The Role of Dynamic Contrast- Enhanced MRI in the Differential Diagnosis of Psoriatic and Rheumatoid Arthritis

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1 Musculoskeletal Imaging Original Research Schwenzer et al. MRI in Psoriatic and Rheumatoid Arthritis Musculoskeletal Imaging Original Research Nina F. Schwenzer 1,2 Ina Kötter 3 Jörg C. Henes 3 Christina Schraml 1,2 Jan Fritz 1 Claus D. Claussen 1 Marius Horger 1 Schwenzer NF, Kötter I, Henes JC, et al. Keywords: DCE-MRI, dynamic contrast-enhanced MRI, psoriatic arthritis, RA, rheumatoid arthritis DOI: /AJR Received February 28, 2009; accepted after revision September 2, Department of Diagnostic and Interventional Radiology, University Hospital of Tübingen, Hoppe-Seyler-Strasse 3, Tübingen, Germany. Address correspondence to N. F. Schwenzer (nina.schwenzer@med.uni-tuebingen.de). 2 Section on Experimental Radiology, Department of Diagnostic and Interventional Radiology, University Hospital of Tübingen, Tübingen, Germany. 3 Department of Internal Medicine II, University Hospital of Tübingen, Tübingen, Germany. AJR 2010; 194: X/10/ American Roentgen Ray Society The Role of Dynamic Contrast- Enhanced MRI in the Differential Diagnosis of Psoriatic and Rheumatoid Arthritis OBJECTIVE. The purpose of this study was to investigate the role of dynamic contrastenhanced MRI in the differential diagnosis of psoriatic and rheumatoid arthritis in the hand and wrist. SUBJECTS AND METHODS. Forty-five consecutive patients (31 patients with rheumatoid arthritis and 14 patients with psoriatic arthritis) were examined in a 3-T whole-body MR unit. After contrast injection, a 3D encoded spoiled gradient-echo sequence was used for measurement of the time course of contrast-medium uptake in the synovial tissue. On the basis of the gained uptake curves, the rate of early enhancement was calculated after 35 and 52 seconds, and the relative enhancement rate was calculated after 35 seconds, 52 seconds, 3 minutes, and 15 minutes (late enhancement). Dynamic contrast-enhanced MRI rates of patients with rheumatoid arthritis and psoriatic arthritis were compared and correlated with laboratory and clinical data. RESULTS. A statistically significant difference between the two groups was found regarding the relative enhancement rate after 15 minutes (p < 0.01). In contrast, no difference in relative enhancement rate was found 35 seconds, 52 seconds, or 3 minutes after contrast injection (p = 0.695, p = 0.573, and p = 0.278, respectively). Regarding the rate of early enhancement at 35 and 52 seconds, no significant difference between patients with rheumatoid arthritis and those with psoriatic arthritis was found. Significant correlations were found between inflammatory parameters and dynamic contrast-enhanced parameters in patients with rheumatoid arthritis but not in those with psoriatic arthritis. CONCLUSION. Fifteen minutes after contrast injection, a statistically significant difference between rheumatoid arthritis and psoriatic arthritis was found in synovial enhancement that might play an important role in differentiating the two diseases. I n the past, the treatment strategy for patients with psoriatic arthritis was based on that for patients with rheumatoid arthritis. Recent research indicates that the therapeutic management, including medication and therapy monitoring, has to be adapted for each type of arthritis [1]. In particular, there are some new biologic agents for treating rheumatoid arthritis that are not effective or have not been approved for treating psoriatic arthritis, because clinical studies on the treatment of psoriatic arthritis are relatively sparse. Clinically, it may be difficult to distinguish polyarticular psoriatic arthritis from rheumatoid arthritis, at least in cases where distal interphalangeal joints are not affected. In these cases, laboratory examinations may be helpful, but 30% of rheumatoid arthritis cases are seronegative (without rheumatoid factors or cyclic citrullinated peptide antibodies). In early disease stages, radiographs typically are normal; hence, other imaging techniques are evaluated for their performance in the diagnosis of psoriatic arthritis and its differentiation from rheumatoid arthritis. In the course of the inflammation process in rheumatoid arthritis, the synovial tissue is invaded by activated T cells and macrophages. Molecular mediators of inflammation, including tumor necrosis factor α and interleukins, are released. Granulation tissue accumulates at the edges of the synovial lining (pannus) with extensive angiogenesis and production of enzymes that cause damage of soft tissue and bone, leading to deformity, ankylosis, and severe secondary degenerative damage in the joints. Similarly, psoriatic arthritis synovium shows infiltration with B cells and macrophages, as well as interleukin, interferon-γ, and tumor necrosis factor α, and a marked increase in osteoclastic precursors, which can AJR:194, March

2 Schwenzer et al. explain the extensive bone erosions in patients with psoriatic arthritis. MRI has been established as a valuable imaging technique in arthritic patients [2 9]. Several researchers have shown that dynamic contrast-enhanced MRI measurements correlate with clinical, imaging, and histologic measures of inflammation [2 9]. Because dynamic contrast-enhanced MRI is able to identify increased vascularization and perfusion through the capillaries in the synovial membrane in both rheumatoid and psoriatic arthritis, it should thereby provide information about inflammation activity in the affected joint [3, 10]. The goal of the current study was therefore to investigate the role of dynamic contrast-enhanced MRI in the differential diagnosis of psoriatic and rheumatoid arthritis in the hand and wrist. Subjects and Methods Patient Population Studies were performed on 45 consecutive patients (Table 1). Patients either did not receive medication for at least 5 weeks or were taking stable lowdose oral steroid medication (< 10 mg/d). Patients with active arthritis were assessed using the Disease Activity Score 28 (> 3.5). Patients with rheumatoid arthritis fulfilled the American College of Rheumatology revised criteria for classification of functional status in rheumatoid arthritis [11]. A polyarticular rheumatoidlike pattern of arthritis was found in all patients with psoriatic arthritis. Only patients with a confirmed diagnosis of psoriasis were included. All patients diagnosed as having psoriatic arthritis were negative for rheumatoid factors and antibodies against cyclic citrullinated peptides, as well as for antinuclear antibodies according to the Classification of Psoriatic Arthritis criteria [12]. Blood samples were obtained for the determination of C- reactive protein, anti cyclic citrullinated peptides, and IgM rheumatoid factor by standard laboratory methods (Table 1). The region of one hand (wrist, metacarpophalangeal, or proximal interphalangeal joints) that was clinically most conspicuous was imaged. If several regions were symptomatic, the most proximal joint was evaluated. The study was performed at a single institution. Subjects written consent was obtained according to the Declaration of Helsinki, and the design of the work has been approved by our institutional research ethics board. MRI Examination Protocol All measurements were performed on a 3-T whole-body MRI scanner (Magnetom Trio, Siemens Healthcare). A one-channel receive/transmit wrist-coil was applied. Patients were placed in TABLE 1: Anthropometric, clinical, and laboratory data Characteristic prone position with the arm extended over the head. The hand and the wrist were tightly fixed with sand bags. After placement of gradient-echo localizers, the following sequences were used: axial T1- weighted 2D spin-echo (TR/TE, 600/12; slice thickness, 2.0 mm; matrix size, ; in-plane resolution, mm; bandwidth, 195 Hz/pixel; no fat saturation; 2 signal averages; acquisition time, 4 minutes 10 seconds), coronal T1-weighted 2D spin-echo (400/12; slice thickness, 1.5 mm; matrix size, ; in-plane resolution, mm; bandwidth, 194 Hz/pixel; no fat saturation; 2 signal averages; acquisition time, 5 minutes 12 seconds), and coronal T2-weighted 2D fast spinecho (4,220/81; slice thickness, 1.5 mm; matrix size, ; in-plane resolution, mm; bandwidth, 182 Hz/pixel; echo-train length, 15; 4 signal averages; application of spectral fat saturation; acquisition time, 6 minutes 17 seconds). Subsequently, a 3D-encoded spoiled gradientecho sequence (FLASH; 3.91/1.45; resolution, mm; bandwidth, 350 Hz/pixel; 32 slices per slab; slice partial Fourier, 6/8; flip angle, 20 ; spectral fat saturation; acquisition time, 10 seconds) was used for measurement of the time course of contrast-medium uptake in the synovial tissue. After bolus injection of 0.1 mmol of gadopentetate dimeglumine (Magnevist, Bayer- Rheumatoid Arthritis (n = 31) Psoriatic Arthritis (n = 14) Sex (no. male/no. female) 6/25 7/7 Age (y), mean ± SD 54 ± ± 7 Disease duration (y), mean ± SD 9.6 ± ± 8.4 C-reactive protein level (mg/dl), mean ± SD 1.5 ± ± 2.2 Disease Activity Score 28, mean ± SD 5.0 ± ± 1.1 No. of patients with IgM rheumatoid factor 21 0 No. of patients with anti cyclic citrullinated peptides antibodies St / S Time (s) 22 0 Schering) per kilogram of body weight, with an injection rate of 2 ml/s, 16 acquisitions were performed within 2 minutes 47 seconds. Fifteen minutes after contrast medium injection, another four acquisitions were performed for late enhancement (acquisition time, 42 seconds) (Fig. 1). Afterward, a coronal T1-weighted spin-echo sequence was applied (798/12; 2 signal averages; matrix size, ; slice thickness, 1.5 mm; in-plane resolution, mm; bandwidth, 195 Hz/pixel; spectral fat saturation; acquisition time, 5 minutes 31 seconds) for contrast-enhanced imaging. Image Analysis Regions of interest of synovitis were manually placed for each examination in axial slices covering pixels. For better differentiation, the inflamed synovial tissue was outlined on the contrast-enhanced images. For interesting regions of interest placed in affected synovial tissue gadopentetate dimeglumine uptake curves were drawn. Samples of dynamic data sets and corresponding color-coded maps (created with Matlab Version , MathWorks) of exemplary patients with psoriatic arthritis and rheumatoid arthritis are shown in Figures 2 and 3. The rate of early enhancement per second (REE t ) was calculated as follows: 800 1,000 1,200 Fig. 1 Example of gadopentetate dimeglumine enhancement curves showing differences between rheumatoid arthritis ( ) and psoriatic arthritis ( ) in two representative patients. x-axis represents time after gadopentetate dimeglumine injection, and y-axis indicates relative signal enhancement. Note decrease of signal enhancement in psoriatic arthritis 15 minutes after contrast injection (t = 0). 716 AJR:194, March 2010

3 MRI in Psoriatic and Rheumatoid Arthritis Fig. 2 Axial slices of two representative patients from series of dynamic 3D data sets showing images acquired before and 52 seconds, 3 minutes, and 15 minutes after administration of IV contrast agent. Metacarpophalangeal joint region is shown. Third and fourth rows show corresponding color-coded maps. Note pronounced synovial late enhancement of 58-year-old woman with rheumatoid arthritis (RA), compared with 43-year-old man with psoriatic arthritis (PsA). Disease Activity Score was similar in both patients (4.51 for patient with rheumatoid arthritis and 4.27 for patient with psoriatic arthritis). S t S 0 100% S 0 t where t indicates the time after contrast injection (35 and 52 seconds, respectively), and S 0 and S t refer to the signal intensity before and t seconds after contrast injection, respectively. Fig. 3 Coronal 3D double-echo steady-state gradient-echo images of two representative patients. A, Right hand of 38-year-old man with psoriatic arthritis (Disease Activity Score 28 = 5.82). Note involvement of fourth metacarpophalangeal joint. White bar indicates selected slice of dynamic contrast-enhanced data sets (see C). B, Left hand of 47-year-old man with rheumatoid arthritis with involvement of metacarpophalangeal and proximal interphalangeal joints (Disease Activity Score 28 = 6.49). White bar indicates selected slice of dynamic contrast-enhanced data sets (see C). C, Axial slices (white bars in A and B) of two patients shown in A and B from series of dynamic 3D data sets showing images acquired before and 52 seconds, 3 minutes, and 15 minutes after administration of IV contrast agent. Proximal interphalangeal joint region is chosen. In both patients, third digit is affected. Third and fourth rows show corresponding colorcoded maps. Note rapid synovial enhancement of synovium in patient with rheumatoid arthritis (RA) and pronounced synovial enhancement after 15 minutes in both types of arthritis. Although late enhancement is distinct in patient with psoriatic arthritis (PsA), signal intensity declines, compared with patient with rheumatoid arthritis. There is additional inflammatory involvement of distal interphalangeal region and fifth digit in patient with rheumatoid arthritis. Although joint is only marginally covered, distinct synovial contrast enhancement can be seen. Additionally, the relative enhancement in relation to S 0 (RE t ) was calculated as follows: S t S 0 S 0 100% at t = 35 seconds, t = 52 seconds, t = 3 minutes, and t = 15 minutes. Thus, the slope of the enhancement A curve as well as the late enhancement (t = 15 minutes) was assessed. Statistical Analysis Statistical analysis was performed by using statistical software (SPSS version 14.0, SPSS) for B C AJR:194, March

4 Schwenzer et al. Microsoft Windows. For each parameter, mean values and SDs were calculated. Means were compared by the Student s t test if their distribution was normal and by the Mann-Whitney test when the distribution was nonparametric. The Shapiro- Wilk test was used to test for normal distribution of the parameters. Correlations were calculated by Spearman s rank test. The significance level was set to 5%. Results For all 45 patients, diagnostic image quality was reached. For 28 patients, 20 with rheumatoid arthritis and eight with psoriatic arthritis, the metacarpophalangeal joints of the clinically most symptomatic hand were examined. For eight patients, seven with rheumatoid arthritis and one with psoriatic arthritis, the region of the wrist was examined. For 10 patients, five with rheumatoid arthritis and five with psoriatic arthritis, the proximal interphalangeal joints were examined. In 13 cases, 12 patients with rheumatoid arthritis and one with psoriatic arthritis, no late enhancement value was assessed because the prone position in the scanner caused discomfort for the patients. As is shown in Table 1, the clinical and laboratory parameters between the two groups were similar. Table 2 displays the mean and SD of the assessed dynamic contrast-enhanced parameters. A statistically significant difference between the groups was found regarding the relative (late) enhancement after 15 minutes (p = 0.007). In contrast, no difference in relative enhancement was found 35 seconds, 52 seconds, or 3 minutes after contrast injection (p = 0.695, p = 0.573, and p = 0.278, respectively). Regarding the rate of early enhancement at 35 and 52 seconds, no significant difference between patients with rheumatoid arthritis and psoriatic arthritis was found (p = and p = 0.564, respectively). At all investigated time points, the mean relative enhancement after contrast-medium injection was higher among patients with rheumatoid arthritis, although statistical significance was only reached at 15 minutes. In patients with rheumatoid arthritis, a significant correlation was found between Disease Activity Score 28 and the relative enhancement or rate of early enhancement at 35 seconds (ρ = 0.53; p = 0.003) and 52 seconds (ρ = 0.41; p = 0.023) and the relative enhancement at 3 minutes (ρ = 0.41; p = 0.033). No significant correlation was found between Disease Activity Score 28 and the relative enhancement after 15 minutes. A significant correlation was found TABLE 2: dynamic contrast-enhanced MRI parameters in rheumatoid arthritis and psoriatic arthritis Parameter Rate of early enhancement (%/s) Rheumatoid Arthritis between C-reactive protein and the relative enhancement or rate of early enhancement at 35 seconds (ρ = 0.40; p = 0.028). In contrast, no correlation between C-reactive protein, Disease Activity Score 28, and dynamic contrast-enhanced parameters could be found in patients with psoriatic arthritis. Discussion Several studies have shown that MRI is more sensitive than conventional radiography in detecting early inflammatory changes in rheumatoid arthritis [13 16] and psoriatic arthritis [17, 18]. In addition to synovitis and tenosynovitis, bone edema, periostitis, and erosions and their distribution play an important role in the differential diagnosis [3, 10, 19 21]. Only a few studies have compared MRI findings of the hand in patients with psoriatic arthritis and rheumatoid arthritis. Schoellnast et al. [19] found that periostitis and synovitis were more frequent in the proximal interphalangeal joints in psoriatic arthritis, whereas synovitis and erosions of the wrist are typical findings in patients with rheumatoid arthritis. In contrast, Tehranzadeh et al. [17] described more distinct changes in the wrists than in the hands of patients with psoriatic arthritis. It seems crucial to mention that the rheumatoid-like pattern of distribution of lesions was more common in their group of patients with psoriatic arthritis. They argued that this pattern of distribution is related to the synovial prevalence of this psoriatic arthritis subtype. The synovial or polyarticular rheumatoid-like pattern of psoriatic arthritis and its differentiation from rheumatoid arthritis pose a special problem because of the clinical resemblance. It has been suggested that the inflamed synovial membrane of psoriatic arthritis Psoriatic Arthritis At 35 s (5.1 ± 4.3) (4.3 ± 2.7) At 52 s (4.2 ± 2.6) (3.7 ± 2.3) Relative enhancement rate (%) At 35 s (176.8 ± 150.8) (133.8 ± 95.3) At 52 s (217.5 ± 136.5) (191.4 ± 120.4) At 3 min (275.8 ± 100.2) (238.3 ± 104.9) At 15 min (239.4 ± 57.5) (179.6 ± 57.5) a Note Data are shown as range (mean ± SD). a Statistically significant. differs slightly from rheumatoid synovium. Histopathologic studies showed a greater number of synovial vessels per square millimeter, in contrast to rheumatoid arthritis, and a marked thickening in the walls of capillaries and small arteries with inflammatory perivascular infiltrates [22, 23]. Consequently, the uptake of contrast media in psoriatic arthritis and rheumatoid arthritis is presumed to be different, especially regarding the slope of the uptake curve and late enhancement behavior. In the present dynamic contrast-enhanced MRI study, it was possible to differentiate between psoriatic arthritis and rheumatoid arthritis on the basis of synovial late enhancement after 15 minutes. It is known that, in rheumatoid arthritis, the perivascular space is infiltrated by mononuclear cells and the synovium becomes thickened during the course of disease, which goes along with hyperplasia and hypertrophy of the synovial lining cells [24]. The inflamed synovium is composed of proliferating fibroblasts and small blood vessels. In contrast, in psoriatic arthritis, the inflamed synovium shows less cellularity and hyperplasia than in rheumatoid arthritis. This fact could account for the significant difference in late enhancement contrast behavior: Because gadopentetate dimeglumine is transported in the plasma as an unlinked molecule and diffuses freely to the extracellular space, it accounts for the signal increase in T1-weighted images. It seems possible that the volume of the extravascular extracellular space is wider in rheumatoid arthritis because of the higher cellularity and the multiple synovial layers of the highly inflamed synovium, leading to a slower washout of contrast medium. Another explanation could reside in the histologic differences in synovial vascular- p 718 AJR:194, March 2010

5 MRI in Psoriatic and Rheumatoid Arthritis ity. The blood vessels in psoriatic arthritis synovium are tortuous and dilated, whereas those in rheumatoid arthritis membranes have a straight pattern [24 26]. This could have an influence on the washout in psoriatic arthritis, which could be shown to be more rapid in the current study, compared with rheumatoid arthritis. Interestingly, no difference could be found in the rate of early enhancement and the relative enhancement at 35 seconds, 52 seconds, and 3 minutes. Thus, the results are in accordance with findings reported in literature. Cimmino et al. [3] investigated the role of dynamic contrast-enhanced MRI in the diagnosis of psoriatic arthritis and rheumatoid arthritis using a 0.2-T unit and could not find any differences regarding the curve of contrast uptake of the wrist covering a period of six minutes. It is assumed that the rate of early enhancement and relative enhancement rate is more strongly dependent on synovial vascularity and capillary permeability than is late enhancement [10]. Interestingly, findings of several studies indicate a higher degree of synovial vascularity in psoriatic arthritis than in rheumatoid arthritis [27, 28]. On the other hand, the vascular wall seems to be markedly thickened in psoriatic arthritis than in rheumatoid arthritis, which could pose a hindrance in capillary permeability [23]. Nevertheless, these two effects could compensate for one another to a certain degree, leading to a similar wash-in pattern in dynamic contrastenhanced MRI. Regardless of this assumption, there was a tendency toward higher synovial relative enhancement values in patients with rheumatoid arthritis, compared with patients with psoriatic arthritis, at 35 seconds, 52 seconds, and 3 minutes. A significant correlation was found between inflammatory parameters and early enhancement rates in rheumatoid arthritis. On the basis of the hypothesis that the inflammatory process enhances capillary perfusion and permeability, several studies measured the rate of early enhancement and relative enhancement rate over a fixed time period between 30 and 60 seconds and found good correlations between rate of early enhancement and relative enhancement rate and activity scores, inflammation parameters, and medication in patients with rheumatoid arthritis [2, 10, 21]. Cimmino et al. [2] also found significant correlations between Disease Activity Score 28, C-reactive protein, and erythrocyte sedimentation rate and rate of early enhancement and relative enhancement rate (t = 55 seconds) in rheumatoid arthritis, but not in psoriatic arthritis. In the current study, significant correlations could be found between early enhancement and inflammation parameters in rheumatoid arthritis, which is in accordance with the results found in literature. No significant correlation between inflammation parameters and contrast enhancement could be found in psoriatic arthritis, as also found by Cimmino et al. [3]. Obviously, there is the need to correlate synovial and vascular immunohistochemical changes with dynamic contrast-enhanced MRI appearances to validate this result. Although a standardization of the infusion technique was intended, several influencing factors, such as size of the vein, cardiac rate, and blood pressure, could not be controlled. These variables could account for the substantial SD in relative enhancement rate and rate of early enhancement. Regarding the enhancement after 3 and 15 minutes, the influence of these variables decreased, and the changes in diffusion of the contrast agent, as well as the permeability, number, and size of the synovial vessels, seemed to play a predominant role. In the current study, higher values of the dynamic contrast-enhanced parameters were reached, compared with those of dynamic contrast-enhanced MRI studies. In previously published studies, the choice of the examination protocol varied among the research groups. In the current study the chosen gradient-echo sequence was highly T1 weighted, which could account for the higher signal intensities measured after contrast injection. Tam et al. [29] used a gradient-echo sequence at 1.5 T (TR/TE, 2.7/0.95; flip angle, 15 ; slice thickness, 4 mm; number of slices, 11). Although they assessed the enhancement slope slightly differently, their dynamic contrast-enhanced values are comparable to the values presented in this study. In the current study, the aim was to identify enhancement characteristics that could be helpful in the differentiation between rheumatoid arthritis and psoriatic arthritis. However, it might be possible that the enhancement differences we found in clinically unambiguous cases might not be valid for cases that cannot be classified on the basis of laboratory tests and clinical symptoms alone. All patients included in the current study fulfilled the revised American College of Rheumatology and Classification of Psoriatic Arthritis criteria for either rheumatoid arthritis or psoriatic arthritis. Because the included patients were not all in the early stage of the disease, the clinical differentiation was further facilitated because of the course of disease. Whether the difference in the late enhancement we found is valid for an early stage of the disease needs to be investigated in a prospective follow-up study of clinically ambiguous cases. 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