The Prevalence of Psoriatic Arthritis in People With Psoriasis

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1 Arthritis & Rheumatism (Arthritis Care & Research) Vol. 61, No. 10, October 15, 2009, pp DOI /art , American College of Rheumatology SPECIAL ARTICLE: EPIDEMIOLOGY OF THE RHEUMATIC DISEASES The Prevalence of Psoriatic Arthritis in People With Psoriasis G. IBRAHIM, 1 R. WAXMAN, 2 AND P. S. HELLIWELL 3 Objective. To determine the prevalence of psoriatic arthritis (PsA) using the ClASsification criteria for Psoriatic ARthritis (CASPAR) for classification. Methods. People with psoriasis were identified from the computerized morbidity indices of 2 large UK general practices, total population 22,500. Questionnaires were mailed to all 633 patients thus identified. Of the respondents, a 50% sample was assessed clinically and a proportion had blood samples and radiographs taken. Patients labeled as having psoriasis were also cross-referenced with a local secondary care morbidity index for PsA and rheumatoid arthritis. Figures for the prevalence of PsA were estimated from these data. Results. One hundred sixty-eight questionnaires were returned (response rate 27%) and 93 people (55% of questionnaire respondents) were examined. Of these 93 people, 12 (4 of whom were cross-referenced to the hospital database) were thought to have PsA clinically, all fulfilling the CASPAR criteria for PsA. Six of the 93 examined patients did not have psoriasis or a family history of psoriasis and had no historical features or clinical signs of psoriasis on interview and examination. Extrapolating from the data of those people actually examined, the estimated (corrected) prevalence was 13.8% (95% confidence interval %). Conclusion. The estimated prevalence of PsA in this population, using the CASPAR criteria, was 13.8%. Misclassification of psoriasis and arthritis, and response bias, indicate that this is probably an overestimate. INTRODUCTION Psoriatic arthritis (PsA) is characterized by chronic arthritis in the presence of psoriasis and is found in up to 30% of people with psoriasis (1). Certain clinical features help differentiate this disorder from rheumatoid arthritis (RA) and other forms of arthritis, including the presence of axial involvement, distal interphalangeal involvement, dactylitis, and enthesitis. However, the classification of PsA poses methodologic difficulties: the spectrum of the clinical disease is wide, the disease is relapsing and remitting, prevalence of the disease is low, and the methods for ascertaining past arthritis and psoriasis need clarification. A recent review of the incidence and prevalence of PsA 1 G. Ibrahim, ABMS, MRCP, MSc: St. Luke s Hospital, Bradford Teaching NHS Foundation Trust, Bradford, UK; 2 R. Waxman, BSc, MPH: University of Leeds, Leeds, UK; 3 P. S. Helliwell, DM, PhD, FRCP: St. Luke s Hospital, Bradford Teaching NHS Foundation Trust, Academic Unit of Musculoskeletal Disease, University of Leeds, Leeds, UK. Address correspondence to P. S. Helliwell, DM, PhD, FRCP, Leeds Institute of Molecular Medicine, Section of Musculoskeletal Disease, University of Leeds, Second Floor, Chapel Allerton Hospital, Harehills Lane, Leeds, LS7 4SA, UK. p.helliwell@leeds.ac.uk. Submitted for publication December 23, 2008; accepted in revised form March 30, found that most studies had used arthritis and psoriasis as the case definition (2). With the publication of new, internationally agreed-upon criteria, future studies should at least have a validated approach to case definition (3). There are 2 general approaches to studying the prevalence of PsA. The first method sets out to determine the prevalence in the (adult) population as a whole, and this was the basis for the studies reviewed by Alamanos et al (2). This systematic review found a wide prevalence for PsA, ranging from cases per 100,000 people. Possible reasons for this discrepancy include methodologic differences and true ethnic variations in disease prevalence. The second approach is to examine the prevalence of PsA in the population of people with psoriasis, being that most cases of PsA arise in cases of existing psoriasis. This approach can be further subdivided into those studies of people referred to secondary care, presumably the more severe cases, or all of those with psoriasis, both referred and not referred. Theoretically, the latter approach will provide a more valid overall estimate of the prevalence of PsA in the general psoriasis population, but only one such study has been reported, and that only as an abstract (4). The current study sought to estimate the prevalence of PsA in a sample of community-based people coded electronically as having psoriasis by their primary care practitioner. 1373

2 1374 Ibrahim et al PATIENTS AND METHODS Full ethical committee approval was given for this study, and all patients gave their signed, informed consent to take part. Three databases were used for this study. The first and second databases were morbidity indices from 2 general practices in Bradford, West Yorkshire, UK (the diagnostic Read codes used for identifying the subjects were M16: psoriasis and similar disorders, and MYU30: other psoriasis). The codes used in this database are entered by the general practitioners at the time of consultation or upon receipt of information from other sources (such as letters from specialists). The third database was based in the adjacent secondary care facility and recorded all rheumatologic diagnoses of patients seen since 1993 (n 14,607). This database is coded using the International Classification of Diseases, Ninth Revision, and the code used to identify people seen with a diagnosis of PsA was 696.0: psoriatic arthropathy. Using the general practitioner database as the sampling frame, each subject received a packet in the mail. The packet contained a questionnaire together with a patient information sheet, a consent form, and an accompanying letter from their general practitioner. A final question asked whether they would be available to be examined. Alternate consenting responders were invited for examination. The subjects were sent the full packet on only 1 occasion, but all nonresponders at 4 weeks were sent a letter containing an addressed, stamped postcard asking 6 simple questions (these were taken from the longer version of the questionnaire). The starting point for the current instrument was the Swedish modification of the Psoriasis Assessment Questionnaire (5). To these questions were added questions used to screen for spondylarthropathy, developed by Guillemin et al (6). The final questionnaire included items asking about peripheral and axial arthritis, buttock and heel pain, and skin and nail disease. In addition, a manikin was provided on which respondents could indicate painful joints. The examination schedule was standardized and emulated the protocol used in the ClASsification criteria for Psoriatic ARthritis (CASPAR) study (3). Both historic and examination data were collected, including a 76 swollen/78 tender/78 damaged joint count. Attendees were asked to complete the British Modification of the Health Assessment Questionnaire (HAQ) (7). Both the Maastricht Ankylosing Spondylitis Enthesitis Score (MASES) (8) and the Leeds Enthesitis Index (9) were measured. Where present, dactylitis was assessed using the Leeds Dactylitis Index (10). Finally, the skin was assessed using the Psoriasis Area and Severity Index (PASI) (11). In order to avoid inconvenience and unnecessary radiation exposure, only those patients thought to have a diagnosis of PsA underwent subsequent testing with blood tests for rheumatoid factor and C-reactive protein (CRP) level, and with radiographs of the hands, feet, pelvis, and lumbar spine. Statistical analysis. All statistical analyses were carried out using SPSS, version 15.0 (SPSS, Chicago, IL). The estimated prevalence of PsA was taken from the figures obtained from the people examined, extrapolating to the whole population. As a check, prevalence figures were estimated by both extrapolation (newly identified PsA) and the known cases of PsA from the hospital morbidity index. Some adjustment to the crude prevalence figures was necessary because there were some subjects identified on the general practitioner morbidity index as having psoriasis who denied having psoriasis or a family history of psoriasis and had no clinical sign of psoriasis on interview and examination. These no psoriasis subjects were noted, and an adjustment was made to the whole group based on these patients. Further adjustments (weighting) according to the age of the respondents were not possible owing to the small number of newly identified cases of PsA. The 95% confidence interval (95% CI) for prevalence was calculated using Schoenberg s tables (12). RESULTS The 2 general practices had a combined patient population of 22,500. From this combined population, 633 people had one of the psoriasis diagnostic labels indicated. This equates to a psoriasis prevalence of 2.8%. One hundred sixty-eight questionnaires were returned (response rate 27%), and 93 people (55% of questionnaire respondents) were examined. Of these 93, 12 were thought to have PsA clinically, all fulfilling the CASPAR criteria for PsA, which are given in Table 1 (3). Four of these people were already known and registered in the hospital database, therefore, 8 received a new diagnosis of PsA, as shown in Figure 1. Of the examined patients, none had an elevated CRP level and all were seronegative. Only 1 patient had abnormal radiographs, demonstrating juxtaarticular new bone formation. The 12 people diagnosed with PsA (6 men, 6 women) had a mean SD age of years, a mean SD duration of psoriasis of years, a mean SD duration of arthritis symptoms of years, a mean SD swollen joint count of , a mean SD HAQ score of , and a mean SD PASI score of Ten patients had clinical enthesitis, with a mean MASES score of 3.2 and a mean Leeds Enthesitis Index score of Only 1 patient had dactylitis, with a Leeds Dactylitis Index score of 22. None of the patients diagnosed with PsA had spinal involvement clinically or radiographically. For the other people examined and found not to have PsA, the diagnoses included osteoarthritis (26 patients), mechanical low back pain (15 patients), unclassified polyarthralgia (12 patients), hypermobility syndrome (3 patients), and 1 patient each with RA, gout, fibromyalgia, and Raynaud s phenomenon. Inaccuracies in general practitioner coding and patient response. Of the 93 patients examined, 2 denied having psoriasis or a family history of psoriasis and had no historic features or clinical signs of psoriasis on interview and examination. A further 4 reported a personal or family history of psoriasis that was not corroborated on interview and examination. Thirteen patients denied having psoriasis or a family history of psoriasis but were found to either have psoriasis or a convincing family history of psoriasis

3 PsA Prevalence in Patients With Psoriasis 1375 Table 1. The CASPAR criteria: inflammatory articular disease (joint, spine, or entheseal) with >3 points from the following* Criteria Evidence of psoriasis (1 of the following) Current psoriasis Personal history of psoriasis Family history of psoriasis Psoriatic nail dystrophy A negative test for RF Dactylitis (1 of the following) Current History Radiologic evidence of juxtaarticular new bone formation Definition Psoriatic skin or scalp disease present today as judged by a dermatologist or rheumatologist A history of psoriasis that may be obtained from the patient, family doctor, dermatologist, rheumatologist, or other qualified health care provider A history of psoriasis in a first- or second-degree relative according to patient report Typical psoriatic nail dystrophy, including onycholysis, pitting, and hyperkeratosis, observed on current physical examination By any method except latex, but preferably by ELISA or nephelometry, according to the local laboratory reference range Swelling of an entire digit A history of dactylitis recorded by a rheumatologist Ill-defined ossification near joint margins (but excluding osteophyte formation) on plain radiographs of the hand or foot * Current psoriasis scores 2, whereas all other items score 1. CASPAR ClASsification criteria for Psoriatic ARthritis; RF rheumatoid factor; ELISA enzyme-linked immunosorbent assay. at interview and examination. These results are summarized in Table 2. An adjustment to the exposed population was therefore made, and an estimate of the population prevalence was derived from this adjusted figure (n 582). Response bias. In order to estimate response bias, 2 comparisons were made (Table 3). The index group was composed of the people who were examined, on which the prevalence estimate was based. The comparator groups were the total population of questionnaire respondents and the people who responded to the postcard mailing (the second mailing overall; 122 responded of 467 who were mailed, response rate to postcard mailing 26%). Because the postcard was by design a brief version of the full screening questionnaire, not all of the questions were able to be matched. There was little difference in the responses between those who were examined and the whole group of questionnaire respondents (Table 3). However, those who failed to respond to the initial questionnaire but who did respond to the followup postcard request were less likely to report buttock and heel pain or a history of a swollen joint, but were just as likely to report a swollen digit or have had a radiograph of the back or hips. In all 3 groups a similar percentage of respondents (82 84%) reported a family history or a personal history of psoriasis. Prevalence estimates. After correcting for the truenegative and false-positive rates (Table 2) and extrapolating from the data of those people actually examined, the estimated (corrected) prevalence of PsA in people with Table 2. Responses to the question in the screening questionnaire Is there any family history or have you ever had psoriasis? compared with findings on history and examination Screening questionnaire History and examination Yes No Figure 1. Flow diagram indicating the origin of the patients in this study. GP general practitioner; CASPAR ClASsification criteria for Psoriatic ARthritis. Yes No 4 2

4 1376 Ibrahim et al Table 3. Comparison of the people examined, of all the respondents to the screening questionnaire, and of those who only responded to the postcard mailing* Examined (n 93) All questionnaire respondents (n 166) Postcard only (n 122) Male sex 49 (53) 79 (47) 51 (46) Q1: Have you ever 61 (66) 113 (68) n/a thought you might have arthritis? Q2: Have you ever had a 44 (47) 94 (56) 51 (42) swollen joint (or joints)? Q3: Has a doctor ever 41 (45) 66 (40) n/a told you that you have arthritis? Q13: Have you had pain 30 (32) 56 (34) 21 (18) in your buttocks? Q14: Have you had pain 32 (34) 67 (40) 32 (27) in your heel? Q15: Have you ever had a 35 (27) 57 (34) 30 (25) finger or toe that was completely swollen and painful for no apparent reason? Q16: Have you ever had a 24 (26) 49 (29) 30 (25) radiograph of your back or hips? Q18: Is there any family history or have you ever had psoriasis? 78 (84) 139 (84) 100 (82) * Values are the number (percentage). n/a not available. psoriasis was 13.8% (12 of 87 people; 95% CI %). Taking into account both data from known cases and from those identified at examination, the estimated prevalence of PsA in people with psoriasis was 11.7%. DISCUSSION The epidemiology of PsA is difficult and has lagged behind the study of other arthropathies, particularly RA and ankylosing spondylitis (13). Therefore, there has been some discrepancy in the literature regarding the incidence and prevalence of PsA, with population prevalence figures ranging from % (2) and prevalence figures within the population of people with psoriasis varying from 6 42% (1). One reason for this discrepancy is that until recently, there have been no universally agreedupon or properly validated case definitions for PsA, hampering both epidemiologic research and intervention trials (14). The current study represents the first attempt to our knowledge to determine the prevalence of PsA in people with psoriasis using the newly developed CASPAR criteria (3). The estimated prevalence from the patients examined was identified as the most reliable estimate, although the 95% CIs were wide. This prevalence, at 13.8%, is less than hospital-based estimates (where a prevalence of up to 39% has been reported) (15), estimates based on self-report (26%) (16), and estimates based on both community and referral populations (20.6%) (17). Likely reasons for this discrepancy are the criteria for case identification and the population on whom the survey was based. Some studies have used the European Spondylarthropathy Study Group (ESSG) criteria for PsA, which have had lower sensitivity (0.55) than, for example, the Moll and Wright criteria (sensitivity 0.95) in comparative studies (18). Other studies have simply used the combination of psoriasis and (inflammatory) arthritis as a definition, not distinguishing or excluding other diagnoses, such as RA with coincidental psoriasis. Studies using the ESSG criteria are therefore likely to give an underestimate, which makes the overall population prevalence estimate reported by De Angelis et al of 0.42% even more surprising (19). The use of the arthritis and psoriasis combined definition is likely to give an overestimate. The CASPAR criteria have both good sensitivity (0.91) and specificity (0.99) but, importantly, the criteria are validated and internationally accepted, and can form the basis of other population studies. Moreover, it is also likely that cross-sectional prevalence studies that use hospital-based patients (either as inpatients or outpatients) are likely to give higher estimates of PsA, partly because of more intense and systematic case detection and partly because this group is at the more severe end of the spectrum of disease (20). The association between the severity of disease and the prevalence of arthritis has been noted in the past (15,21) and also more recently (22). Of interest is the overall prevalence of PsA in people with

5 PsA Prevalence in Patients With Psoriasis 1377 psoriasis of 11% found by Gelfand et al (22), obtained by a telephone survey of randomly selected community-dwelling people. Although that survey relied on self-report, the estimate is similar to that obtained in the present study. All studies attempting to determine the prevalence of PsA, and thus be inclusive, face similar problems, which can be summarized as follows. First, psoriasis and RA are common diseases, and some patients with RA will have coincidental psoriasis; psoriasis may precede, occur simultaneously, or follow the onset of arthritis such that, in the latter case, the patient may be mistakenly diagnosed as having an inflammatory arthritis other than PsA (23). Second, psoriasis may be present but may be hidden, or may be misdiagnosed (by rheumatologists) (24). Psoriasis may only be apparent in the natal cleft or some other hidden area such as under the breasts, around the umbilicus, or in the hairline. The psoriasis may only be evident in the nails. In these circumstances, criteria that do not mandate the presence of psoriasis but include a positive family history and specific features of the skin and articular disease, all of which are included in the CASPAR criteria, will offer an advantage over alternative criteria both in terms of sensitivity and specificity. On the other hand, the CASPAR criteria were developed using cases of established disease, and so they may not function well in early disease. There is conflicting data about this. Chandran and colleagues found that the CASPAR criteria worked well for patients with a symptom duration of 12 months (25), but a recent publication from Italy reported a reduced sensitivity of 77% for the CASPAR criteria in recent-onset, rheumatologistdiagnosed PsA (26). A number of limitations of the current data are evident. First, the electronic databases from which the sample was drawn contain errors. A recently published study reported an error of 27% in a community-based electronic database for psoriasis (27). In the current study the estimated error rate was lower, but a false-positive rate of 6.5% is important in the context of prevalence studies. Electronic coding is subject to error in several ways, but mainly due to errors of coding the diagnosis and errors in entering the data. The former may occur due to the clinical inexperience of the person making the diagnosis, but there are no data in this study on this process in the general practice databases used. It could be argued that the verification of the diagnosis is also subject to error, given that a dermatologist was not involved in this study. However, the senior author has worked in this field for 20 years, and for 10 of these in a combined dermatology/rheumatology clinic jointly seeing cases of psoriasis on a weekly basis. Of course, it is impossible to be completely sure when there is a reported history of psoriasis but no skin disease evident at the time of examination. In terms of the secondary care database, the case notes of all 16 patients were reviewed and appraised using the CASPAR criteria. Fifteen of these fulfilled the criteria, giving a false-positive rate of 6.3%. The one patient who did not fulfill the criteria had oligoarthritis and a positive family history of psoriasis. The response rate to the initial questionnaire was disappointing at 27%, and suggests that response bias is important in this estimate of prevalence, those with more joint problems being more likely to reply (the stated purpose of the survey was to estimate the prevalence of PsA). This study permitted a glimpse of the nonresponders to the initial survey and, to some extent, the nonresponders had fewer articular complaints (Table 3). For this reason, the prevalence is likely to be an overestimate. It is of interest that the 8 newly diagnosed patients did not have recent-onset disease, with a mean duration of arthritis symptoms of 17.6 years. How could these people have been missed? There are a number of possible reasons for this. First, the articular complaints may not have been presented to a health professional. Second, if presented, the health professional may have wrongly attributed them to some other diagnostic category, such as osteoarthritis (the mean age of this group was 54 years). This may also have been an error of omission, given that PsA is less frequent and less recognizable than, for example, RA. It is also worth noting that the average swollen joint count in those newly diagnosed patients was only just 2, and that the impairment and impact on function may not have been severe enough to cause a visit to the general practitioner, or a referral to a specialist clinic. In summary, the estimated prevalence of PsA in this population with psoriasis, using the CASPAR criteria, was 13.8%. Misclassification of psoriasis and arthritis, and response bias, indicate that this is probably an overestimate. ACKNOWLEDGMENTS We thank the doctors and patients of the Ridge Medical Practice and Haigh Hall Medical Centre, Bradford, West Yorkshire, UK. We would also like to thank Drs. Cathy Lawson and Maya Buch for help with data collection and Mrs. Pauline Oldfield for administrative assistance. AUTHOR CONTRIBUTIONS All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors approved the final version to be submitted for publication. Dr. Helliwell had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study conception and design. Helliwell. Acquisition of data. Ibrahim, Helliwell. 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