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Rheumatology 2007 46(12):1819-1823; doi:10.1093/rheumatology/kem270
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© The Author 2007. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Five-year outcome of a primary-care-based inception cohort of patients with inflammatory polyarthritis plus psoriasis

C. Morgan1, M. Lunt1, D. Bunn2, D. G. I. Scott2 and D. P. M. Symmons1

1ARC Epidemiology Unit, Stopford Building, University of Manchester, Manchester and 2Norfolk Arthritis Register, Department of Rheumatology, Norfolk and Norwich University Hospital, Norwich, UK.

Correspondence to: D. P. M. Symmons, ARC Epidemiology Unit, Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK. E-mail: deborah.symmons{at}manchester.ac.uk


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 
Objectives. To establish whether patients with inflammatory arthritis plus psoriasis have a different outcome from those who do not have psoriasis.

Methods. Seventy-nine patients with inflammatory arthritis plus psoriasis were recruited by the Norfolk Arthritis Register (NOAR) in 1990–94 and followed for 5 yrs. Their outcome was compared with the remainder (n = 755) of the NOAR cohort. We then restricted the analysis to subjects who were rheumatoid factor (RF)-negative, and compared those with and without psoriasis. Outcomes studied included remission, deformed joint count, the presence and extent of erosive damage and physical function.

Results. Patients with psoriasis were younger, more likely to be male, less likely to be RF-positive and more likely to have been treated with disease-modifying drugs than patients without psoriasis. After adjustment for age, gender and treatment, the only differences between the psoriasis and non-psoriasis groups were in RF positivity (adjusted odds ratio 0.44; 95% CI 0.25, 0.78) and in the Larsen score in patients with erosions.

Conclusions. Patients with inflammatory arthritis plus psoriasis have a similar outcome to other RF-negative patients with arthritis.

KEY WORDS: Psoriatic arthritis, Outcome, Inflammatory arthritis, Psoriasis


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 
It is well recognized that patients with psoriasis develop peripheral joint inflammatory arthritis (IA) more often than would be expected by chance [1] and that patients with psoriasis plus IA are more often rheumatoid factor (RF)-negative than patients without psoriasis who have IA [2]. Most rheumatologists also accept that psoriatic arthritis (PsA) is a distinct disease entity and that not all patients with psoriasis plus IA have PsA [3]. Work continues to try and establish robust internationally recognized classification criteria for PsA. The classification of psoriatic arthritis (CASPAR) project has recently collected information on 558 patients with physician diagnosed PsA and 525 controls with other forms of IA [70% had rheumatoid arthritis (RA)] in order to develop such a criteria set [4]. It is, however, likely to be some years before prospective studies of outcome of PsA which have used the CASPAR criteria can be published.

In the meantime, there is some controversy in the literature as to whether PsA is a mild disease in the majority of cases [5–7] or whether, as in RA, the number of joints involved and the degree of damage becomes progressively worse [8]. Work from the University of Toronto Psoriatic Arthritis Clinic suggests that only 17% of patients enter remission [9]. The discrepancies between the studies may be explained by different referral patterns (selection bias) and different disease definition.

This study took a different approach and aimed to describe the 5-yr outcome in patients with IA recruited by the Norfolk Arthritis Register (NOAR) with and without psoriasis without attempting to classify patients as having PsA. Within the cohort, we first compared the outcome in all patients with psoriasis with that in all patients without psoriasis and second we compared seronegative patients with psoriasis with seronegative patients without psoriasis.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 Acknowledgements
 References
 
NOAR is a primary-care-based inception cohort of patients with inflammatory polyarthritis (IP). All the general practitioners (GPs) and rheumatologists in the former Norwich Health Authority are asked to register all patients with synovitis of two or more joints with a duration of four or more weeks and an onset since 1 January 1990 [10]. Patients are seen by a research nurse who completes a standardized questionnaire which includes a question about a history of psoriasis, examines the patient's joints and skin on the limbs and scalp, and takes blood for RF estimation. RF is measured using the latex agglutination test and patients are designated RF-positive if they have a titre of ≥1/40. A structured examination of the DIP joints, proximal interphalangeal joints (PIP), metacarpophalangeal (MCP) joints, wrists, elbows, shoulders, neck, hips, knees, ankles and metatarsophalangeal joints (MTP) is conducted for tenderness, swelling and deformity [11]. The research nurses were trained in examination of the skin by two rheumatologists (D.P.M.S, D.G.I.S.) and attended some dermatology clinics. The patient is asked to complete the Health Assessment Questionnaire (HAQ) [12] validated for use in British patients [13]. For the first 5 yrs all patients are followed annually. Information about disease-modifying anti-rheumatic drug (DMARD) therapy and steroids is collected at baseline and at each annual follow-up.

At 5 yrs, the joint examination is repeated, patients complete the HAQ and short form 36-item health survey (SF-36) [14] and have X-rays taken of the hands and feet. The HAQ and SF-36 have been validated in patients with PsA [15]. The X-rays are read by two observers, blind to the presence of psoriasis, using Larsen's method [16]. A third reader arbitrates in cases of disagreement. The DIP joints are not included in the Larsen method. The 1987 ACR criteria for RA [17] are applied at baseline and cumulatively over the 5 yrs. Remission is defined as no swollen joints on examination, and not on DMARDs or steroids for at least 3 months.

To be eligible for this study, patients had to have completed 5 yrs of follow-up. Patients were categorized as having psoriasis if they ever had psoriasis on examination by one of the research nurses at baseline or at any subsequent assessment up to 5 yrs.

Statistical methods
Most of the outcome variables were treated as continuous with the data presented as medians with interquartile ranges (IQR). The Mann–Whitney U test was used to compare medians between the two groups. Some outcome results were dichotomized as present/absent (erosions, nodules, remission). Chi-squared test was then used to compare proportions between the groups.

In order to examine the influence of psoriasis on outcome, for the dichotomous variables, logistic regression was used to examine the odds of a patient with psoriasis being in the worse outcome category. These results were adjusted first for age and gender, then age, gender and treatment (ever treated with a DMARD). The remaining outcomes, except for the Larsen score, were divided into tertiles and ordinal regression (adjusted for confounders) was conducted to examine the relative odds of psoriasis patients being in a worse grouping. Finally, the Larsen score was analysed using negative binomial regression and the results expressed as percentage changes in score.

In addition, the outcomes were examined as the predictor variables with the presence of psoriasis as the dependent variable using logistic regression. A multivariate model was constructed with psoriasis as the dependent variable and items identified as significant in the univariate analysis entered into the model which was adjusted for age, gender and treatment with DMARDs. All analysis was performed using STATA 8.

Ethical approval for the NOAR project was given by the Norwich Local Research Ethics Committee and all participants gave informed consent.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 Acknowledgements
 References
 
Seventy-nine patients with IP plus psoriasis were recruited between 1990 and 1994 and completed 5 yrs of follow-up. They were compared with 755 patients with IP and no psoriasis recruited in the same time period (Table 1). Patients with psoriasis were more likely to be male (45.6 vs 31.4%; risk difference –14; –26, –3) and were somewhat younger at arthritis onset. They were also less likely to be RF-positive (16.5 vs 25.3%; risk difference –10.4; –20.0, –0.7) at baseline.


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  		TABLE 1. Baseline characteristics of patients with and without psoriasis recruited from 1990 to 1994

 
At 5 yrs, the patients with psoriasis were still less likely to be RF-positive (26.6 vs 38.4%; risk difference –12; –23, –2). However, a similar proportion of patients in the psoriasis and no psoriasis groups satisfied the 1987 ACR criteria for RA (Table 2). There were no differences in the number of tender, swollen or deformed joints in the two groups, nor in the proportion with radiological erosions. However, erosive patients with psoriasis had lower Larsen scores (median 13, IQR 9–26) than erosive patients without psoriasis (median 28, IQR 15–43) (P = 0.0009). Patients with psoriasis had a lower score in the social domain of the SF-36 (62.5 vs 75) (P = 0.006) and the mental component summary score (48.6 vs 51.8) (P = 0.03) but scores in the other domains were similar.


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  		TABLE 2. Outcome at 5 yrs in patients with and without psoriasis recruited from 1990 to 1994

 
Many of the patients with psoriasis were on DMARDs (40.5 vs 29.9%; risk difference 10.6; –0.7, 21.9) although this was not statistically significant. The delay to first DMARD was significantly longer in patients with psoriasis (18 vs 9 months) (P = 0.02) but the total duration of DMARD exposure was approximately the same in the two groups. This suggests that patients with psoriasis are more likely to remain on DMARDs.

We then restricted the analysis to subjects who were RF-negative and compared the difference in outcome in patients with (n = 58) and without (n = 475) psoriasis (Table 3). At baseline, RF-negative patients with psoriasis were younger (48.6 vs 52.6 yrs; P = 0.05) and more likely to be male (46.5 vs 30.5%; risk difference –16; –30, –3). Patients with psoriasis also presented later (10 vs 5 months; P = 0.0006) and were more likely to have forefoot involvement. Perhaps because of the longer disease duration, there was also a longer delay to the initiation of the first DMARD (19 vs 9.3 months; P = 0.01) in patients with psoriasis (Table 4). Again, RF-negative patients with psoriasis were more likely to develop erosions in their hands and feet (37.9 vs 25.3%; risk difference 16.8; 1.5, 32.1), but the degree of erosive damage (Larsen score at 5 yrs) was less (11.5 vs 23.5; P = 0.0003).


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  		TABLE 3. Baseline characteristics of RF-negative patients with and without psoriasis recruited from 1990 to 1994

 

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  		TABLE 4. Outcome at 5 yrs of RF-negative (at baseline) patients with and without psoriasis recruited from 1990 to 1994 adjusted for age and gender

 
Given that the psoriasis patients were more likely to be male, younger and to have been treated with DMARDs, we then explored the relationship between psoriasis and the various outcomes using ordinal logistic regression and negative binomial regression adjusting for these differences (Table 5) in the whole cohort. After adjustment, the only differences between the psoriasis and non-psoriasis groups were in RF positivity [adjusted odds ratio (OR) 0.44; 95% CI 0.25–0.78] and in the Larsen score in patients with erosions (the adjusted Larsen score was 37% lower in the psoriasis group, 95% CI 17–51%). As would be expected, very similar results were obtained when the outcome variables were used to predict which patients had psoriasis using logistic regression (data not shown). RF, Larsen score in the erosive patients and social domain in the SF-36 were the only significant univariate predictors. When entered into a multivariate model (adjusting for age, gender and DMARD use), ever RF-positive (adjusted OR 0.10; 95% CI 0.03–0.30) and Larsen score (adjusted OR 0.97; 95% CI 0.94–1.00) were the only significant predictors in erosive patients. In the whole cohort, ever RF-positive (adjusted OR 0.40; 95% CI 0.22–0.73) and social domain of the SF-36 < 38 (adjusted OR 2.40; 95% CI 1.31–4.42) were the only significant predictors of psoriasis.


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  		TABLE 5. Odds ratio of an individual with psoriasis on examination, scoring in the ‘worse’ category in the outcome variable, registered between 1990 and 1994

 

   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
Acknowledgements
 References
 
This study confirms that patients with psoriasis who develop IP are more likely to be male, develop arthritis at a younger age and to be RF-negative than patients without psoriasis. During follow-up, after allowing for these differences at baseline, the only outcome difference was in the degree of erosive damage in patients who develop erosions. Psoriasis also appears, in some way, to protect against the development of RF—although, nevertheless, in the whole series 17% of psoriatic patients were RF-positive at baseline (Table 1) and 27% by 5 yrs (Table 2). This level of RF-positivity is higher than that generally reported in patients with PsA. RF measurements were performed using latex fixation between 1990 and 1999. We now use nephelometry which is recognized to be more specific. We used the conventional cut-off for RF-positivity (latex titre ≥1/40) and so the likely explanation is that there are patients with psoriasis plus RA included in this cohort who would have been excluded from studies of PsA.

We have previously shown that psoriasis does not influence the short-term outcome of IP [18]. It is now apparent that the presence of psoriasis also does not appear to influence the long-term outcome of IP, having allowed for the fact that most patients are seronegative. This is not to say that there may not be, within this group, a small number of patients with the so-called characteristic features of PsA such as DIP involvement and dactylitis. McHugh et al. [19] found arthritis mutilans and DIP joint disease in less than 5% of a cohort study of 87 PsA patients.

Apart from our earlier report [20], there have been relatively few studies of incidence cohorts of PsA [21, 22]. Punzi et al. [20] and Kane et al. [21] focused on describing the outcome in hospital recruited cohorts of patients with early PsA, and identifying predictors of a poor prognosis within the cohort.

The main strength of this study is that it is primary-care-based with patients recruited close to the onset of their arthritis and followed for 5 yrs. Patients were selected on the basis of the presence of psoriasis on examination of the limbs, face and scalp but without any preconceptions as to the nature of PsA. They were not selected on the basis of hospital referral or a consultant diagnosis of PsA—thus selection bias is avoided. The overall prevalence of psoriasis in this cohort was 9.5%. This compares with an overall prevalence of psoriasis in community surveys of 2–3%. Nevertheless, it is likely that there is some misclassification in the non-psoriasis group—some of whom may have had psoriasis of the trunk or flexural areas. We will also have missed patients with a previous history of psoriasis whose skin disease was in spontaneous or treatment-induced remission on all the occasions they were examined by a nurse. The number of such patients is likely to be a small proportion of the non-psoriasis group. It is also important to emphasize that, because of the recruitment criteria for NOAR, patients with a monoarthritis or isolated spondarthritis are not included. However, patients with an oligoarthritis will be included.

Moll and Wright [2] suggested that PsA was a less severe disease than RA. However, there is mounting evidence from hospital cohorts that this is not so [22]. We have now demonstrated that primary-care-based patients with IP plus psoriasis have a very similar outcome to other patients with RF-negative IP. In the current study, more than 50% of patients had three or more deformed joints by 5 yrs. Gladman [23], in the Toronto hospital-based cohort, found that more than 55% of patients had five or more deformed joints at 5 yrs.

We have found that a similar proportion of patients in the psoriasis and non-psoriasis groups had developed erosions in the hands and/or feet by 5 yrs (36.7 vs 33.8%). This is somewhat lower than the hospital-based inception cohort reported by Kane et al. [21] (47% at 2 yrs), reflecting the primary-care origin of our cohort and despite the delay in starting DMARDs. Like Sokoll and Helliwell [24], we found that the severity of radiological damage was less than that in RA. In a study of 39 matched pairs of X-rays from Toronto (one from a patient with PsA and one from an age, gender and disease duration matched RA patient), the radiological scores were somewhat higher in the RA patients but this did not reach statistical significance [25].

Despite having similar HAQ scores to the patients without psoriasis, the patients with psoriasis and IP had lower scores in the social domain of the SF-36, perhaps because of their skin disease. Husted et al. [26], using the SF-36, found that patients with PsA had less vitality than patients with RA.

In summary, this study highlights two important aspects about the 5-yr outcome of IP in patients with psoriasis: it is not a benign disease and it has a similar outcome to other forms of seronegative IP.

Formula


   Acknowledgements
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
References
 
We acknowledge the contribution of the Rheumatology Department at the Norfolk and Norwich Hospital for their continued support of NOAR. We also thank the local GPs for referring patients and the NOAR metrologists for careful assessment of the patients.

Funding: The Norfolk Arthritis Register is funded as part of the programme grant from the Arthritis Research Campaign to the ARC Epidemiology Unit at the University of Manchester.

Disclosure statement: The authors have declared no conflicts of interest.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Acknowledgements
 References
 

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Submitted 22 August 2007; revised version accepted 5 September 2007.
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