Symptoms dermatologists should look for in daily practice to improve detection of psoriatic arthritis in psoriasis patients: an expert group consensus

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1 DOI: /jdv JEADV ORIGINAL ARTICLE Symptoms dermatologists should look for in daily practice to improve detection of psoriatic arthritis in psoriasis patients: an expert group consensus A.P. Villani, 1, * M. Rouzaud, 2 M. Sevrain, 3 T. Barnetche, 4 C. Paul, 5 M.-A. Richard, 6 M. Beylot-Barry, 2 L. Misery, 3 P. Joly, 7 S. Aractingi, 8 F. Aubin, 9 M. Le Ma^ıtre, 10 A. Cantagrel, 11 J.-P. Ortonne, 12 D. Jullien 1 1 Dermatology Department, Lyon University, Edouard Herriot Hospital, Lyon, France 2 Dermatology Department, CHU Bordeaux, University Bordeaux, Bordeaux, France 3 Dermatology Department, Morvan University Hospital, Brest, France 4 Rheumatology Department, Bordeaux University Hospital, Bordeaux, France 5 Dermatology Department, Paul Sabatier University, UMR CNRS 5165, INSERM 1056, Toulouse, France 6 Aix-Marseille University, UMR 911, INSERM CRO2, Assistance Publique and Dermatology Department, Timone Hospital, Marseille, France 7 Clinique Dermatologique, Rouen University Hospital, Inserm U905, Institute for Research and Innovation in Biomedicine (IRIB), Rouen University, Normandy, France 8 Dermatology Department, Cochin Tarnier Hospital, APHP, Paris 5 Descartes University, INSERM UMR S 938, UPMC, CDR Saint- Antoine Hospital, Paris, France 9 Dermatology Department, Besancßon University Hospital and University of Franche-Comte, Besancßon, France 10 Dermatologist (private practice), Caen, France 11 Rheumatology Center, Purpan Teaching Hospital, Toulouse, France 12 Dermatology Department, Nice University, L Archet II Hospital, Nice, France *Correspondence: A.P. Villani. axel.villani@chu-lyon.fr Abstract Background Up to 29% of patients with psoriasis seen by dermatologists have undiagnosed psoriatic arthritis (PsA). As early detection of PsA may be associated with improved joint and skin outcomes, it is essential for dermatologists to improve their ability to diagnose PsA. Skin and nail features of psoriasis associated with PsA are well known to dermatologists but they may feel less confortable assessing other symptoms and they rarely use PsA screening questionnaires. Objective To develop a limited list of clinical signs and symptoms that a dermatologist should be looking for in a psoriasis patient in addition to specific skin features and nail involvement, to improve PsA detection. Methods A systematic search was performed in Pubmed, Cochrane and Embase databases to identify clinical key symptoms associated with PsA. It yielded 27 studies in which we extracted a list of clinical signs and symptoms observed in PsA and submitted it to a panel of dermatology experts through a DELPHI selection process. The experts had to determine which minimal set of signs and symptoms dermatologists should look for in daily practice to improve detection of PsA in patients with psoriasis. Results The four items that received a score higher than 90% in the DELPHI process were finally selected. Those items were as follows: peripheral inflammatory pain (100%), axial inflammatory pain (95.3%), dactylitis (93%), buttock and sciatic pain (90.7%). The remaining items: distal interphalangeal joints (DIPs) involvement (83.7%), Talalgia (79.1%), swollen Achille s tendon (41.9%), costo-chondral involvement (32.6%), uveitis (7%), mouth ulcerations (2.3%), were not retained. Conclusion We propose a set of four items to screen psoriasis patients for psoriatic arthritis for routine clinical use by dermatologists. Accepted: 8 April 2014 Conflicts of interest All the authors have been paid as consultants of AbbVie. In addition, Selim Aractingi has been paid as a consultant for board meetings or symposia by AbbVie, Jansen, Pfizer; Marie Beylot-Barry has been paid as a consultant for Janssen- Cilag, Pfizer, MSD, AbbVie and an investigator for AbbVie, Amgen, Novartis, Celgene; Pascal Joly has been paid as a consultant for Novartis, Janssen, AbbVie and Roche; Denis Jullien has been paid as a consultant and/or investigator and/or speaker for, and/or he has been reimbursed for conference attendance by: Janssen-Cilag, Novartis, Pfizer, MSD, AbbVie, Lilly, Theradiag; Laurent Misery has been paid as a consultant for Abbvie, Amgen, Janssen, Novartis, Pfizer;

2 28 Villani et al. Marie-Aleth Richard has been an investigator for Amgen, Lilly, Novartis, and Leo Pharma and a paid consultant for MSD, Pfizer, Novartis, Janssen, AbbVie, UCB Funding sources AbbVie provided financial support for publication but took no further part in the project. The authors have no financial interest in the subject matter or materials discussed in the manuscript. Introduction Psoriasis is a chronic inflammatory skin disease, with a prevalence that ranges from 0.91% (United States) to 8.5% (Norway) in Western countries. 1 Psoriatic arthritis (PsA) prevalence among psoriasis patients varies widely and increases with time since psoriasis diagnosis, reaching 20.5% after 30 years. 2 The potential risk of tissue destruction associated with PsA 3,4 has triggered efforts aimed at improving treatment strategies. The TICOPA (TIght COntrol of early Psoriatic Arthritis) trial addressed the benefit of tight control of early PsA defined as PsA with less than 24 months symptom duration. 5 Tight control of PsA was shown to significantly improve joint outcomes for early PsA patients when compared to a standard care protocol (OR = 2.36, 95% CI: [1.25, 4.47] for the ACR50 response and OR = 2.64, 95% CI: [1.32, 5.26] for the ACR70 response). Therefore, early detection of PsA may be critical to improve optimal PsA management and outcome. In 84% of patients with psoriasis and PsA, skin lesions precede PsA indicating dermatologists are at the forefront for early PsA detection. 6 The mean time to occurrence of PsA in psoriasis is 12 years, 6 which provides dermatologists with recurrent opportunities to detect rheumatologic involvement. Nevertheless, an epidemiological study has recently shown that up to 29% of patients with psoriasis seen by dermatologists have undiagnosed PsA. 7 Skin predictors of PsA have been identified in patients with psoriasis: scalp involvement, nail dystrophy, intergluteal and perianal lesions as well as large body surface area involvement. 8,9 These predictors which are reviewed elsewhere in this issue 9 are well known to dermatologists. Dermatologists may, however, feel less confortable to assess the joint symptoms associated with PsA. Although several questionnaires have been developed to help physician screening patients for PsA, none of them 7 is commonly used in daily dermatological practice. Most of these questionnaires are relatively sophisticated and may be too time consuming for implementation in everyday dermatology practice. Defining a small set of questions to screen psoriasis patients for PsA might be a more feasible approach for routine clinical use. The aim of this study was to develop a limited set of clinical signs and symptoms that a dermatologist should investigate systematically in psoriasis patients in addition to specific skin features and nail involvement, to allow for early PsA detection. The intention was to develop an easy to use method for routine implementation in dermatology clinics. The results from this study helped to develop new French recommendations on the role of dermatologists in the diagnosis and management of PsA. 16 Material and methods A list of key clinical symptoms associated with PsA was derived from the CASPAR criteria for PsA, 17 the Moll and Wright criteria for PsA 18 and from published PsA screening questionnaires ,19 A systematic search was performed in Pubmed, Cochrane and Embase databases to identify additional clinical symptoms associated with PsA including early PsA. The search included studies published between January 1980 and February 2013 and used combinations of the words arthritis, psoriatic and diagnosis from the Medical Subject Headings (MeSH). A total of 856 eligible articles were identified. On the basis of title, Figure 1 Potentially relevant studies screened for retrieval n = 856 (Pubmed = 549, Embase = 209, Cochrane Library = 98) Studies excluded (reading of article) n = 15 Potentially appropriate studies for systematic review n = 27 Study selection flowchart. Studies excluded (reading of title or abstract) n = 820 Studies added (systematic research on PsA prevalence) n = 6

3 Signs and symptoms of psoriatic arthritis 29 Table 1 PsA screening questionnaires used to extract key signs and symptoms of PsA and their sensitivity (Se) and specificity (Sp) in initial validation studies and in the study by Haroon et al. for PASE, PEST and the ToPAS Questionnaire Full name Initial validation study Haroon et al. study 7 Se (%) Sp (%) Se (%) Sp (%) EARP Early Psoriatic Arthritis Screening questionnaire NA NA GEPARD GErman Psoriasis ARthritis Diagnostic questionnaire NA NA PASQ Psoriatic Arthritis Screening Questionnaire NA NA PAQ Psoriasis and Arthritis Questionnaire NA NA PASE Psoriatic Arthritis Screening and Evaluation PEST Psoriasis Epidemiology Screening Tool ToPAS Toronto Psoriatic Arthritis Screening questionnaire Questionnaires are listed alphabetically, NA = non-available. abstract and full-text reading, 27 studies were selected (Fig. 1). 3,17,19 44 Three of them were specifically dedicated to early PsA (<12 months symptom duration in these three studies), 27,30,32 the others were prevalence studies or studies which systematically listed clinical features of the patients. The list was developed by two of the authors (AV and DJ) with the input of members of the scientific committee (TB, CP, MAR, MBB, LM, PJ, MLM, SA, FA, AC, JPO). The clinical symptoms related to similar clinical forms of PsA were grouped together. Statement understandable by patients was also produced. The resulting list (Table 1) was submitted to a panel of 43 dermatology experts through a DELPHI survey. Experts had to answer the question: in the following list, choose the symptoms a dermatologist should systematically investigate to detect PsA when seeing psoriasis patients. Items chosen by more than 90% of dermatologists from the expert panel were finally selected. Results The four items that received a score higher than 90% were: peripheral inflammatory pain (100%), axial inflammatory pain (95.3%), dactylitis (93%), buttock and sciatic pain (90,7%). The remaining items: distal interphalangeal joints (DIPs) involvement (83.7%), talalgia (79.1%), swollen Achille s tendon (41.9%), costo-chondral involvement (32.6%), uveitis (7%), mouth ulcerations (2.3%), were not selected. Complete results are shown in Fig. 2. Discussion We have identified through DELPHI survey a list of four clinical key signs and symptoms that dermatologists should be looking for in psoriasis patients to improve PsA detection. This list was established by a panel of 43 dermatologists who reached a >90% agreement on the adequacy and the feasibility of the list to be implemented in routine clinical use. Many PsA screening questionnaires have been developed in the past 20 years to help practitioners screening psoriasis patients for PsA ,19 However, community dermatologists almost never use those questionnaires. There are several potential explanations for this. Most of these questionnaires were developed and validated in English without linguistic, cultural and psychometric validation in other languages. Some, like the ToPAS include questions investigating the likelihood of skin psoriasis in patients and have little relevance for dermatologists. Many are complex 11,13 and lengthy to complete (up to 5 7 min for the PASE). 11 Furthermore, the diagnostic properties of most of the questionnaires have not been fully validated outside centres of excellence. Although most questionnaires perform very well in their validation study population, 10 13,15 lower performance 7 of the three most commonly used questionnaires (PASE, PEST, ToPAS, see Table 1) has been shown in a broader population. Considering these issues, the primary objective of this consensus work was to establish a short list of clinical signs and symptoms a dermatologist should systematically investigate in psoriasis patients to help diagnose PsA early. Results of the DELPHI survey showed a biphasic distribution of the PsA signs and symptoms submitted to the experts: six items obtained about 80% of the votes or more and four items around 40% or less (Fig. 2). Only four clinical features were considered as essential by dermatologists for PsA diagnosis: peripheral inflammatory pain, axial inflammatory pain, dactylitis and buttock and sciatic pain. These four features can be investigated through simple questions in daily practice by physicians who see psoriasis patients. 32 The questions we proposed are listed in Table 2. The highest rated symptom by the experts was inflammatory pain. This is in accordance with the CASPAR criteria, the gold standard for PsA diagnosis, which considers inflammatory arthritis as an absolute prerequisite. The interest of assessing this symptom is further supported by the study from Bonifati et al., showing that inflammatory arthritis occurred in 100% of early PsA patients (60.6% polyarthritis and 39.4% oligoarthritis). Distal interphalangeal (DIP) joints involvement item was not selected in the final list. It represents a major sign of peripheral

4 30 Villani et al. Figure 2 Complete DELPHI results: the items selected with a 90% cut-off appear in orange, the items selected with an 80% cut-off appear in blue. PsA helping to differentiate from rheumatoid arthritis. McGonagle et al. formulated the hypothesis that the initial site of inflammation in peripheral PsA could be enthesitis of the extensor tendon of the fingers. 45 By contiguity, inflammation would spread to the DIP joint and to the nail plate (psoriatic nail disease). 46 Using MRI, it was shown that inflammation of the DIP joints extended to the nail bed in patients with both psoriasis and PsA. Therefore, assessing the hands of a psoriasis patient is important to detect peripheral PsA. Dermatologists usually screen patients for nail dystrophy and may investigate DIP involvement at the same time. In the study by Bonifati et al., 32 DIP involvement was found in 36% of the patients. DIP involvement has to be considered with caution as it may be linked to several other conditions, notably osteoarthritis which may sometimes be difficult to differentiate from PsA. Enthesitis and dactylitis are other important symptoms of early PsA. In the aforementioned study by Bonifati et al., enthesitis and dactylitis were found, respectively, in 39% and 27% of patients respectively. Dactylitis is present in our final list of questions. Plantar talalgia was selected by 79% of the experts but Achilles tendon swelling (41.9%) and costo-chondral pain (32.6%) were not considered as priority for investigation by the majority of assessors. Swollen or painful Achille s tendon is an important sign of enthesitis and is part of the items of the Leeds Enthesitis Index 47 and the EARP questionnaire. 10 The fact it was not selected may indicate that dermatologists are not familiar with enthesitis assessment, leading them to neglect these symptoms. Outside of enthesitis, our short list contains the three most frequent clinical symptoms observed in early PsA (inflammatory arthritis, DIP involvement and dactylitis) and may improve early PsA detection/screening by dermatologists. The EARP questionnaire 10 which was designed to detect early PsA also contains these items. The other items of the EARP are feet or ankles pain, elbow or hips pain, swollen Achille s tendon and the question Have you taken anti-inflammatory more than twice a week for joint pain in the last 3 months?. Though interesting, this last item was not selected for the DELPHI survey as it is not primarily a clinical symptom. Inflammatory back pain was found in only 15.1% of the patients of Bonifati et al. study 32 and is not part of the EARP questionnaire. Although axial involvement is important for PsA screening it may be less important for early PsA screening. As early treatment of axial forms of PsA may be critical to avoid joint destruction, rapid diagnosis is important. Inadequate

5 Signs and symptoms of psoriatic arthritis 31 Table 2 Selected symptoms of psoriatic arthritis before DELPHI process No Clinical signs and symptoms 1 Peripheral Inflammatory arthritis Inflammatory arthritis* in hands, fingers, wrists, shoulders, knees and feet *night wake up, morning stiffness, swollen joints Do you wake up at night due to joint pain? Do you suffer from morning stiffness? Have you ever had swollen joints? 2 Axial Inflammatory arthritis Inflammatory arthritis** in the cervix or in the dorso-lumbar area ** night wake up, morning stiffness Do you wake up at night due to joint pain? Are your joints stiff when you wake up in the morning? 3 Dactylitis Have you ever had one painful and swollen finger (sausage-like finger)? 4 Inflammatory buttock pain or sciatic pain Have you ever had pain in your buttocks? Have you ever been diagnosed with sciatica? 5 Distal interphalangeal joints involvement 6 Plantar talalgia 7 Swollen or painful Achille s tendon 8 Costo-chondral pain (spontaneous or under pressure) 9 Uveitis 10 Mouth ulcers detection of patterns of arthritis other than polyarticular disease is supposed to be one of the reasons that account for the poor sensitivity of some PsA questionnaires in some studies. 7 We believe that our list provides a rapid assessment of enthesitis, peripheral and axial involvement and is short enough to be incorporated in daily practice. There are several limitations in our work. Our initial list of ten items was developed in French, and the DELPHI survey explored only French dermatologist s thoughts. Cross-cultural validation will be required. The initial list could easily be translated in other languages and a similar DEPHI survey as the one we performed could be implemented in other countries. The sensitivity, the specificity and the acceptability of this short list of items need to be tested with dermatologists who handle patients with skin psoriasis in all kind of settings, notably private practice. Although we cannot exclude it may perform less well than the available validated screening questionnaires, our goal was to propose a tool that can fit easily in daily practice and therefore that is more suitable to be used widely. Conclusion Dermatologists play a key role in identifying PsA at an early stage when progressive structural damage may be avoided or minimized. The most important question dermatologists should ask their psoriasis patients is whether they have inflammatory joint pain or not. We propose a limited set of four questions investigating PsA suitable for routine use in dermatology clinical practice. 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