MAGNETIC RESONANCE IMAGING OF SACROILIAC JOINT INFLAMMATION

Transcription

1 1763 MGNETI RESONNE IMGING OF SROILI JOINT INFLMMTION H. HLSTROM, N. FELTELIUS, R. NYMN, and R. HLLGREN consecutive series of 27 patients with symptoms compatible with sacroiliitis underwent magnetic resonance imaging (MRI) of the sacroiliac joints. The diagnostic sensitivity of MRI was similar to that of computed tomography or conventional radiography. However, MRI seems to have the potential of providing unique information about the disease process in sacroiliitis by demonstrating abnormalities in subchondral bone and periarticular bone marrow. The results of this study suggest that early inflammatory changes in sacroiliitis occur in the subchondral structures of the sacroiliac joints. The morphologic characteristics of sacroiliac joint inflammation have been defined mainly by conventional radiology. Radiologic sacroiliitis is a diagnostic hallmark of ankylosing spondylitis (I), but may also be seen in other inflammatory conditions. number of radiographic techniques have been developed to reveal different aspects of sacroiliac joint pathology. Recent studies have indicated that computed tomography (T) may be superior to conventional radiography in the detection of early erosive sacroiliitis and joint space narrowing (2,3). Magnetic resonance imaging (MRI) has the ability to display the From the Departments of Diagnostic Radiology and Internal Medicine, Rheumatology Section, University Hospital, Uppsala, Sweden. Supported by a grant from the Swedish Medical Research ouncil. H. hlstrom, MD: Department of Diagnostic Radiology; N. Feltelius, MD: Department of Internal Medicine; R. Nyman, MD: Department of Diagnostic Radiology; R. Hallgren, MD: Department of Internal Medicine. ddress reprint requests to H. hlstrom, MD, Department of Diagnostic Radiology, kademiska sjukhuset, University Hospital, S Uppsala, Sweden. Submitted for publication pril 13, 1990; accepted in revised form July 27, hyaline cartilage in peripheral joints and has therefore been used in the detection of various pathologic joint conditions (4-6). MRI is also more efficient than T and conventional radiography in discriminating between different soft tissue lesions, such as fibrotic and inflammatory tissue (7). Until now, only preliminary reports concerning the diagnostic value of MRI in inflammatory diseases of the sacroiliac joints have been available (63). The aim of this study was to evaluate MRI characteristics and the diagnostic sensitivity of MRI in patients with sacroiliitis. The results were compared with findings obtained by T and conventional radiography. PTIENTS ND METHODS Twenty-seven patients (18 men and 9 women) with symptoms suggestive of sacroiliitis were evaluated by MRI, T, and conventional radiography. The mean age of the patients was 37 years (range years). Eleven healthy hospital staff members and medical students with a mean age of 31 years (range years) were examined by MRI and served as controls. The clinical investigation included an evaluation of lumbar spine mobility (Schober test), chest expansion (fourth intercostal space), and estimation of sacroiliac pain (directly by palpation of the sacroiliac joint and indirectly by forced abduction of the hip in flexion with the pelvis fixed [Patrick s test]). The laboratory assessment of inflammatory activity included measurement of the erythrocyte sedimentation rate (ESR) (Westergren) and serum concentrations of haptoglobin, -reactive protein (RP), and Ig. These were determined at the Department of linical hemistry, University Hospital, Uppsala. HL-27 tissue typing was performed at the Department of linical Immunology, University Hospital, Uppsala. The MRI examinations were performed in a superconductive unit (0.5T Magnetom; Siemens, Erlangen, FRG). Double-echo, multislice, and spin-echo techniques were rthritis and Rheumatism, Vol. 33, No. 12 (December 1990)

2 1764 HLSTROM ET L used with a repetition time (TR) of 2,000 milliseconds and echo times (TE) of 30 ms and 90 ms. Single-echo techniques were also used with TRiTE of and 1, (phase contrast). The number of acquisitions was 1 for 2,000130, 2,000/90, and 1,500137, and 2 for The acquisition matrix was 256 X 256 for and 1,500/37, and 128 X 256 for 2,000/30 and 2, xial slices with a thickness of 7 mm and an interslice gap of I.4 mm were recorded. oronal images were also recorded with TRITE of spine coil (elliptical surface coil measuring 125 x 230 mm, mounted in a mattress) was placed over the sacrum and used in all examinations. The phase-contrast sequence is a normal spin-echo sequence with a delayed data acquisition (7 ms) causing protons in water and hydrocarbon protons in fat to be phase shifted (9,lO). Tissue containing only fat or water protons will then be displayed with a high signal intensity, while mixed tissue will have a reduced signal intensity. The T examinations were performed with a Siemens DR 2 unit. ontiguous, 4-mmthick slices of the sacroiliac joint were obtained with a nontilted gantry. onventional radiography included a posteroanterior view of the pelvis and oblique views of the sacroiliac joints. onventional radiographs were evaluated together with the corresponding T images, and pathologic findings in each case were rated on a 04 scale according to the radiologic criteria for sacroiliitis (1 11, where 0 = normal, 1 = suspicious changes, 2 = minimal abnormality, 3 = unequivocal abnormality, and 4 = total ankylosis. The T images and radiographs were considered to reveal sacroiliitis if bony ankylosis, sclerosis on both sides of the joint, cortical erosions, or irregular joint space narrowing was present. If only isolated iliac sclerosis was present, the images were interpreted as normal (3). In the MRI, the variations in signal intensity in the joint space, the surrounding bone, and the bone marrow adjacent to the joint were evaluated subjectively in each sequence. The signal intensity in all pulse sequences was described as high when it was equal to that of fat, low when it was equal to or lower than that of muscle, and intermediate when it was between that of fat and muscle. ny MRI findings in the area of the sacroiliac joint that were not found in any of the controls were regarded as abnormal. ll images from each patient were evaluated and compared by 2 radiologists (H and RN) who worked together and were not aware of the clinical condition of the patients. The T and MRI were compared at each corresponding level and abnormalities were noted. RESULTS linical and laboratory data on the 27 patients are summarized in Table 1. ll patients had sacroiliac pain. Only 9, however, experienced sacroiliac joint pain in objective tests. Increased inflammatory activity, defined by an elevated ESR (>15 mmlhour) or serum haptoglobin level (>2.0 gditer), was present in 9 of 27 patients. oth conventional radiography and T of the sacroiliac joints showed that I1 of 27 patients fulfilled the radiologic criteria necessary for a Table 1. linical and laboratory data of 27 patients with sacroiliac pain* ESR, mm/hour (<IS) Haptoglobin, gmlliter ( ) RP, mghiter (<lo) Serum Ig, gdliter ( ) Schober test, cm (<3) Thoracic expansion, cm (6-8) Mean rt SEM 13 rt ? f * Normal values or ranges are shown in parentheses. ESR = erythrocyte sedimentation rate; RP = -reactive protein. definite diagnosis of sacroiliitis, i.e., radiologic score of 3 (10 patients) or 4 (1 patient) (11). In 2 patients, minimal changes (score of 2) were observed by both conventional radiography and T. hanges suspicious of sacroiliitis (score of 1) were noted in 4 patients by conventional radiography and in 1 patient by T. MRI of the sacroiliac joint. y MRI, 13 of the 27 patients were considered to have normal sacroiliac joints, as defined by comparison with the controls. The normal sacroiliac joint space had a symmetric and homogeneous signal intensity in all sequences (Figure 1). The typical signal intensity pattern of the joint space was an intermediate signal in the T1-weighted and the TZweighted images and a high signal in the phase-contrast image. The joint space was barely visible in 2 controls as well as in 3 patients who were considered to have normal findings on MRI examinations. The corresponding T examinations of these patients showed a normal but narrow joint space. mong the controls, the region corresponding to the subchondral bone cortex had a low signal intensity in all sequences. The periarticular bone marrow usually had a homogeneous signal intensity, which was intermediate in the T1-weighted and the TZweighted images and low in the phase-contrast image. However, in 2 of the older controls, a patchy pattern with small areas of high signal intensity in all sequences, which corresponded to fat, was observed in the bone marrow on the iliac side. In 2 controls, a relatively broad zone of low signal intensity was observed in all sequences adjacent to the joint space on the iliac side. similar zone was seen in 2 female patients and corresponded to a subchondral sclerotic zone seen on T images. These patients were considered to have normal findings on MRI. Fourteen of the 27 patients were diagnosed as having abnormalities of the sacroiliac joints when evaluated by MRI. The 13 patients who had radiologic scores of 2 4 on conventional radiography had the same score when evaluated by T; all 13 of these patients also had pathologic findings on MRI. Patients

3 MRI OF SROILIITIS 1765 Figure 1. Magnetic resonance images of the caudal area of the sacroiliac joints (arrows) of a healthy control subject., Intermediate signal intensity is seen from the joint space and the periarticular iliac bone marrow in a coronal TI-weighted image (repetition time/echo time [TR/TE] 500/22) and, in an axial T2-weighted image (TRKE 2,000/90)., xial phase-contrast image (TmE 1,500/37), showing high and low signal intensity at the joint space and iliac bone marrow, respectively. Subchondrally in all images, there are thin zones with signal void corresponding to the cortex. Figure 2. xial magnetic resonance images and a computed tomography (T) image of the sacroiliac joints of a 17-year-old patient with suspected sacroiliitis, but normal findings on T and conventional radiography. Symmetric bands of type I lesions (arrows) in, the T1-weighted image (repetition time/echo time [TRRE] 500/22), showing low signal intensity, and in, a phase-contrast image (TRfF'E 1,500/37), showing high signal intensity, are seen in periarticular bone marrow., normal T image at the same level.

4 1766 HLSTROM ET L Figure 3. xial magnetic resonance images and a computed tomography (T) image of the sacroiliac joints of a 26-year-old patient with sacroiliitis. Type I lesions (arrows), diffusely distributed in the right dorsal periarticular bone marrow on both sides of the joint, are seen, with low signal intensity in a T1-weighted image (repetition time/echo time [TR/TE] 500/22) and, with high signal intensity in a phase-contrast image (TR/TE 1,500/37)., T image at the same level, showing erosions in the right joint, but only on the iliac side, corresponding to the type I lesion in the iliac bone marrow. There are erosions corresponding to type I lesions on the left side of this image. with a radiologic score of 1 on conventional radiography (n = 4) or T (n = 1) showed no apparent abnormalities on MRI. One patient with normal findings on T and on conventional radiography had pathologic findings on MRI (Figure 2). Two types of pathologic lesions were seen in the periarticular region when evaluated by MRI; they are referred to below as type I and type I1 lesions. Type 1 lesions, which were seen in 5 of 14 patients with pathologic findings by MRI, were characterized by a low signal intensity in the TI-weighted image and a high signal intensity in both phase-contrast and T2- weighted images (Figure 2). These lesions were localized in patchy areas close to the joint space and/or were more or less diffusely distributed in the periarticular bone marrow (Figures 3 and 4). They were associated with erosions seen by T in 4 of 5 patients (radiologic scores of 2 or 3). In I of the patients with a type 1 lesion, no corresponding abnormalities were seen on T images (Figure 2). This patient was 17 years old, was HL-27 positive, and had a family history of ankylosing spondylitis among first-degree relatives. In another patient, type I lesions were noted on both sides of the joint, while T of the same area revealed erosions only on the iliac side (Figure 3). Type I1 lesions, which were seen in 13 of 14 patients with pathologic findings by MRI, were characterized by a low signal intensity in all sequences (Figures 4 and 5). These lesions were associated with erosions and more or less extensive sclerotic changes seen on T scans. In 3 patients with more extensive sclerosis and erosions visualized by T, the individual erosion could not be demarcated as a type 11 lesion by MRI. In 4 patients, some erosions were associated with type I1 lesions, while others were associated with type I lesions. In 1 patient with total ankylosis, type I1 lesions corresponded to the obliterated joint space. The joint space close to the areas of lesions was either irregularly delineated or diminished, while the joint space in areas not affected by lesions appeared normal (Figure 4). nkylosis was well demonstrated by both MRI and T. In 9 of the 14 patients with abnormal findings on MRI, a thin zone of high signal intensity in all sequences was seen in the periarticular bone marrow on the iliac side of the joint, indicating an accumulation of fat (Figures 4 and 5). This distribution of fat differed from the patchy distribution of fat found in the bone marrow among some of the older controls. T evaluation of all patients with this periarticular fat accumulation demonstrated unequivocal signs of sacroiliitis: erosions in 8 patients, extensive sclerosis in 1 patient, and partial-to-total ankylosis in 4 patients. Type I1

5 MRI OF SROILIITIS 1767 Figure 4., xial TI-weighted (repetition time/echo time [TR/TEl 500/22) and, phase-contrast (TRfTE 1,500/37) magnetic resonance images (MRI) of the sacroiliac joints of a patient with ankylosing spondylitis, showing subchondral type I1 lesions and fat accumulation in the juxtaarticular bone marrow on the right side. Note the irregularly delineated joint space in the right joint close to the lesions (right arrows). On the left side, the signal intensity of the joint space is more homogeneous, and type I lesions localized to patchy areas are seen dorsally (left arrows)., The corresponding computed tomography image, showing erosions associated with the lesions in the MRI. Figure 5. xial magnetic resonance images (MRI) and a computed tomography (T) image of the sacroiliac joints of a patient with sacroiliac pain, high inflammatory activity (erythrocyte sedimentation rate 108 mm/hour), and confirmed ankylosing spondylitis. Type I1 lesions (arrows) are seen with low signal intensity in, a TI-weighted image (repetition time/echo time [TR/TE] 500/22) and, a T2-weighted image ( TWE 2,000/90)., The corresponding T image, showing erosions consistent with those seen in the MRI. In the MRI, a region with high signal intensity indicating fat accumulation is seen in the periarticular iliac bone marrow.

6 1768 HLSTROM ET L lesions, but not type I lesions, were associated with this periarticular fat accumulation. One patient had type I1 lesions with periarticular fat accumulation in one joint, but had type I lesions and no fat accumulation on the other side; there was no apparent difference between the joints when evaluated by T (Figure 4). No correlation was found between clinical or laboratory data (Schober test, thoracic expansion, disease duration, patient age, ESR, serum haptoglobin, RP, or serum Ig) and any type of lesions seen by MRI. DISUSSION In this study of a consecutive series of 27 patients with symptoms compatible with sacroiliitis, the majority (59%) fulfilled the New York criteria for ankylosing spondylitis (I). bnormal findings in the sacroiliac joints were seen by MRI in 14 of the 27 patients. ll patients with more distinct abnormalities seen by conventional radiography and T, i.e., radiologic scores of 2-4 (1 I), showed distinct abnormalities when evaluated by MRI. However, joint abnormalities suggestive of sacroiliitis seen by conventional radiography or more discreet erosions seen by T were not identified by MRI. The more sensitive technique was expected to reveal more early pathologic changes, since it was reasonable to assume that some patients who did not fulfill the diagnostic criteria for ankylosing spondylitis at the time of the study might later be found to have the disease. This assumption is based on the experience that radiologic signs of sacroiliitis may appear a long time after the first presentation of clinical symptoms and signs of inflamed sacroiliac joints. The frequency of the transplantation antigen HL-27 is highly increased in ankylosing spondylitis. Thus, the high prevalence (94%) of HL-27 in our patients further supports the suspicio$ that early sacroiliitis may have been underestimated. The poor sensitivity of clinical tests in sacroiliac joint pain is illustrated by the fact that only 9 of 27 patients had positive findings on tests for pain at the time of the study. The sensitivity of MRI for detecting early pathologic changes of the sacroiliac joints for purposes of diagnosis might be improved with more suitable surface coils and a higher field strength than those used in this study. Furthermore, the use of gadolinium diethylenetriamine pentaacetic acid should also improve the sensitivity, since it is well known that the signal intensity of acutely inflamed tissue is enhanced after intravenous injection of this compound, a procedure that facilitates the early diagnosis of rheumatoid arthritis (12,13). Irrespective of the diagnostic potential of MRI, other features of the technique may be of clinical value in the evaluation of affected sacroiliac joints, and may also increase our knowledge of the pathophysiology of the disease process in the sacroiliac joint. Visualization of articular cartilage in the sacroiliac joint can only be accomplished indirectly when using conventional radiography and T. In contrast, with MRI, the cartilage can be visualized directly (6). The signal intensity pattern of the sacroiliac joint space in our healthy controls was probably due to the presence of cartilage. Direct visualization of the joint space, which was hampered in patients and controls who had a narrow sacroiliac joint space, might be improved with better resolution techniques. The observation that the signal intensity of the joint space was apparently normal in parts of the sacroiliac joint adjacent to areas with lesions seems to be essential to the histopathologic concept of a patchy distribution of the inflammatory changes in cartilage in HL-27-associated sacroiliitis (14). The different signal intensity patterns of type I and type I1 lesions indicate differences in their water content. This observation suggests that MRI has the potential to differentiate lesions with a higher water content (type I lesion) due to inflammatory edema from lesions with a reduced water content (type I1 lesion) due to invasive fibrotic tissue or sclerosis. This interpretation of the nature of the lesions demonstrated by MRI is supported by the findings of an open biopsy study of patients with early sacroiliitis, which indicated that the early histopathologic changes occurred in the subchondral bone (15); the earliest subchondral lesions appeared to be inflammatory and were followed by fibrous tissue proliferation. When evaluating the effects of disease-modifying drugs, it may be particularly valuable to follow these different lesions, since they are likely to be invariably progressive or may even be partly reversible. The finding that the periarticular type I lesion of the bone marrow (Figures 2 and 3) may appear with no subchondral erosions suggests that early inflammatory processes in sacroiliac joints may be localized to the subcortical areas. The observation that some patients demonstrated periarticular fat accumulation in the bone marrow, especially on the iliac side, has no apparent pathophysiologic explanation. However, it seems to reflect a later stage of inflammatory joint disease, since it was associated only with type I1 lesions and with more severe involvement of the sacroiliac joint as seen on T (radiologic scores of 3 and 4). The observed fat accumulation supports the concept that the disease process in sacroiliitis involves subcortical areas and

7 MRI OF SROILIITIS 1769 may be due to an ongoing effect of inflammatory products on local fat metabolism (16,17). similar type of penarticular fat accumulation in vertebral bone marrow adjacent to degenerated discs, shown by MRI, has recently been reported (18). The pathologic process of sacroiliac joint inflammation is poorly understood due to the limited number of direct of studies of this joint. Previous studies have been mainly performed on autopsy specimens from patients with longstanding disease. Some investigators have described pannus formation ( 19), while others have not (20). It has been proposed that capsular ossification is the primary cause of sacroiliac joint inflammation and that enchondrdl ossification occurs later (21). Others have claimed that subchondral cartilaginous metaplasia underlies the development of ankylosis (22). Since our understanding of the histopathologic processes involved has been limited (23), methods for evaluating therapeutic evaluation have been poorly developed. It appears at present that pathologic changes of sacroiliitis cannot be reorganized at an earlier stage with the use of MRI than with conventional radiography or T. However, MRI seems to have the potential for providing new insights into the pathologic events in sacroiliitis, due to its unique ability to identify and differentiate certain abnormalities that occur during the local disease process. This potential of MRI may also be of clinical value in evaluating therapeutic response in sacroiliitis. The demonstration of subchondral lesions and periarticular bone marrow changes in sacroiliitis by MRI should be considered in future attempts to explore the pathogenesis of this inflammatory joint disease REFERENES ennett PH, Wood PHN: Population Studies of the Rheumatic Diseases. 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