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Musculoskeletal Imaging |
Treatment: Pilot Study1
1 From the Department of Rheumatology, Center for Cellular and Molecular Therapy (C.R., B.A., O.K., L.M., V.B., M.G.M.), Department of Bone and Joint Radiology (S.M.), and Department of Nuclear Medicine (C.B.), University Hospital of Liège, Room 155 BC + 3, CHU Sart-Tilman B35, B-4000 Liège, Belgium. Received March 5, 2002; revision requested May 22; final revision received January 14, 2003; accepted February 24. Address correspondence to C.R. (e-mail: clio.ribbens@ulg.ac.be).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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agent infliximab.
MATERIALS AND METHODS: Wrists, metacarpophalangeal (MCP) joints, and proximal interphalangeal (PIP) joints in 11 patients with active RA were assessed before and 6 weeks after three infliximab infusions. US assessment was performed at a single site in the MCP and PIP joints and at two sites (radiocarpal and intercarpal) in the wrists. Twenty measurements were performed in the wrists; 110 measurements, in the MCP joints; and 103 measurements, in the PIP joints. Two wrists and seven PIP joints were excluded owing to complete joint destruction. US parameters (synovial thickness, number of US-positive joints [ie, with synovial thickness 
1 mm], cumulative synovial thickness index, and presence of Doppler signal) and clinical parameters (swollen joint count) were independently assessed and compared with baseline values by using the McNemar 
2 and paired Student t tests.
RESULTS: After infliximab treatment, there was a significant decrease in the mean numbers of swollen and US-positive joints and in the cumulative synovial thickness (P < .05). The mean synovial thickness decreased in all joints swollen at baseline and in the MCP and PIP joints not swollen at baseline (P < .01). Change from baseline cumulative synovial thickness correlated significantly with change in disease activity score (r = 0.69, P < .05). The number of positive Doppler US signals decreased significantly (in 13 US-positive joints at baseline, in five after treatment; P < .05).
CONCLUSION: US is a feasible imaging modality for measurement of the response of RA small-joint synovitis to therapy.
© RSNA, 2003
Index terms: Arthritis, rheumatoid, 43.71 • Hand, arthritis, 43.71 • Joints, US, 43.12983, 43.12984, 43.12989 • Synovitis, 43.71 • Ultrasound (US), power Doppler studies, 43.12989 • Wrist, arthritis, 43.71
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Until recently, the evaluation of disease activity and therapeutic response was largely based on clinical assessment findings—that is, the tender and/or swollen joint count—in addition to biologic markers of inflammation. However, determination of the number of tender and/or swollen joints is a subjective evaluation that may vary from one assessor to another (6). Furthermore, the swelling of a joint represents a crude estimation of the inflammatory process occurring in the joint, and it may represent abnormalities other than synovitis—for example, sheer joint effusion, tenosynovitis, increased thickness of the capsule or periarticular structures, or accompanying or isolated bursitis. Therefore, radiographic techniques for depicting synovitis, particularly that of joints such as the wrists and metacarpophalangeal (MCP) and proximal interphalangeal (PIP) joints, which are early and frequently affected in RA (9), have been developed (7–10).
Magnetic resonance (MR) imaging has been shown to be more sensitive than conventional radiography for depicting erosions (1,2,11,12), and contrast material–enhanced MR imaging allows early identification of inflammatory processes such as synovitis, joint effusion, and tenosynovitis (2,13,14). However, the assessment of multiple joints with MR imaging is time-consuming and too expensive for routine use (1). In contrast, ultrasonography (US) is a noninvasive imaging method of lower cost and greater availability that can be used routinely in the outpatient clinic (8,9,15). It allows visualization of the pannus developing in the inflamed joint, measurements of synovial thickness (at gray-scale US) (1,16,17) and vascularization (at power Doppler US) (4,16–20), and early detection of erosions (3,16,21). US is sensitive, yields reproducible results (1,8,17,18,22), and is applicable to most, if not all, joints involved in RA (7).
Although US can help detect early synovitis and be effective for diagnostic purposes (1,7,17), its role in measuring therapeutic response has been proposed (4,8,23) but rarely studied in patients with RA. Corticosteroids have been shown to induce a decrease in both synovial thickness and power Doppler signal after intraarticular knee injection (4,23). To the best of our knowledge, no studies have focused on the use of US imaging of multiple hand joints for the therapeutic assessment of disease-modifying antirheumatic drugs.
Recent biologic treatments that inhibit the proinflammatory cytokine tumor necrosis factor– (TNF-), such as infliximab (Remicade; Schering-Plough, Brussels, Belgium), are efficacious for treatment of joint inflammation, evaluated clinically and biologically, as well as radiologic destruction in patients with RA (24). In addition to facilitating the down regulation of the proinflammatory cytokine cascade, infliximab reduces synovial membrane neovascularization and hence synovial cellularity (24). Accordingly, the clinical benefit gained with infliximab should result not only from a rapid decrease in the volume of joint effusion but also from a reduction in the synovial thickness. We therefore conducted a pilot prospective study to evaluate with clinical and US assessments the response of hand (ie, wrist, MCP, and PIP) joint synovitis in patients with active RA to treatment with infliximab.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Inclusion criteria for treatment with infliximab were the presence of erosions and active RA despite methotrexate therapy, as determined on the basis of six or more swollen joints, 10 or more tender joints, and one of the following: morning stiffness for longer than 45 minutes, erythrocyte sedimentation rate of greater than 28 mm/hr, or C-reactive protein levels greater than 20 mg/L. The trial was open label: All patients underwent an active treatment regimen of 3 mg of infliximab per kilogram of body weight infused at the start of the study (week 0) and then 2 and 6 weeks after the start of the study. Functional evaluation of disease activity was performed by using the health assessment questionnaire (26), as well as visual analogue scales with values ranging from 0 to 100 mm for pain, fatigue, and patient and physician global assessments of disease activity.
The composite disease activity score (DAS) (27) customarily used for assessing rheumatoid disease activity, DAS28 (28), was calculated for each patient. Because US evaluation of the wrists, MCP joints, and PIP joints was performed, a DAS based on these 22 joints (DAS22) in each patient (excluding elbows, shoulders, and knees) was also calculated by using the same formula used to calculate the validated DAS28:
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Standard laboratory tests included erythrocyte sedimentation rate determined by using the Westergren method and C-reactive protein levels measured by using nephelometry. All biologic, clinical, and functional parameters were assessed the day before the first infusion of infliximab and the day after the third infusion, with the number of swollen joints being determined by an independent physician experienced in joint assessment (C.R.).
US Examination
After the clinical determinations, two physicians experienced in musculoskeletal US—one radiologist (S.M.) and one rheumatologist (O.K.)—performed US examinations of the same joints in each patient consecutively. US was performed by both physicians at baseline (ie, before infliximab treatment) and 6 weeks after treatment. The physicians were not aware of the clinical and laboratory findings in the patients, and at week 6, US was carried out without access to the baseline US results, limiting the possibility of bias at the second examination.
US (Aloka Prosound 5500; Aloka, Tokyo, Japan) was performed by using a B-mode 13.0-MHz transducer and a power Doppler 5-MHz pulse repetition frequency of 521 Hz. Power Doppler settings were standardized to a pulse repetition frequency of 651 Hz. US positioning was standardized for reproducibility and determined according to anatomic landmarks as follows: Wrist scanning was performed in the sagittal plane over the dorsal surface of the radius, lunate bone, and capitate bone; the short axis of the synovial tissues of the radiocarpal joint (on top of lunate bone) and intercarpal joint (on top of capitate bone) was measured. MCP joint scanning was performed in the sagittal plane over the dorsal surface of the joint; the thickness of the hypoechoic tissue between the hyperechoic extensor tendon and the cortical line of the metacarpal neck was measured without exerting any pressure. PIP joint scanning was performed in the sagittal plane over the joint space; the thickness of the hypoechoic tissue over the dorsal surface of the first phalanx was measured.
Synovial measurements were systematically carried out perpendicular to the great axis and at the point of greatest thickness. This standardization of synovial measurements and the fact that US was performed at week 6 without access to the baseline results explain why the bone contours may appear to be slightly different on the figures depicting the same joint in individual patients before and after treatment. Since synovitis is an inflammatory joint process involving cellular and fluid components that cannot be distinguished with US because both synovial tissue and joint effusion can be hypoechoic or anechoic (29,30), synovitis was defined as a hypoechoic or anechoic area in the joint space of the wrist, MCP joint, or PIP joint (1). A cutoff for US positivity was defined as synovitis involving a synovial thickness of at least 1 mm. We determined this value after studying the wrists, MCP joints, and PIP joints in 10 age-matched healthy (control) subjects (seven women and three men) with no rheumatic disease who were evaluated after approval from the institutional review board and informed subject consent were received.
The mean synovial thickness detected in all studied joints was 0.5 mm ± 0.2 (SD), so a US signal was considered to be abnormal when the synovial thickness was equal to or greater than 1 mm (mean of normal values + 2 SDs). Doppler US measurements were simultaneously carried out, and when they were positive, the signal was scored according to a semiquantitative scale on which a score of 0 meant no perfusion; 1, low perfusion; 2, moderate perfusion; and 3, intense intraarticular joint perfusion (4,31). Intraobserver and interobserver variation coefficients for US measurements were determined by performing 10 additional measurements in each joint type and by assessing one wrist, one MCP joint, and one PIP joint in each of 10 patients with RA.
Statistical Analysis
All of the US data presented represent the findings of the two investigators, who reached a consensus in cases of discordance, which represented less than 10% of the cases. Values of synovial thickness are expressed as means ± SDs. Censored values (<1 mm) were replaced by their upper limit (1 mm). The standard Student paired t test was used for comparing individual values before and after infliximab treatment. Qualitative data were compared by using the 2 and McNemar 2 tests for unpaired and paired data, respectively. Results were considered significant at the 5% critical level (P < .05). The association between two quantitative variables was measured by means of the correlation coefficient (linear regression), whereas odds ratios were used to assess the association between two binary findings.
Furthermore, data were analyzed by means of the general linear mixed model. This method allows one to test the effects of laterality (ie, left or right side) and clinical status of the joint (ie, swollen or nonswollen) on synovial thickness while accounting for repeated data (ie, results for the same patients) and therefore avoid a possible hidden correlation when comparing swollen and nonswollen joints and when comparing before- and after-treatment values for the same 11 patients.
Interobserver and intraobserver variation coefficients were calculated according to the method of Snedecor (32). Interobserver variation coefficients were calculated according to US measurements in one wrist, one MCP joint, and one PIP joint in each of 10 patients, with one patient left out for logistic reasons. Owing to the good precision of the technique, only three patients underwent repeat US measurements in the wrist, MCP joint, and PIP joint for intraobserver variation coefficient determination. All statistical calculations were carried out by using computer software (StatView II 1.03; Abacus Concepts, Berkeley, Calif), and the SAS mixed procedure (version 8.2 for Windows; SAS Institute, Cary, NC) was performed for statistical calculations by using the general linear mixed model. All statistical tests were two sided.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Baseline US and Clinical Joint Assessments
The baseline disease activity of the 11 patients with RA was assessed by using clinical, functional, and biologic parameters. The mean numbers of tender and swollen joints were 29 (range, 12–51) and 19 (range, 7–31), respectively. Mean values of functional parameters were 1.51 (range, 0.75–3.00) for the health assessment questionnaire score and 61 mm (range, 38–85 mm), 69 mm (range, 24–95 mm), 68 mm (range, 45–88 mm), and 69 mm (range, 46–90 mm) for visual analogue scale values of pain, fatigue, and patient and physician global assessments of disease activity, respectively. The mean erythrocyte sedimentation rate was 37 mm/hr (range, 15–72 mm/hr), and the mean C-reactive protein level was 33 mg/L (range, 13–68 mg/L). The mean composite DAS28 was 7.5 (5.6–9.3), with all patients exhibiting high disease activity (DAS28 > 5.1) (28,33).
The results of clinical evaluation of the wrists and the MCP and PIP joints were compared with the results of US evaluation of these structures. Two hundred thirty-three (96%) of 242 joints were analyzed; seven PIP joints and two wrists were excluded from US evaluation owing to complete joint destruction. Joints were clinically judged to be positive for synovitis if they were swollen and were judged with US to be positive if they had a synovial thickness of 1 mm or greater. The mean number of swollen hand joints (ie, PIP joints, MCP joints, and wrists) per patient was 11 (range, five to 22), and the mean number of US-positive joints was 11 (range, one to 18). The numbers of each type of clinically positive and US-positive joint are shown in Table 1. Overall, about 50% of the joints assessed were swollen and about 50% were positive at US. The value of US was evaluated by determining its sensitivity and specificity compared with those of the clinical examination, the current standard of reference.
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We next compared the number of US-positive joints and the synovial thickness of swollen and nonswollen joints at baseline clinical evaluation (Table 2). Since there could have been a hidden correlation when comparing multiple joints in the same 11 patients, a general linear mixed-model approach accounting for repeated data was used. In all joints studied, the percentage of US positivity was twice as high in the swollen joints as it was in the nonswollen joints (Table 2). The synovial thickness was significantly higher in the swollen wrists, MCP joints, and PIP joints than in the corresponding nonswollen joints (Table 2).
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US and Clinical Joint Assessments after Infliximab Treatment
After 6 weeks of infliximab treatment, both the number of swollen joints and the number of US-positive joints decreased significantly (Table 1). The global disease activity of hand joints assessed by using the DAS22 also showed a significant decrease, from a mean value of 6.2 to a mean value of 4.5 (P < .01, paired t test). Similarly, the mean cumulative synovial thickness significantly decreased from 32 to 16 mm (P < .01, paired t test). When each joint was analyzed separately, there was a significant decrease in the number of swollen wrists and MCP joints but not in the number of swollen PIP joints (Table 1).
In contrast, US evaluation revealed a significant decrease in the number of US-positive MCP joints and PIP joints but not in the number of US-positive wrists (Table 1). The synovial thicknesses at week 6 were compared with baseline values, again by using the general linear mixed-model approach. As shown in Table 2, the synovial thickness was significantly decreased after infliximab treatment not only in the joints that were swollen at baseline but also in the MCP and PIP joints that were clinically judged to be nonswollen at baseline. The image in Figure 1 is a typical depiction of synovial thickness in an MCP joint, as represented by the dotted line between the white marks, before and after treatment.
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With application of the same criteria to the individual analysis of the 13 US-positive PIP joints that were swollen at both baseline and 6 weeks, with no significant change in mean synovial thickness (Table 3), we identified six joints that had significantly improved (mean decrease in synovial thickness, 0.9 mm ± 0.3; P < .01) and five that had significantly worsened (mean increase in synovial thickness, 0.6 mm ± 0.4; P < .05). Finally, the number of positive Doppler signals decreased significantly: 13 joints had positive signals at baseline, and five had positive signals after infliximab treatment (P < .05). Eight signals disappeared, as illustrated in Figure 2 (ie, perfusion score changed from 2 to 0), three decreased (ie, perfusion score changed from 2 to 1), and two remained unchanged.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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agent infliximab in patients with RA. We still do not have a reference standard for the evaluation of joint inflammation (23), and the standardized assessment of rheumatoid disease activity requires evaluation of a combination of clinical, functional, and biologic variables (28). As shown by the odds ratios for swollen and US-positive joints in the present study, clinical and US assessments are markedly related. Furthermore, we observed a higher frequency of US positivity in the swollen joints than in the nonswollen joints and significantly greater synovial thickness in the swollen versus nonswollen wrists, MCP joints, and PIP joints. However, while US and clinical assessments are related, they do not strictly convey the same information and are complementary rather than redundant. US depicted synovitis in about 30% of joints that were clinically considered to be uninjured because they were not swollen.
Furthermore, the US and clinical parameters did not correlate with the same biologic parameter. The correlation between erythrocyte sedimentation rate and the US parameters of synovitis was previously reported by Qvistgaard et al, who found that erythrocyte sedimentation rate correlated with the vascularization of the synovial membrane evaluated by using power Doppler US (18). In accordance with these authors, we did not observe a correlation between US parameters and either clinical parameters, functional parameters, or composite indexes of disease activity at baseline. Considered together, our study data indicate that US yields additional information about joint inflammation and is a complement to clinical examination, the current standard of reference.
While US is widely accepted for the diagnostic evaluation of RA, its use for the assessment of response to treatment has not been extensively studied. Gray-scale US has been shown to reliably depict changes in knee joint synovitis in response to arthroscopic synovectomy (34). Intraarticular administration of steroids in knees with RA is followed by a persistent decrease in synovial thickness (23) and by a qualitative decrease in knee synovial perfusion as assessed by using power Doppler US (4). Oral and parenteral steroids also induce a decrease in power Doppler signal in the MCP joints of patients with RA (19). Furthermore, the results of a recent study involving five patients with RA who were treated with the anti–TNF- treatment etanercept (Enbrel; Wyeth) showed that high-resolution US depicts a decrease in pannus vascularization in the second MCP joint (35).
Our study data show that in response to another anti–TNF- treatment, infliximab, the US parameters (ie, number of US-positive joints and synovial thickness) for the wrists and MCP and PIP joints improved as the disease activity decreased. However, US offers several advantages over simultaneously performed clinical assessment. In joints that clinically respond to treatment, US allows one to measure the synovial thickness as well as visualize the improvement of the pannus, the final target of anti–TNF- therapy. In our study, US also depicted a significant decrease in the mean synovial thickness of the MCP and PIP joints that were thought not to be involved by synovitis since they were judged clinically to be nonswollen and in the mean synovial thickness of the wrists and MCP joints that were classified as 
nonresponding
(ie, still swollen at week 6).
On the basis of results of an individual analysis of the synovial response in this study, one can calculate that 60%–86% of US-positive joints had a significant decrease in synovial thickness after three infliximab infusions. The somewhat lower response in the wrists (60%) might have been associated with the synovial thickness detected with US, which is more important; the smaller the volume of the pannus the greater the efficacy of infliximab. When US and clinical evaluations are considered together, the response to treatment is greater in joints evaluated by using US than in those evaluated by using clinical examination: A significant reduction in synovial thickness was observed in 78% of the US-positive joints but in only 57% of the swollen joints. These data further highlight the fact that clinical examination, although the current standard of reference, is certainly not a gold standard and emphasize the interest in combining clinical and US assessments.
We believe it is interesting that we observed significant correlations between the change in the cumulative synovial thickness of the 22 hand joints, which is likely to reflect disease severity, and both the change in the DAS calculated for these 22 joints (ie, DAS22) and the change in the physician global disease assessment. These observations strongly suggest that the decrease in the size of the pannus, as assessed by using US, is a genuine clinical corollary in patients with RA.
Power Doppler US also offers the opportunity to study the vascularization of the pannus. Walther et al recently showed the concordance between the identification of a Doppler signal within the pannus and the histologic identification of vessels within the same pannus (36). It has also been shown with use of an intravenous US contrast agent that a positive Doppler signal can be used to identify a vessel (18). In our work, only 10% of the US-positive joints, mainly the wrists, had a positive Doppler signal at baseline. This small percentage of Doppler signals was probably due to the fact that all patients were treated with 15 mg of methotrexate per week, and most of them were also taking steroids. Data on patients with active RA who have not taken disease-modifying antirheumatic drugs show a higher incidence of Doppler signals: in 13% (PIP joints) to 51% (wrists) of US-positive joints (37).
In the present study, after infliximab treatment, the number of positive Doppler signals was significantly reduced; only two joints did not exhibit a change in Doppler score with use of the semiquantitative scale. Our study data thus confirmed in vivo that infliximab can induce a reduction in angiogenesis, as previously suggested in vitro (24).
A limitation of our study is related to the trial being an open-label one, with neither the patients nor the physicians being blinded to the treatment regimen. However, our study results have shown that it is feasible to use US to assess the therapeutic response of synovitis. Furthermore, we believe the fact that the clinical and US assessments were performed completely independently of each other and the findings of significant correlations between the US and clinical parameters before as well as after treatment reinforce the validity of the data. A larger long-term double-blind trial is necessary to confirm the results of this pilot study and is in progress.
In conclusion, our study results show that joint US examination is complementary to the standard clinical joint count in the assessment of synovitis in patients with RA and helps monitor the response to infliximab treatment. Power Doppler US findings reflect the vascularization of the pannus, which is a target of anti–TNF- therapies. Joint US could therefore become an essential tool for RA joint monitoring in view of its sensitivity in the detection of synovitis, feasibility in the outpatient clinic, and low cost.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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= tumor necrosis factor– Author contributions: Guarantor of integrity of entire study, M.G.M.; study concepts, C.R., L.M., C.B., M.G.M.; study design, C.R., B.A., S.M., O.K., V.B., M.G.M.; literature research, C.R., O.K., C.B.; clinical studies, C.R., B.A., V.B.; data acquisition, C.R., S.M., O.K., V.B.; data analysis/interpretation, C.R., S.M., O.K., M.G.M.; statistical analysis, C.R., M.G.M.; manuscript preparation, C.R., S.M., O.K., M.G.M.; manuscript definition of intellectual content, C.R., L.M., M.G.M.; manuscript editing, C.R., M.G.M.; manuscript revision/review, C.R., S.M., L.M., M.G.M.; manuscript final version approval, C.R., B.A., S.M., O.K., L.M., V.B., M.G.M.
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