Skeletal Radiol (1999) 28:196±201

� International Skeletal Society 1999 A R T I C L E

Michael J. BattistoneB.J. ManasterDomenic J. RedaDaniel O. Clegg

The prevalence of sacroiliitis inpsoriatic arthritis: new perspectives from a large,multicenter cohortA Department of Veterans Affairs Cooperative Study

Received: 21 October 1998Revision requested: 11 December 1998Revision received: 19 January 1999Accepted: 22 January 1999

M.J. Battistone, M.D. ())D.O. Clegg, M.D.Division of Rheumatology,University of Utah Medical Center,50 North Medical Drive, Salt Lake City,UT 84132, USA

M.J. Battistone, M.D. ´ D.O. Clegg, M.D.Department of Medicine,Division of Rheumatology,Veterans Affairs Medical Center,Salt Lake City, Utah, USA

B.J. Manaster, M.D., Ph.D.Department of Radiology,Division of Musculoskeletal Imaging,Medical College of Virginia/VirginiaCommonwealth University,Richmond, Virginia, USA

D.J. Reda, M.S.Cooperative Studies Program CoordinatingCenter, VA Hospital, Hines, Illinois, USA

Abstract Objective. To determinethe prevalence of radiographic evi-dence of sacroiliitis in a large popu-lation of patients with psoriatic ar-thritis.Patients and design. Patients wererecruited from 15 clinical centers.This was part of a large, multicenterstudy of patients with an establisheddiagnosis of ankylosing spondylitis,psoriatic arthritis, or reactive ar-thritis. For this cohort, an estab-lished diagnosis of psoriatic arthritiswas required, with cutaneous mani-festations and involvement of atleast three appendicular joints. Atentry, patients were not selected forthe presence of axial involvement.Radiographs ± one anteroposteriorview of the pelvis and one obliqueview of each sacroiliac joint ± weregraded using the New York classi-fication scale by a musculoskeletalradiologist masked to the specificdiagnosis and clinical symptoms.

Re-evaluation of 10% of the films3 years later quantified intraobserv-er variability.Results. Two hundred and two pa-tients with psoriatic arthritis werestudied. Duration of the disease av-eraged 12 years; all patients hadpsoriasis and peripheral arthritis.The prevalence of radiographic evi-dence of sacroiliitis (grade 2 orhigher) was 78%; 71% of these hadgrade 3 disease.Conclusions. Previously reportedprevalence of sacroiliitis in patientswith psoriatic arthritis ranges from30% to 50%. The prevalence of ra-diographic evidence of sacroiliitis inthis large multicenter cohort of pa-tients with appendicular psoriaticarthritis was substantially higher.

Key words Sacroiliitis ´Psoriatic arthritis ´ Seronegativespondyloarthropathy ´ Spondylitis

Introduction

Since the first published descriptions of psoriatic arthritisappeared in 1818 [1], discussions of this condition haveoften been marked by controversy. Even through muchof this century, many rheumatologists rejected the charac-terization of psoriatic arthritis as a distinct clinical entity[2], arguing that the prevalence of rheumatoid arthritis isincreased in patients with psoriasis, and that in many casesthe joint disease is indistinguishable from that present inrheumatoid arthritis patients without psoriasis. In themid-1950s, several large epidemiologic surveys [3±5] pro-

vided convincing evidence of a distinct arthropathy relatedto psoriasis, and in 1964 it was recognized by the Ameri-can Rheumatism Association (now the American Collegeof Rheumatology). It was classified as one of the seroneg-ative spondyloarthropathies, a group of diseases that alsoincludes ankylosing spondylitis, and Reiter's syndrome,or reactive arthritis [6]. In 1973, Moll and Wright [7] pub-lished a landmark paper proposing a standardized defini-tion of psoriatic arthritis, as well as criteria for classifica-tion of five clinical subsets. Although widely accepted, theusefulness of the original Moll and Wright descriptionshas been increasingly questioned [8±10], in at least one

197

case by one of the authors himself [11], and newer catego-rization schemes continue to be proposed [10].

As with other seronegative spondyloarthropathies, theradiographic features of psoriatic arthritis may be varied.General features include fusiform soft tissue swelling, ar-ticular disruption, bone erosion and production, and distalphalangeal tuft resorption involving both hands and feet.In contrast to rheumatoid arthritis, bone density is pre-served, and most cases of psoriatic arthritis are distin-guished from other seronegative arthropathies by the in-volvement of both the appendicular and axial skeleton, in-tra-articular bone ankylosis, and tuft resorption [12]. Thereported prevalence of sacroiliac joint involvement isvariable, ranging from 14% to 63% [10, 13], and is gen-erally accepted to approximate 30±50% [12].

Recently, a large prospective, multicenter study of theefficacy of sulfasalazine (SSZ) in treating seronegativespondyloarthropathies was completed [14±16]. Two hun-dred and twenty-one patients with psoriatic arthritis wereenrolled in this investigation, which we believe representsthe largest cohort ever rigorously assembled. As part ofthis study, baseline radiographs were obtained for 202of these patients and the incidence of sacroiliitis was ob-served to be substantially higher than that which has pre-viously been reported. This prompted us to pursue a moredetailed subset analysis of these patients.

Patients and methods

Study design

The data were collected as part of a multicenter, double-masked,randomized, placebo-controlled parallel trial that compared the effi-

cacy of 2 g/day SSZ with placebo for the treatment of seronegativespondyloarthropathies (ankylosing spondylitis, psoriatic arthritis,and reactive arthritis). The methods of this study have been reportedin detail [14±16].

Eligibility

Patients were required to have an established diagnosis of psoriasis.If the skin disease was atypical, diagnosis was confirmed by a der-matologist and/or skin biopsy. Patients must have had one or moreof the following presentations of psoriatic arthritis: (1) distal inter-phalangeal joint involvement; (2) asymmetrical peripheral arthritis;or (3) symmetrical polyarthritis. Additionally, at the time of intake,patients must have had three ªactiveº joints defined as joint tender-ness and joint swelling of £2 on a 4-point scale and physician/pa-tient global assessments of moderate on a none/mild/moderate/se-vere/very severe scale. Axial joint involvement was not required.Patients were excluded from the study if rheumatoid factor(>1:80) or antinuclear antibodies (>1:160) were detected in the se-rum.

Enrollment and radiographic interpretation

At the screening visit patients underwent a radiographic survey ofaxial and, when clinically appropriate, peripheral joints. This includ-ed views of the pelvis (anteroposterior projection) and dedicated ob-lique sacroiliac views. These films were obtained at the clinicthrough which patients entered the study, and were sent to the StudyChairman's office at the Salt Lake City Veterans Affairs MedicalCenter. Because of the very large number of films in our overall pa-tient population (n=619), radiographs were interpreted by a singleexperienced musculoskeletal radiologist, masked to the patients'specific spondyloarthropathy (ankylosing spondylitis, psoriatic ar-thritis or reactive arthritis) and severity of symptoms, and gradedon a 5-point scale according to the Atlas of Standard Radiographsin Arthritis [17], following the recommendations of the New YorkConference for Population Studies [18]. According to these criteria,the scores ranged from 0 to 4: grade 0=normal; grade 1=suspicious

Fig. 1 Anteroposterior view of the sacroiliac joints, as an exampleof the minimal abnormalities seen in grade 2 sacroiliitis. Note thatwhile the synovial portions of the joints are not widened, narrowed,or fused, they do show cortical indistinctness. This is more obviouson the left side, but it is a bilateral finding

Fig. 2 Anteroposterior view of the sacroiliac joints, as an exampleof the unequivocal abnormalities seen in grade 3 sacroiliitis. In thiscase, the synovial portions of both joints show not only cortical in-distinctness, but narrowing as well. The findings are much more ob-vious than those of Fig. 1

198

changes; grade 2=minimal abnormalities (small localized areas oferosion or sclerosis without alteration in the joint width) (Fig. 1);grade 3=unequivocal abnormalities (moderate or advanced sacroili-itis with erosions, sclerosis, widening, narrowing, or partial ankylo-sis) (Fig. 2); and grade 4=total ankylosis. Each radiograph was readindependently, and interpreted only once; in other words, in no in-stance was an ªequivocalº grading (or any other rating) changedon the basis of additional information obtained from the viewingof other films. There were multiple films of peripheral joints in thesestudies; the pelvic and sacroiliac radiographs were evaluated in ran-dom order along with these other studies.

In an attempt to reduce intraobserver variability in scoring, largebatches of study films were read over week-long sessions. To calcu-late the degree of intraobserver variability, the radiographs of 19 pa-tients (38 joints) were re-evaluated by the same radiologist 3 yearsafter the initial interpretations were made, using the same scoringsystem.

Statistical analysis

Statistical analysis was done using SAS version 6.08 [19]. Statisticaltests were two-sided and a P value of £0.05 was the criterion for sta-tistical significance.

Statistical comparison of continuous measures between patientswith and without sacroiliitis was done using the t-test for indepen-dent groups. Similar comparisons for categorical data used Fisher'sexact test.

Results

Two hundred and twenty-one patients with psoriatic ar-thritis entered the study, over an enrollment period of32 months. One hundred and seventy (77%) were male.Radiographs were available for interpretation for 202cases; in the other 19 cases, the films were either not ob-tained or were of poor technical quality so that an accu-rate reading of the sacroiliac joints was not possible.

Figure 3 illustrates the distribution of radiographicgradings. One hundred and fifty-seven patients (78% ofthose for whom radiographs were available) had radio-graphic evidence of sacroiliitis, as defined by New Yorkclassification grade 2 or higher. One hundred and twelve(55%) patients had grade 3 or higher (ªunequivocalº) dis-ease.

Tables 1 and 2 summarize the baseline comparisons ofpatients with and without sacroiliitis. Table 1 reportsmeans, standard deviations, and t-test P values for the

continuous measures. Though there were trends towardstatistical significance for a longer time since diagnosisof arthritis (P=0.16), higher spondylitis functional index(P=0.11), and, most strongly, for a greater number of in-volved peripheral joints (P=0.09), none of these was sta-tistically significant.

Table 2 reports category percentages and Fisher's ex-act test P values for categorical and ordinal data. Interest-ingly, there was no relationship between the presence ofthe HLA-B27 antigen and sacroiliitis (P=1.00). Also,though there was a trend toward an increased prevalenceof sacroiliitis in males, this was not statistically signifi-cant (P=0.17).

Fig. 3 The distribution of radiographic grading of sacroiliitis for202 patients with psoriatic arthritis

Table 1 Baseline comparisonof patients by presence of sa-croiliitis: continuous measure-ments

Measure No sacroiliitis(n=45)

Sacroiliitis(n=157)

P value

Mean SD Mean SD

Time since arthritis diagnosed (years) 10.1 9.1 12.5 10.7 0.16Time since psoriasis diagnosed (years) 14.2 13.2 15.9 11.6 0.43Age (years) 50.3 11.9 49.8 12.9 0.81No. of involved joints 12.0 8.1 14.7 11.8 0.09Spondylitis functional index 11.6 6.2 13.3 6.3 0.11Enthesopathy index 4.9 5.9 5.7 5.9 0.44

Table 2 Baseline comparison of patients by presence of sacroiliitis:categorical and ordinal measurements

Measure No sacroiliitis(n=45)

Sacroiliitis(n=157)

P value

HLA-B27 (% positive) 15.6 17.2 1.00Gender (% female) 31.1 21.0 0.17Night pain

Not bothered (%) 22.2 15.3 0.33Bothered a little (%) 26.7 36.9Bothered a lot (%) 46.7 38.9Bothered terribly (%) 4.4 8.9

199

Intraobserver variability in radiographic interpretationis presented in Tables 3 and 4 [20]. All 38 sacroiliac joints(100%) had readings that differed by one grade or less;perfect agreement was observed in 21 of 38 joints (55%).

Discussion

Psoriatic arthritis, though first described almost 200 yearsago, has been recognized as a distinct clinical entity onlycomparatively recently, and today many aspects remaincontroversial. Although it is classified as one of the sero-negative spondyloarthropathies, sacroiliac disease is notuniformly present, and in fact there is significant variabil-ity in the literature regarding the prevalence of sacroiliitisin patients with psoriatic arthritis [5, 9, 10, 13, 21±25].This inconsistency is probably attributable to many fac-tors, including the wide spectrum of disease intensity, re-cent modifications in the criteria of radiographic grades,and the difficulty in achieving consensus among clini-cians regarding standardized classification patterns forpsoriatic arthritis.

In 1975, Little et al. [13] reported a series of 100 pa-tients hospitalized with psoriasis, 32 of whom had clinicalevidence of psoriatic arthritis. Twenty of these (63%) hadevidence of erosions and sclerosis involving the sacroiliacjoints. More recently, however, Veale et al. [10], in their1994 proposal of a revised, three-subgroup classificationschema of psoriatic arthritis, reported that the prevalenceof sacroiliitis in a cohort of 100 patients was only 14%[10]. An analysis of a large group of patients with PsAwas published by Gladman et al. [23] in 1987. In this co-

hort of 220 patients assembled over an 11-year period, theprevalence of sacroiliitis (as defined by New York grade 2or greater disease) was reported to be 27%. In subsequentstudies of the subset of patients with ªpsoriatic spondylo-arthropathyº (as defined by at least one of the following:inflammatory back pain, sacroiliitis demonstrated byphysical examination, or radiographs demonstrating grade2 (or higher) sacroiliitis or classical or paramarginal syn-desmophytes), no statistical relationship between the fre-quency of HLA-B27 antigen and either patient gender orclinical progression of disease was observed [26, 27].

In the enrollment phase of a large, multicenter pro-spective investigation of the treatment of psoriatic arthri-tis, we observed a 78% prevalence of sacroiliitis, a valuewhich is substantially higher than that previously report-ed. In reviewing the data we considered several possiblesources of error. First, there is concern that this study,conducted under the auspices of the Department of Veter-ans Affairs, may have implicit bias in favor of male par-ticipants. Though we did recruit more men to the studythan women, the prevalence of sacroiliitis was not signif-icantly linked to gender. In addition, in another large co-hort of patients with psoriatic arthritis, the male/femaleratio of those with back disease and either oligoarthritisor polyarthritis (i.e., a comparable group to those selectedfor our study) was essentially 1:1 [23]. We do not find ev-idence of significant gender bias in this investigation.

Second, we considered the possibility that we had se-lected a cohort in which the prevalence of sacroiliitiswas inordinately high. However, this project was de-signed as a prospective interventional study, and the par-ticipants were recruited on the basis of peripheral, not ax-

Table 3 Intraobservervariability in left sacroiliac jointreadings

Initial reading Second reading

Normal Suspicious Minimallyabnormal

Unequivocallyabnormal

Totalankylosis

Total

Normal 1 0 0 0 0 1Suspicious 0 0 2 0 0 2Minimally abnormal 2 0 1 3 0 6Unequivocally abnormal 0 0 3 6 1 10Total ankylosis 0 0 0 0 0 0Total 3 0 6 9 1 19

Table 4 Intraobservervariability in right sacroiliacjoint readings

Initial reading Second reading

Normal Suspicious Minimallyabnormal

Unequiocallyabnormal

Totalankylosis

Total

Normal 0 1 0 0 0 1Suspicious 0 0 1 0 0 1Minimally abnormal 1 1 1 2 0 5Unequivocally abnormal 0 1 3 7 1 12Total ankylosis 0 0 0 0 0 0Total 1 3 5 9 1 19

200

ial, joint disease. We do not find evidence of significantselection bias.

Third, we did not obtain radiographic evaluation ofsacroiliitis in 19 (8.6%) patients. In the extreme scenariothat none of these patients had sacroiliitis, the prevalencerate for the study would only drop to 71%, a figure thatremains higher than reported elsewhere.

Finally, we recognize that one of the potential limita-tions of these data is that the radiographs were read byone radiologist; there was no control for interobserver bi-as, which may represent a source of error. No normal con-trols were included. Thus the radiologist was aware thatthe radiographs were taken from study patients, but shewas masked to the underlying diagnosis (ankylosingspondylitis, psoriatic arthritis, reactive arthritis). Howev-er, it should be noted that of 12 published studies that re-port a prevalence of radiographic sacroiliitis in psoriaticarthritis, eight do not describe how or by whom the filmswere interpreted [2, 5, 9, 10, 18, 21, 24, 25], and three in-dicate that the radiographs were read by rheumatologists[23, 27, 29]. In the remaining study, the participation ofa single radiologist was documented, in combination witha rheumatologist [26]. Perhaps the variability of publishedprevalence figures may, to some degree, reflect the vari-ance of methodology in the interpretation of radiographsin these studies.

In consideration of intraobserver variability for oursingle radiologist observer, our study shows that there

was substantial variability in rating according to the clas-sification system (45% of the second readings showed adifferent classification of degree of sacroiliitis). However,in none of these cases did the difference in classificationchange the diagnosis from unequivocal sacroiliitis to nor-mal, or vice versa. Furthermore, none of the classificationdifferences was greater than one degree (for example,ªsuspiciousº versus ªminimal abnormalityº).

In conclusion, we report our observation of a 78%prevalence of sacroiliitis in a large, multicenter cohortof patients with psoriatic arthritis. We believe these re-sults are important because this is the first observationalstudy of this size and demographic distribution, and be-cause no effort was made to recruit patients on the basisof axial symptoms. Although the prevalence of sacroiliitisin psoriatic arthritis is generally accepted to be consider-ably lower, the wide range of reported data suggests thatthe accuracy of this figure may be in question. As newclassification systems for psoriatic arthritis continue tobe proposed, consideration should be given to the possi-bility that a large majority of patients with peripheral ar-thritis will also have axial disease.

Acknowledgements Supported by the Cooperative Studies Pro-gram of the Department of Veterans Affairs Research and Develop-ment Service and by an unrestricted grant to the Western Institutefor Biomedical Research, Inc. (a not for profit foundation) fromKabi Pharmacia, AB.

References

1. Alibert JL. PrØcis theorique et pratiquesur les maladies de la peau. Paris: Cailleet Ravier, 1818.

2. Avila R, Pugh DG, Slocumb CH,Winkelmann RK. Psoriatic arthritis: aroentgenologic study. Radiology 1960;75:691±701.

3. Wright V. Rheumatism and psoriasis: are-evaluation. Am J Med 1959; 27:454±462.

4. Wright V. Psoriatic arthritis: a compar-ative study of rheumatoid arthritis andarthritis associated with psoriasis. ArchDermatol 1959; 80:27.

5. Wright V. Psoriatic arthritis: a compar-ative radiographic study of rheumatoidarthritis and arthritis associated withpsoriasis. Ann Rheum Dis 1959;20:123±132.

6. Blumberb BS, Bunim JJ, Calkins E,Pirani CL, Zvaifler NJ. ARA nomen-clature and classification of arthritis andrheumatism (tentative). Arthritis Rheum1964; 7:93±97.

7. Moll JMH, Wright V. Psoriatic arthritis.Semin Arthritis Rheum 1973; 3:55±78.

8. Gladman DD, Stafford-Brady F, ChangCH, Lewandowski K, Russell ML.Longitudinal study of clinical and ra-diological progression in psoriatic ar-thritis. J Rheumatol 1990; 17:809±812.

9. Torre Alonso JC, Perez AR, CastrilloJMA, Garcia JB, Noriega JLR, LarreaCL. Psoriatic arthritis: a clinical, im-munological and radiological study of180 patients. Br J Rheumatol 1991;30:245±250.

10. Veale D, Rogers S, Fitzgerald O. Clas-sification of clinical subsets in psoriaticarthritis. Br J Rheumatol 1994; 33:133±138.

11. Helliwell P, Marchesoni A, Peters M,Barker M, Wright V. A re-evaluation ofthe osteoarticular manifestations ofpsoriasis. Br J Rheumatol 1991; 30:339±345.

12. Resnick D, Niwayama G. Psoriatic ar-thritis. In: Resnick D, ed. Bone and jointimaging. Philadelphia: WB Saunders,1989: 320±328.

13. Little H, Harvie JN, Lester RS. Psoriaticarthritis in severe psoriasis. C Med As-soc J 1975; 112:317±319.

14. Clegg DO, et al. Comparison of sulfa-salazine and placebo in the treatment ofankylosing spondylitis: a Department ofVeterans Affairs cooperative study. Ar-thritis Rheum 1996; 39:2004±2012.

15. Clegg DO, et al. Comparison of sulfa-salazine and placebo in the treatment ofpsoriatic arthritis: a Department of Vet-erans Affairs cooperative study. Arthri-tis Rheum 1996; 39:2013±2020.

16. Clegg DO, et al. Comparison of sulfa-salazine and placebo in the treatment ofreactive arthritis (Reiter's syndrome): aDepartment of Veterans Affairs cooper-ative study. Arthritis Rheum 1996;39:2021±2027.

17. Kellgren JH, Jeffrey MR. Epidemiologyof chronic rheumatism. In: Atlas ofstandard radiographs in arthritis, vol 11.Oxford: Blackwell Scientific, 1963: 36±40.

18. Van der Linden S, Valkenburg HA, CatsA. Evaluation of diagnostic criteria forankylosing spondylitis: a proposal formodification of the New York Criteria.Arthritis Rheum 1984; 27:361±368.

201

19. SAS Institute. SAS/STAT user's guide,version 6, 4th edn. Cary, NC: SAS In-stitute, 1990.

20. Battistone MJ, Manaster BJ, Reda DJ,Clegg DO. Radiographic diagnosis ofsacroiliitis: are sacroiliac views reallybetter? J Rheumatol 1998; 25:2395±2401.

21. Leonard DG, O'Duffy JD, Rogers RS.Prospective analysis of psoriatic arthritisin patients hospitalized for psoriasis.Mayo Clin Proc 1978; 53:511±518.

22. Scarpa R, Oriente P, Pucino A, TorellaM, Vignone L, Riccio A, Oriente CB.Psoriatic arthritis in psoriatic patients.Br J Rheumatol 1984; 23:246±250.

23. Gladman DD, Shuckett R, Russell ML,Thorne JC, Schachter RK. Psoriatic ar-thritis: an analysis of 220 patients. Q JMed 1987; 62:127±141.

24. Suarez-Almazor ME, Russell AS. Sac-roiliitis in psoriasis: relationship to pe-ripheral arthritis and HLA-B27. JRheumatol 1990; 17:804±808.

25. Golfieri R, Giampala E, Tosti A,Calculli L, Berardi R, Gavelli G. Psori-atic arthritis: a review of radiologicalfindings and personal experience. Ra-diol Med (Torino) 1992; 84:228±235.

26. Gladman DD, Brubacher B, Buskila D,Langevitz P, Farewell VT. Psoriaticspondyloarthropathy in men and wom-en: a clinical, radiographic and HLAstudy. Clin Invest Med 1992; 15:371±375.

27. Hanly JG, Russell ML, Gladman DD.Psoriatic spondyloarthropathy: a longterm prospective study. Ann Rheum Dis1988; 47:386±393.

28. Meaney TF, Hays RA. Roentgen mani-festations of psoriatic arthritis. Radiolo-gy 1957; 68:403±407.

29. McEwen C, DiTata D, Lingg C, PoriniA, Good A, Rankin T. Ankylosingspondylitis and spondylitis accompany-ing ulcerative colitis, regional enteritis,psoriasis, and Reiter's disease: a com-parative study. Arthritis Rheum 1973;14:291±318.