COMPUTED TOMOGRAPHY IN THE DIAGNOSIS OF EARLY ANKYLOSING SPONDYLIT-IS

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1 COMPUTED TOMOGRAPHY IN THE DIAGNOSIS OF EARLY ANKYLOSING SPONDYLITIS ADEL G. FAM, JOEL D. RUBENSTEIN, HYACINTH CHINSANG, and FRANCES Y. K. LEUNG Computed tomography (CT) was compared with plain radiography and quantitative sacroiliac (SI) scintigraphy in 28 patients with early ankylosing spondylitis (AS) of 510 years duration. Compared with conventional radiography, CT improved delineation of the SI joints and revealed more abnormalities and higher grades of sacroiliitis; this was significant in patients with early AS of 13 years duration. Quantitative sacroiliac scintigraphy showed higher SI joint:sacrum ratios of radioisotope uptake in patients with AS compared with controls. However, its diagnostic usefulness was limited by the frequency of inconsistent results and the lack of specificity. CT examination of the SI joints may be a useful adjunct in the diagnosis of early AS. The clinical diagnosis of ankylosing spondylitis (AS) is largely based upon the radiologic demonstration of sacroiliitis (1,2). However, early radiographic changes are often subtle and subject to considerable observer error (36). Other imaging techniques have been used in the evaluation of sacroiliac (SI) joints, including special views of SI joints (7,8), conventional From the Division of Rheumatology, Department of Medicine, and the Department of Radiology, Sunnybrook Medical Centre, University of Toronto, Toronto, Ontario, Canada. Supported by a grant from the Sunnybrook Trust for Medical Research. Adel G. Fam, MD, FRCP(C): Associate Professor of Medicine; Joel D. Rubenstein, MD, FRCP(C): Assistant Professor of Radiology; Hyacinth ChinSang, MD, FRCP(C): Assistant Professor of Radiology; Frances Y. K. Leung, MD, FRCP(C): Lecturer in Medicine. Address reprint requests to Adel G. Fam, MD, Division of Rheumatology, Sunnybrook Medical Centre, 2075 Bayview Avenue, 'Toronto, Ontario, Canada M4N 3M5. Submitted for publication July 19, 1984; accepted in revised form February 8, tomography (9, lo), quantitative sacroiliac scintigraphy (QSS) (1115), and more recently, computed tomography (CT) (4,1621). The role of CT in the diagnosis of sacroiliitis is controversial. Recent studies indicate that CT is more sensitive and accurate than plain radiography in the evaluation of inflammatory sacroiliitis (4,8,16,1921). However, other studies have not found CT to be superior in the detection of sacroiliitis (17,18). This study was designed to define the role of CT in the evaluation of sacroiliitis in patients with early symptomatic AS. Our results indicate that CT is useful in clarifying suspected SI joint abnormalities in those patients whose plain film findings are still equivocal. PATIENTS AND METHODS Patients. Between January 1982 and March 1984 we studied 28 consecutive patients with inflammatory low back pain of 5 10 years duration and clinical findings suggestive of AS. The group consisted of 22 men and 6 women with a mean age of 29.7 years (range 2143). AS was diagnosed in patients who were 1840 years of age at the time of onset of symptoms and had a typical history of chronic inflammatory back pain (22) in association with 1 or more of the following signs: tender SI joints, positive results of SI joint stress test (23), limited lumbar spine movement (modified Schober's test) (24), or restricted chest expansion. Inflammatory back pain was defined as the insidious onset of lumbar or thoracic pain for 2 3 months, that was improved by movement or light exercise, was aggravated by rest, and was associated with 230 minutes of morning back stiffness (22). We excluded those patients who fulfilled criteria for rheumatoid arthritis, metabolic bone disease, or other types of spondylarthropathy secondary to psoriasis, Reiter's syndrome, or inflammatory bowel disease. A standard anteroposterior radiograph of the SI joints with a 20" caudal tube angle, QSS, and CT of the SI joints were performed on all AS patients. For QSS, ratios of peak counts over each SI joint:peak sacral count, or SI:S Arthritis and Rheumatism, Vol. 28, No. 8 (August 1985)

2 CT IN EARLY AS 93 1 Table 1. Clinical and laboratory findings in 28 patients with ankvlosinrr srrondvlitis Characteristic' Number of patients Duration of back symptoms 53 years 15 >310 years 13 Morning back stiffness 230 minutes duration 26 Diminished chest expansion 8 Decreased lumbar mobility 15 SI joint tenderness 15 Positive results on SI joint stress test 9 Peripheral arthritis 9 Manubriosternal arthritis 3 Intis 3 Elevated ESR 8 HLAB27 25 * SI = sacroiliac; ESR = erythrocyte sedimentation rate, ratios, were cakuiated 3 hours after intravenous injection of 15 mci of *"Tclabeled methylene diphosphonate. Nonsteroidal antiinflammatory drugs were withheld for at least 10 days prior to scintigraphy. CT and plain radiographs of the SI joints were obtained on the same day in 12 patients. The interval of time between examinations was less than 3 months in 11 patients, and within 36 months in the remaining 5. Six to eight contiguous 5 mmthick CT sections were obtained through the SIjoints on a GE 8800 scanner with no gantry angulation. The correct anatomic level was localized on the scout view prior to CT examination, and only those sections through the synovial compartment of the joints (4) were assessed. Controls. Ten control patients (8 men and 2 women), with a mean age of 29. I years (range 1741) and no history of back pain, underwent pelvic radiography and CT for reasons other than arthritis (e.g., lymphoma, metastases). Computed Tomography Table 2. Comparison of computed tomography (CT) and plain radiography in the detection of sacroiliitis* ~~ ~ ~ No. of cases Control patients (n = 10) Agreement between methods Patients with AS (n = 28) 10 Agreement between methods 26 CT falsenegative result 1 Radiography falsenegative result 1 * Agreement statistic (kappa) = Fifty additional control patients underwent QSS. This group consisted of 10 patients with mechanical \ow back pain (9 men and 1 woman, mean age 29.5 years, age range 2938; all but 1 were HLAB27 negative) and 40 patients without back pain (23 men and 17 women, mean age 56.3 years, age range 3086) who had whole body bone scintigraphs for reasons other than suspected arthritis (e.g., metastatic disease or fracture). All radiographs and CT scans were examined independently by 3 observers (2 radiologists and 1 rheumatologist) who had no knowledge of the clinical diagnoses, HLA type, or scintigraphic findings. Each SI joint was graded separately using the New York criteria (I): grade 0 = normal; grade 1 = suspicious for erosions or sclerosis; grade 2 = mildly abnormal with definite erosions or sclerosis but without alteration In joint width; grade 3 = moderately abnormal with erosions, iliac and sacral sclerosis, joint space narrowing or widening and/or partial ankylosis; grade 4 = severe abnormality with complete ankylosis. The independent scores were reviewed, and for those on which the observers disagreed (5% of the initial readings), the radiographs and CT scans were reexamined by the 3 observers together, and a reconciled grade was recorded. Analysis of data. Data were anasyzed by Cohen's kappa agreement coefficient statistics (25), the chisquare test of independence, and Student's ttest of the means. A P level <OM was arbitrarily chosen as indicative of significant differences. % + Cra I 47 I Kappa statistic = 0.83 Figure 1. Interrater agreement statistic (kappa) between computed tomography and plain radiography in the detection of sacroiliitis in 28 ankylosing spondylitis patients and 10 control patients. Numbers are the total number of sacroiliac joints positive or negative for sacroiliitis, as evidenced by that technique. RESULTS Clinical findings. Table 1 summarizes the clinical and laboratory findings or the 28 patients with AS. By definition, all 28 patients had back symptoms for (10 years. Fifteen patients had back symptoms for 5 3 years, including 6 patients who were evaluated within 1 year of symptom onset. All but 3 patients were HLA 327 positive. The most common objective findings were tenderness of the SI joints and slight limitation of lumbar spine movements. Chest expansion was limited in 8 patients, most of whom had symptoms for >3 years. Nine patients had peripheral arthritis, and 3 had iritis. Manubriosternal arthritis was seen in 3 patients and was the presenting symptom in 1.

3 932 FAM ET AL Figure 2. A, Plain radiograph of the sacroiliac (SI) joints, showing no evidence of sacroiliitis. B, Computed tomography image through the synovial part of the SI joints of the same patient, obtained 3 days after the plain films, demonstrating sclerosis and erosions in right SI joint (arrows). The left SI joint shows irregular articular surfaces.

4 CT IN EARLY AS 933 Table 3. Comparison of plain radiography and computed tomography in the grading of sacroiliitis in 28 patients with ankylosing soondvlitis* Sacroiliitis grade Plain radiography (56 joints) Computed tomography scans (56 joints) * Pooled results of 3 observers. Numbers are the total number of joints positive for that grade. Differences not statistically significant (P < 0.09). CT findings. In the control patients and in the patients with AS, there was good correlation between interpretations of sacroiliitis from plain radiographs and from CT (Figure 1). CT did not significantly increase the probability of detecting sacroiliitis, compared with plain radiography (Table 2). However, in 5 SI joints, CT demonstrated changes of sacroiliitis that were not evident radiographically (Figure 1). This included 1 AS patient who had a positive CT result but a negative result on plain films (Table 2 and Figures 2A and B). One patient had unilateral grade 1 sacroiliitis by radiography... but a negative.....~.~~ CT result (Table 2). Plain radiographs and CT were'negative for sacroiliitis in all 10 control patients (those without history of back pain undergoing radiography and CT for lymphoma, metastases, etc.). Three CT scans showed focal iliac sclerosis that was not visible on plain radiographs: this finding has been recently described in CT of normal SI joints (21). In patients with AS, CT revealed more SI joint abnormalities (erosions, sclerosis, and joint space narrowing or widening) and higher grades of sacroiliitis, compared with conventional radiography (Table 3), but the differences were not statistically significant (x2 = 6.53, 3 df, P < 0.09). However, in patients with early AS, there was a significant change in sacroiliitis grade when evaluated by CT (Table 4). Eleven of 15 patients (17 of 30 SI joints) with disease of 53 years had a higher grade of sacroiliitis shown on CT, compared with plain films (Figures 3A and B). In the group with disease duration of >3 years, only 6 of 13 patients, or 7 of 26 SIjoints, demonstrated a change in grade (x2 = 3.89, 1 df, P < 0.05 versus patients with disease of 13 years). Therefore, CT was useful in patients with disease duration of 13 years and normal or equivocal results on plain films, but was of littie additional value in interpreting advanced grades of sacroiliitis (Figures 4A and B). Table 4. Comparison of computed tomography (CT) and plain radiography in the detection of sacroiliitis, according to disease duration Duration of ankylosing spondylitis 53 years >3 years (15 patients) (13 patients) Stable, CT and plain films showed same grade of sacroiliitis Change, CT showed higher grade 17 7* of sacroiliitis than did plain films Total number of sacroiliac joints * P < 0.05 compared with patients with disease duration of 53 years. Quantitative sacroiliac seintigraphy. Patients with AS had significantly higher SI : S ratios compared with nonrheumatic disease controls (P < 0.001) and compared with those with mechanical low back pain (P < 0.003), but there was frequent overlap between these groups (Table 5 and Figure 5). The SI:S ratios were significantly higher in patients with early AS of 53 years duration compared with those with AS for >3 years (P < 0.03) (Table 5 and Figure 5). DISCUSSION The diagnostic criteria for AS that are presently being used are too restrictive and are heavily dependent upon the detection of unequivocal radiologic evidence of sacroiliitis (1,2). Clinical diagnosis of early AS is often difficult because of the high incidence of back pain in the general population (26), the nonspecificity of objective findings (23,27), and because of difficulties in radiologic diagnosis of early inflammatory changes of the SI joints (36). The curved and oblique orientation of the SI joints, the overlying soft tissues, and the presence of unrelated degenerative changes (28,29) complicate the radiologic interpretation of inflammatory sacroiliitis (36). A number of diagnostic methods have been proposed as being superior to plain radiography in the evaluation of early sacroiliitis. These include special views of the SI joints (7,8), conventional tomography (9,10), QSS (1113, and CT (4,1621). However, special radiographic projections of the SI joints, including oblique views, have not been shown to significantly increase the accuracy of diagnosis of sacroiliitis (7,8). Although conventional tomography improves the definition of the SI joints, it is associated with high radiation exposure (9,lO).

5 934 FAM ET AL Figure 3. A, Plain radiograph of the sacroiliac (SI) joints, showing minimal bilateral iliac and sacral sclerosis. B, Computed tomography image of the SI joints of the same patient, obtained 22 days after the plain films, demonstrating irregular sclerosis, erosions, and pseudowidening of the right SI joint, and sclerosis and indistinct articular margins of the left SI joint. Quantitative sacroiliac scintigraphy revealed higher SI: S ratios in our patients with AS, particularly those with early disease of 53 years duration, compared with the controls. Although the probability of detecting sacroiliitis was increased in the presence of a high SI : S ratio, QSS was not consistently diagnostic in differentiating patients with AS from the control patients and from those with mechanical low back pain. These findings are in agreement with recent studies that have shown that radionuclide scanning of SIjoints

CT IN EARLY AS 935 Figure 4. Advanced (grade 3) sacroiliitis. A, Plain radiograph; B, Computed tomography image, showing large erosions and irregular sclerosis in both joints.

6 CT IN EARLY AS 935 Figure 4. Advanced (grade 3) sacroiliitis. A, Plain radiograph; B, Computed tomography image, showing large erosions and irregular sclerosis in both joints. is too nonspecific for effective diagnosis of inflammatory sacroiliitis (1316,30,31). CT of the SI joints is associated with low radiation exposure (16). The technique seems ideally suited to studying the curved, oblique SI joints in a transaxial plane, thereby minimizing interference from the overlying soft tissues and bony structures (4,16,17,21). The tomographic nature of CT images also enhances the definition of changes in the SI joint (20). Although it was not always possible to obtain simultaneous plain radiographs and CT scans in our patients, the interval of time between the 2 procedures was short and, in the majority of cases, did not exceed 3 months.

7 936 FAM ET AL P Y L * t w t I. Table 5. Sacroiliac joint: sacrum (SI: S) ratios in 40 control patients, 10 patients with mechanical low back pain, and 28 patients with ankylosing spondylitis (AS), according to results of quantitative sacroiliac scintigraphy Mechanical AS patients low back Disease duration Disease duration Controls pain All 53 years >3 years No. of SI joints Mean SI:S ratio * 1.55t 1.40 SD ' '0.27 SEM * P < compared with controls, P < compared with patients with mechanical low back pain. t P < 0.03 compared with AS patients with disease duration >3 years. " "... : " I CONTROLS MECHANICAL ANKYLOIINO ANKYLOSINO (N=*Ol BACK SCONDYLITIS SPONDYLITIS PAY <3 YEARS >a YEARS (N.20) (N=30) (N=26) Figure 5. Results of quantitative sacroiliac scintigraphy, showing sacroiliac (SI) joint:sacrum uptake ratios and mean values (horizontal bars) for 40 control patients, 10 patients with mechanical back pain, and 28 patients with ankylosing spondylitis (grouped according to disease duration). Each SI joint is considered individually. The upper and lower bars for patient controls represent the 95% confidence limits for this group. See Patients and Methods for details.. CT images showed better delineation of the SI joints and revealed more abnormalities and higher grades of sacroiliitis, particularly in patients with early AS, than did plain radiographs. Although CT did not significantly increase the diagnostic capability beyond that with plain radiography, mild SI joint abnormalities were more clearly evident on CT. This allowed for greater confidence and accuracy of diagnosis, particularly in patients who did not have limited chest expansion, limited movement of the lumbar spine, and definite radiographic changes at the SI joints, all of which are necessary for a diagnosis of AS by established criteria. However, the technique was of no added value in interpreting higher grades of sacroiliitis. Therefore, CT cannot be recommended for the routine assessment of inflammatory sacroiliitis (32). Rather, it should be reserved for the few patients in whom the diagnosis remains in doubt after results of clinical and radiographic evaluations have been reviewed. CT would be a reasonable next step in patients with an atypical presentation or incompletely expressed AS who fail to manifest overt erosive and sclerotic radiographic changes at the SI joints. It has been established that AS may be symptomatic for years before sacroiliitis becomes manifest on radiographs (33,34). Recognition of the disease in its early stages will allow for patient education, institution of correct therapy including high doses of nonsteroidal antiinflammatory drugs, and avoidance of inappropriate investigative procedures (35). We believe that CT of the SI joints may be a useful adjunct in the evaluation of inflammatory sacroiliitis of recent onset and, hence, in the diagnosis of early AS. ACKNOWLEDGMENTS The authors wish to thank Dr. John Szalai and Marko Katic for help with statistical analysis, and Sylvia Fader for secretarial assistance.

CT IN EARLY AS 937 1. Bennett PH, Wood PHN: Population Studies of the Rheumatic Diseases: Proceedings of the Third International Symposium, New York, June 1966.

8 CT IN EARLY AS Bennett PH, Wood PHN: Population Studies of the Rheumatic Diseases: Proceedings of the Third International Symposium, New York, June Amsterdam, Excerpta Medica, 1968, pp , Van der Linden S, Valkenburg HA, Cats A: Evaluation of diagnostic criteria for ankylosing spondylitis: a proposal for the modification of the New York criteria. Arthritis Rheum 27:361368, MacRae IF, Baslock DI, Wright V: Grading of films for sacroiliitis in population studies. Ann Rheum Dis 30: 5866, Lawson TL, Foley WD, Carrera GF, Berland LL: The sacroiliac joints: anatomic, plain roentgenographic, and computed tomographic analysis. J Comput Assist Tomogr 6:307314, Hollingsworth PN, Cheah PS, Dawkins RL, Owen ET, Calin A, Wood PHN: Observer variation in grading sacroiliac radiographs in HLAB27 positive individuals. J Rheumatol 10:247254, Forrester DM, Hollingsworth PN, Dawkins RL: Difficulties in the radiographic diagnosis of sacroiliitis. Clin Rheum Dis 9:323332, Wasner C, Kraines RG, Kaye RL: Oblique view radiographs in the diagnosis of sacroiliitis (abstract). Arthritis Rheum 22:671, Ryan LM, Carrera GF, Lightfoot RW Jr, Hoffman RG, Kozin F: The radiographic diagnosis of sacroiliitis: a comparison of different views with computed tomograms of the sacroiliac joint. Arthritis Rheum 26: , Wilkinson M, Meikle JA: Tomography of the sacroiliac joints. Ann Rheum Dis 25:433440, De Smet AA, Gardner JD, Lindsley HB, Goin JE, Fritz SL: Tomography for evaluation of sacroiliitis. AJR 139:577581, Russell AS, Lentle BC, Percy JS: Investigation of sacroiliac disease: comparative evaluation of radiological and radionuclide techniques. J Rheumatol 2:4551, Namey TC, McIntyre J, Buse M, LeRoy EC: Nucleographic studies of axial spondarthritides. I. Quantitative sacroiliac scintigraphy in early HLAB27associated sacroiliitis. Arthritis Rheum 20: , Goldberg RP, Genant HK, Shimshak R, Shames D: Applications and limitations of quantitative sacroiliac joint scintigraphy. Radiology 128:683686, Ho G Jr, Sadovnikoff N, Malhotra CM, Claunch BC: Quantitative sacroiliac joint scintigraphy: a critical assessment. Arthritis Rheum 22:837844, Esdaile JM, Rosenthall L, Terkeltaub R, Kloiber R: Prospective evaluation of sacroiliac scintigraphy in chronic inflammatory back pain. Arthritis Rheum 23: , Carrera GF, Foley WD, Kozin F, Ryan L, Lawson TL: CT of sacroiliitis. AJR 136:4146, Borlaza GS, Seigel R, Kuhns LR, Good AE, Rapp R, Martel W: Computed tomography in the evaluation of sacroiliac arthritis. Radiology 139:437440, Khan MA, Miron SD, Kushner I, Ballou SP, Wiesen EJ, Bellon EM: The comparative value of standard radiography, quantitative scintigraphy and computerized tomography in sacroiliitis (abstract). Arthritis Rheum (suppl) 24:S119, Kozin F, Carrera GF, Ryan LM, Foley D, Lawson T: Computed tomography in the diagnosis of sacroiliitis. Arthritis Rheum 24: , Carrera GF: Computed tomography in sacroiliitis. Clin Rheum Dis 9:403415, Vogler JB, Brown WH, Helms CA, Genant HK: The normal sacroiliac joint: a CT study of asymptomatic patients. Radiology 151:433437, Calin A, Porta J, Fries J, Schurman DJ: Clinical history as a screening test for ankylosing spondylitis. JAMA 237: , Russell AS, Maksymowych W, LeClercq S: Clinical examination of the sacroiliac joints: a prospective study. Arthritis Rheum 24: , Moll JMH, Wright V: Normal range of spinal mobility: an objective clinical study. Ann Rheum Dis 30:381386, I Fleiss JL: The measurement of interrater agreement, Statistical Methods for Rates and Proportions. Second edition. New York, John Wiley & Sons, 1981, pp Grabias SL, Mankin HJ: Pain in the lower back. Bull Rheum Dis 30: , Blower PW, Griffin AJ: Clinical sacroiliac tests in ankylosing spondylitis and other causes of low back pain2 studies. Ann Rheum Dis 43:192195, Cohen AS, McNeill JM, Calkins E, Sharp JT, Schubart A: The normal sacroiliac joint. AJR , Resnick D, Niwayama G, Goergen TG: Comparison of radiographic abnormalities of the sacroiliac joint in degenerative disease and ankylosing spondylitis. AJR 128: , Spencer DG, Adams FG, Horton PW, Buchanan W: Scintiscanning in ankylosing spondylitis: a clinical, radiological and quantitative radioisotopic study. J Rheumatol 6: , Snaith ML, Calvin SEJ, Short MD: The value of quantitative radioisotope scanning in the differential diagnosis of low back pain and sacroiliac disease. J Rheumatol 9~435440, Calin A: Abuse of computed tomography (letter). Arthritis Rheum 25: , Parry CBW: Management of ankylosing spondylitis. Proc R SOC Med 59:619623, Bluestone R: Ankylosing spondylitis, Arthritis and Allied Conditions. Ninth edition. Edited by DJ McCarty. Philadelphia, Lea & Febiger, 1979, pp Ankylosing spondylitis and its early diagnosis (editorial). Lancet , 1977

COMPUTED TOMOGRAPHY IN THE DIAGNOSIS OF SACROILIITIS

COMPUTED TOMOGRAPHY IN THE DIAGNOSIS OF SACROILIITIS 1479 COMPUTED TOMOGRPHY IN THE DIGNOSIS OF SCROILIITIS FRNKLIN KOZIN, GUILLERMO F. CRRER, LWRENCE M. RYN, DENIS FOLEY, and THOMS LWSON Computed tomography (CT) and conventional radiography of the sacroiliac