11]. Ostendorf et al. have shown bone edema in the foot joints of 70% of early stage RA patients whose hand joints were normal [12]. In similar to Ostendorf et al., we used T2 weighted imaging which probably allowed a more accurate assessment of bone edema. As shown in our and Ostendorf s study, bone edema seems to be a typical MRI feature in patients with early RA. However, in majority of the patients, we observed that edema was associated with erosion. This is not in agreement with the results of corresponding studies since they did not support the claim that edema could be strong individual predictor of bone erosion. In general, signs of edema are not detectable by clinical examination and imaging modalities such as conventional radiography and ultrasonography. Therefore, assessment of bone edema remains in the domain of MRI. Hand joints are usually affected in patients with RA [17]. Reports of osteodestruction being detected by conventional radiography earlier and more frequently in the foot than in the hand joints [13,14,35] provide accumulating evidence that the foot may be primarily affected in the early stages of RA. In view of this, MR imaging of the feet has potential applications in early diagnosis of RA. Several studies have focused on the MRI appearances of the hands [20,21,36,37]. However,to our knowledge, there are only two published studies describing the MR findings of early RA in the feet or comparing hand and foot involvement [11,12]. It should be noted that both studies were carried out using the axial MRI scans. Furthermore, in foot studies, only rheumatoid changes related to MTP joints were evaluated. In the study of Ostendorf, all patients whose hand MRI was normal showed rheumatoid changes in the foot joints. Based on this, it was thought that RA initially develops in the MTP joints. But in that study, only the MCP joints were evaluated and wrist joints were not examined. In this study, in 4 patients (19%) with RA, MCP joints were normal whereas wrist joints showed rheumatoid arthritis related MRI changes. Based on this result, we suggest that in the examination of hand with MRI, wrist joints have to be analyzed as well. Moreover, the exclusion of wrist joints may be interpreted as a deficiency of that study. In the present study, in the evaluation of the MCP and MTP joints, rheumatoid changes were found only in the MTP joints in two cases. In addition, changes were found only in the MCP joints in four cases. These findings do not support the idea that RA initially starts in the foot joints. Similarly, in the study of Boutry et al. with 30 cases, they observed same ratios of bone lesions in the MCP and MTP joints and proposed that, in the early detection of RA, if hand MRI examination was insufficient, MRI examination of the foot joints could help evaluation. The high sensitivity of our results might be explained by the fact that our patients mean disease duration (10 months) seems to be longer than usual for cases of early RA. Another factor contributing to the high sensitivity of our results might be the fact that none of the patients received disease modifying antirheumatic drugs (DMARD). Unfortunately, in this study disease activity was not evaluated by using the Disease Activity Score 28-joint (DAS-28). This may be regarded as a limitation of the present study. Some groups [17,30,32,38,39] were selected to evaluate only the most symptomatic hand or the dominant hand at

5 366 C. Calisir et al. / Joint Bone Spine 74 (2007) 362e367 the side of the body in a whole-body system. Such assessment is more comfortable for the patient but may lead to falsenegative diagnosis in case of unilateral involvement. According to this, examination of clinically dominant hand and foot by MRI may be regarded as another limitation of the present study. To conclude, as the sensitivity of conventional radiography is especially low in detection of joint changes in the early stages of RA, MRI findings hold a very important role among other radiological modalities [40] in the time of diagnosis. MRI is insufficient or controversial, MRI of the feet can be used as additional diagnostic instrument in the diagnosis of early RA [41]. Supplementary information Supplementary figure (Figs. S1eS4) associated with this article can be found at at doi: /j.jbspin References [1] Gabriel SE, Crowson CS, O Fallon WM. The epidemiology of rheumatoid arthritis in Rochester, Minnesota, 1955e1985. 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