Abstract
Background
Clinical characteristics and manifestations of psoriatic arthritis (PsA) have been extensively studied in western countries, yet data of Korean patients with PsA are very limited. We aimed to investigate the clinical traits of patients with PsA and dissect the characteristics of those with axial involvement.
Methods
In this observational study, we analyzed clinical data of 109 patients with PsA who were enrolled in the Korean College of Rheumatology Biologics and Targeted Therapy registry between December 2012 and March 2022 at the time point of initiating or switching to a biologic agent. Data from 2,221 patients with ankylosing spondylitis (AS) registered during the same period were also analyzed. We divided patients with PsA into patients with or without axial involvement and then added AS patients with psoriasis (total three subgroups) for comparative analyses.
Results
Asymmetric oligoarthritis was the most common clinical manifestation in patients with PsA, followed by symmetric polyarthritis and spondylitis. Our analysis indicated that methotrexate and sulfasalazine were the two most prescribed disease-modifying antirheumatic drugs for patients with PsA before starting biologic therapy. The patients with psoriatic spondylitis had more peripheral joint involvement (P = 0.016), less prior uveitis (P < 0.001), and lower human leukocyte antigen B27 (HLA-B27) positivity (P < 0.001) than the AS patients with psoriasis. Furthermore, syndesmophytes and radiographic sacroiliitis were prevalent among patients with PsA and AS patients with psoriasis who had the HLA-B27 gene.
Graphical Abstract
Psoriatic arthritis (PsA), a subset of spondyloarthritis (SpA), is a chronic inflammatory disease that is generally preceded by psoriasis, and its prevalence is around 6–42% among patients with psoriasis in Western countries.12 The clinical patterns of PsA could be in the form of asymmetric oligoarthritis, symmetric polyarthritis, distal interphalangeal involvement, mutilating arthritis, and spondylitis.3 It can also present with various extra-articular manifestations, such as uveitis.
Studies in Asian countries have shown lower prevalence rates than those from Western countries: 1–13.7% among patients with psoriasis.4567 Two Korean studies have indicated the prevalence of PsA as 9.0–11.2% among patients with psoriasis, and the most common clinical pattern was spondylitis.89 In a study comprising 32 Korean patients with PsA, nail change, dactylitis, and enthesopathy were observed in 36%, 15.4%, and 15.6% patients, respectively.8 They also showed that human leukocyte antigen B27 (HLA-B27) was present in 8% of patients with PsA. However, this was a cross-sectional study from a single center.
Several countries have established national registries that include initial and follow-up data on patients with PsA treated with biologic drugs.101112 The Korean College of Rheumatology Biologics and Targeted Therapy (KOBIO) registry is a large, prospective, observational, disease-based registry initiated in December 2012 that includes data on patients with rheumatoid arthritis (RA), ankylosing spondylitis (AS), and PsA who were initiated on or switched to biologics or targeted synthetic disease-modifying antirheumatic drugs (DMARDs).13 The registry data can provide information on the characteristics and comorbidities of patients in real-world clinical practice.
Though the clinical characteristics and manifestations of PsA have been extensively studied in Western countries, clinical data on Korean patients with PsA are scarce. The aim of this study was to investigate the clinical characteristics of patients with PsA enrolled in a nationwide registry at the time point of initiating or switching to a biologic agent. Furthermore, we intended to dissect the clinical and radiological characteristics of patients with PsA with axial involvement.
This was an observational study using clinical data of patients with PsA registered in the KOBIO registry between December 2012 and March 2022 (Clinicaltrials.gov NCT01965132).13 Patients were eligible for the study if they met the classification criteria for PsA (CASPAR).14 Data of patients with AS were also obtained; patients fulfilled the 1984 modified New York criteria for the diagnosis of AS.15 In South Korea, to obtain a reimbursement of biologic therapy for PsA, patients should have an inadequate response to at least two conventional synthetic DMARDs (csDMARDs) despite treatment for > 6 months. For AS, patients should have an inadequate response to at least two non-steroidal anti-inflammatory drugs or a csDMARD despite treatment for > 3 months. Patients older than 18 years who were started on or switched to other biologics were registered. Patients were enrolled in the registry by rheumatologists, and questionnaires were completed during patient visits as part of routine clinical care. As the Korean National Health Insurance reimburses the cost of biologic DMARDs for patients with PsA who failed to receive relief from at least two conventional DMARDs for 6 months, the registry preferentially included patients with a moderate to severe disease activity. Standardized protocols for patient enrollment and data quality control were monitored by all the participating centers.
Clinical, laboratory, and imaging data of 109 patients with PsA were obtained. We also acquired data of 2,221 patients with AS who were enrolled during the same period. Patients with PsA were divided into those without spondylitis and those with psoriatic spondylitis defined by the designated clinical pattern registered by the rheumatologist; AS patients with psoriasis were included as a comparator group. Lastly, patients with PsA and AS plus psoriasis were grouped together and then stratified according to their HLA-B27 status.
Baseline data at the time of enrollment were used for the analysis. Either the independent Student’s t-test or Mann-Whitney U test was used for continuous variables, and the χ2 test was used for categorical variables. The Kruskal-Wallis test was used for comparing variables among groups. P values of the multiple comparison tests were generated using the Bonferroni correction. All statistical analyses were two-sided and were performed using the SAS statistical software version 9.4 (SAS Institute Inc., Cary, NC, USA). Statistical significance was set at P < 0.05.
The KOBIO registry project was approved by the Institutional Review Board (IRB) of each hospital. The current study protocol was approved by the IRB of Ajou University Hospital (No. AJIRB-MED-MDB-22-146). All procedures were conducted in accordance with principles of the Declaration of Helsinki and good clinical practice guidelines, and all patients provided written informed consent to participate in the development of the registry.
Table 1 shows the clinical characteristics and laboratory findings of 109 patients with PsA and 2,221 patients with AS. The age (mean ± standard deviation) of patients with PsA was 48 ± 11.6 years, and 53.2% were men. Disease duration was 4.4 ± 5.4 years. Among the 109 patients, the most common pattern of PsA was asymmetric oligoarthritis (47.7%), followed by symmetric polyarthritis (40.4%), spondylitis (24.8%), distal interphalangeal involvement (23.9%), and mutilating arthritis (2.8%). The Leeds Enthesitis Index was 0.28 ± 0.67, and the patient global assessment score was 5.56 ± 2.34. The CASPAR score was 3.60 ± 0.96. There was no significant difference in disease duration between patients with PsA and those with AS. HLA-B27 positivity was significantly lower (P < 0.001) in patients with PsA (n = 11, 15.9%) than in those with AS (n = 1,843, 89.2%). Peripheral joint involvement was significantly higher (P < 0.001) in patients with PsA (n = 90, 82.6%) than in those with AS (n = 637, 29%). Additionally, the numbers of tender and swollen joints were both significantly higher (P < 0.001) in patients with PsA than in those with AS. Furthermore, dactylitis was significantly more common (P < 0.001) in patients with PsA (n = 47, 43.5%) than in those with AS (n = 42, 1.9%). Six patients in the PsA group had synovitis, acne, pustulosis, hyperostosis, and osteitis (SAPHO) syndrome.
All values are presented as numbers with corresponding percentages in parentheses or as mean ± standard deviation.
PsA = psoriatic arthritis, AS = ankylosing spondylitis, HLA-B27 = human leukocyte antigen B27, DAS28-ESR = disease activity score 28-erythrocyte sedimentation rate, DAS28-CRP = disease activity score 28-C-reactive protein, ASDAS-ESR = ankylosing spondylitis disease activity score-erythrocyte sedimentation rate, ASDAS-CRP = ankylosing spondylitis disease activity score-C-reactive protein, ESR = erythrocyte sedimentation rate, CRP = C-reactive protein, CASPAR = classification criteria for psoriatic arthritis, SAPHO = synovitis, acne, pustulosis, hyperostosis, and osteitis.
In patients with PsA, the combined comorbidities (Table 2) in a descending order of frequency were hyperlipidemia (n = 39, 35.8%), hypertension (n = 32, 29.4%), anemia (n = 17, 15.6%), obesity (n = 11, 10.1%), and osteoporosis (n = 10, 9.2%). In patients with AS, anemia was the most common comorbidity (n = 471, 21.2%), followed by hypertension (n = 360, 16.2%), hyperlipidemia (n = 318, 14.3%), and obesity (n = 117, 5.3%).
The most prescribed DMARDs in patients with PsA (Table 3) prior to initiation of biologics were methotrexate (90.8%), sulfasalazine (70.6%), leflunomide (18.4%), and cyclosporine (18.4%). The most prescribed biologic agent at enrollment was adalimumab or its biosimilars (n = 44, 40.4%), followed by etanercept or its biosimilars (n = 21, 19.3%), golimumab (n = 15, 13.8%), and secukinumab (n = 14, 12.8%). In patients with AS, the commonly prescribed DMARDs prior to initiation of biologics were sulfasalazine (n = 1,683, 75.8%), methotrexate (n = 556, 25%), and leflunomide (n = 65, 2.9%). The commonly prescribed biologics for the treatment of AS at enrollment were adalimumab or its biosimilars (n = 875, 39.4%), infliximab or its biosimilars (n = 465, 20.9%), golimumab (n = 446, 20.1%), and etanercept or its biosimilars (n = 393, 17.7%).
We compared the clinical characteristics of PsA patients with or without axial involvement: patients with PsA without spondylitis (n = 82, group 1), with psoriatic spondylitis (n = 27, group 2), and as a comparator group, patients with AS with psoriasis (n = 78, group 3) (Table 4). The patients in group 1 (age: 48.8 ± 12 years) were significantly older (P < 0.001) than those in groups 2 (age: 45.3 ± 10.3 years) and 3 (age: 40.8 ± 11.1 years). There were no significant differences between the body mass index and smoking status of patients in the groups. HLA-B27 was positive in 14%, 21.1%, and 76% of patients in groups 1, 2, and 3, respectively. Peripheral joint involvement was significantly (P < 0.001) more common in group 1 (n = 73, 89%) than in groups 2 (n = 17, 63%) and 3 (n = 26, 33.8%). There was no significant difference in the incidence of enthesitis between the groups. Significantly fewer syndesmophytes (P < 0.001) were observed in group 1 (n = 2, 4.1%) than in groups 2 (n = 6, 25%) and 3 (n = 29, 38.8%).
All values are presented as numbers with corresponding percentages in parentheses.
PsA = psoriatic arthritis, AS = ankylosing spondylitis, CASPAR = classification criteria for psoriatic arthritis, ESR = erythrocyte sedimentation rate, CRP = C-reactive protein, HLA-B27 = human leukocyte antigen B27, SAPHO = synovitis, acne, pustulosis, hyperostosis, and osteitis, RAPID3 = routine assessment of patient index data 3, PGA = patient global assessment, SI = sacroiliac.
Furthermore, we combined the three groups and then divided them into two subgroups according to their HLA-B27 status (Supplementary Table 1). The age of patients who were HLA-B27 positive (+) and HLA-B27 negative (−) was similar (42.2 ± 11.7 vs. 44.7 ± 11.0 years; P = 0.198). Disease duration was significantly longer in HLA-B27 (+) patients than in HLA-B27 (−) patients (5.8 ± 6.6 vs. 3.6 ± 5.4 years; P = 0.024). Erythrocyte sedimentation rate was significantly higher in HLA-B27 (+) patients than in HLA-B27 (−) patients (37.8 ± 34.5 vs. 22.8 ± 20.3 mm/h; P = 0.002). On the other hand, peripheral joint involvement was significantly more common (P < 0.001) in HLA-B27 (−) patients (n = 56, 74.7%) than in HLA-B27 (+) patients (n = 25, 36.8%). Although dactylitis was significantly more common (P < 0.001) in HLA-B27 (−) patients (n = 28, 37.8%) than in HLA-B27 (+) patients (n = 5, 7.4%), the incidence of enthesitis was comparable between the two subgroups. Radiographic sacroiliitis (P < 0.001) and syndesmophytes (P < 0.001) were significantly more frequent in HLA-B27 (+) patients.
This study described the distinct clinical features, comorbidities, and medication history of 109 Korean patients with PsA by comparing their characteristics with those of patients with AS. Furthermore, the clinical characteristics of patients with PsA with or without spondylitis were also compared. Despite the fact that patients with PsA needed biologics mainly to control peripheral arthritis, we verified that spondylitis is indeed a common pattern in Korean patients with PsA.
The most common manifestation of joint involvement in PsA has been different in various reports.8161718192021 Some studies have indicated that oligoarthritis, occurring in 37–67% of patients with PsA, is the most common arthropathy in PsA.2021 However, recent studies have shown that polyarthritis is the most common manifestation.1618 One study reported that polyarthritis (38.9%) was more frequent than other manifestations, and its detection rate was higher because of a longer duration of follow-up in the polyarticular group.18 Studies conducted in South Korea showed that spondylitis was the most common clinical pattern of PsA.89 A recent study suggested that racial differences may be associated with the clinical manifestation patterns of PsA.9 In our study, the most common pattern was asymmetric oligoarthritis, which was present in 47.7% of patients. This was followed by symmetric polyarthritis (40.4%), spondylitis (24.8%), distal interphalangeal involvement (23.9%), and mutilating arthritis (2.8%). This result is consistent with the results of some studies161819 but inconsistent with those of previous studies from South Korea.89 This discrepancy could be attributed to dissimilar disease activities of enrolled patients, disease duration, and study methods. As our study used data from the KOBIO-PsA registry, patients tended to have a higher disease activity and shorter disease duration.
Recent studies showed that over half of the patients with PsA have more than one comorbidity, which has a significant impact on their quality of life.222324 In addition, some studies have revealed that similar to patients with RA, patients with PsA have a higher prevalence and incidence of cardiovascular diseases, such as ischemic heart disease and stroke, than the general population.2425 In our study, the comorbidities related to the risk of cardiovascular diseases in patients with PsA were hypertension (29.4%), diabetes mellitus (12.8%), and hyperlipidemia (35.8%). The rates are somewhat higher than those of patients with AS possibly because patients with PsA were older than those with AS. When these results were compared to those of a study of Korean patients with PsA, the prevalence of risk factors was comparable; hypertension (33.4%), diabetes mellitus (16.2%), and hyperlipidemia (14.9%).26 However, we were unable to compare the prevalence of comorbidities in patients with PsA vs. the general population. Furthermore, the mean disease duration of our patients with PsA was relatively shorter than that reported in previous studies.2728
Despite the fact that meta-analysis studies have shown that conventional DMARDs have an inadequate efficacy for treating PsA, they are still the most prescribed class of drugs for treating PsA.29 Methotrexate, sulfasalazine, and leflunomide are the commonly prescribed conventional DMARDs, especially for peripheral arthritis.30 Systemic glucocorticoids are not recommended for treating PsA because they could cause post-steroid flares of psoriasis. Various studies have revealed the efficacy of several biologics, such as anti-tumor necrosis factor agents or secukinumab, in treating patients with PsA who were refractory to conventional DMARDs.2930 Our study showed that the drugs most commonly used before biologics were methotrexate (90.8%) and sulfasalazine (70.6%). Fifty-five (50.5%) patients were still being treated with oral glucocorticoids in real-world practice. Peripheral joint involvement was observed in 82.6% of patients. However, the numbers of tender and swollen joints were lower than those reported in previous studies based on nationwide registries.1011 Our patients had a mean disease duration of 4.37 years at the time of initiation of or switching to biologics. Several biologics, including etanercept, adalimumab, infliximab, golimumab, and secukinumab, were used at a relatively even ratio in patients with PsA, although the most common biologic was adalimumab or its biosimilars. The number of users of ustekinumab, which is an interleukin (IL)-12/IL-23 inhibitor, was relatively small. Notably, most of the patients (82.6%) were treated with a conventional DMARD in addition to biologics.
PsA is a key subset of SpA that could have or incidentally be found to have axial involvement.1431 In patients with PsA predominantly having axial symptoms, inflammatory back pain and stiffness can be similar to the degree observed in patients with AS.32 A recent study showed that the presence of axial involvement was associated with a higher likelihood of moderate or severe skin lesions, higher disease activity, and greater effect on the quality of life.33 As only a subgroup of patients with PsA had axial involvement, we evaluated the clinical characteristics of patients with psoriatic spondylitis and those with AS. Consistent with previous reports, our study demonstrated that patients with psoriatic spondylitis had more peripheral joint involvement and a lower rate of HLA-B27 positivity and prior uveitis than AS patients with psoriasis.213435 We also found that HLA-B27 (+) patients had a higher erythrocyte sedimentation rate and less frequent peripheral joint involvement and dactylitis than HLA-B27 (−) patients. A long-term prospective study of psoriatic spondylitis showed a significant increase in the number of patients with syndesmophytes and sacroiliitis, despite no significant increase in the number of patients with inflammatory back pain and stiffness.3637 This shows that long-term radiographic progression of patients with PsA with axial manifestations seems to be independent of their spinal mobility.3637 Altogether, these results suggest that structural changes, such as syndesmophytes or radiographic sacroiliitis, are more likely to be associated with HLA-B27 positivity in patients with psoriatic spondylitis.
Our study has some limitations. First, this observational study mainly included patients with PsA and AS who had high disease activity and needed biologic therapy. Second, the number of patients with PsA was relatively small for a subgroup analysis. Third, we were unable to compare the data of patients with PsA on a stable regimen of conventional DMARDs. Further investigations using health insurance claims data are currently underway.
In conclusion, we showed that the degree of peripheral arthritis is less severe in Korean patients with PsA who require biologics than that reported in the literature. Furthermore, our study reiterates that psoriatic spondylitis is a common and important clinical pattern in Korean patients with PsA.
ACKNOWLEDGMENTS
The authors thank the Korean College of Rheumatology Biologics and Targeted Therapy (KOBIO) study team for aiding in data management and preparation.
Notes
Author Contributions:
Conceptualization: Kim HA, Shin K.
Data curation: Kim HA, Lee E, Park SY, Shin K.
Formal analysis: Kim HA, Lee E, Shin K.
Investigation: Kim HA, Lee E, Shin K.
Methodology: Kim HA, Lee E, Shin K.
Project administration: Kim HA, Lee E, Park SY, Lee SS, Shin K.
Visualization: Kim HA, Lee E, Park SY, Shin K.
Writing - original draft: Kim HA, Shin K.
Writing - review & editing: Kim HA, Lee E, Park SY, Lee SS, Shin K.
References
2. Karmacharya P, Chakradhar R, Ogdie A. The epidemiology of psoriatic arthritis: a literature review. Best Pract Res Clin Rheumatol. 2021; 35(2):101692. PMID: 34016528.
3. Veale DJ. Psoriatic arthritis: recent progress in pathophysiology and drug development. Arthritis Res Ther. 2013; 15(6):224. PMID: 24611179.
4. Mohd Affandi A, Khan I, Ngah Saaya N. Epidemiology and clinical features of adult patients with psoriasis in Malaysia: 10-year review from the Malaysian Psoriasis Registry (2007-2016). Dermatol Res Pract. 2018; 2018:4371471. PMID: 29849578.
5. Kishimoto M, Yoshida K, Ichikawa N, Inoue H, Kaneko Y, Kawasaki T, et al. Clinical characteristics of patients with spondyloarthritis in Japan in comparison with other regions of the world. J Rheumatol. 2019; 46(8):896–903. PMID: 30770497.
6. Fan X, Yang S, Sun LD, Liang YH, Gao M, Zhang KY, et al. Comparison of clinical features of HLA-Cw*0602-positive and -negative psoriasis patients in a Han Chinese population. Acta Derm Venereol. 2007; 87(4):335–340. PMID: 17598037.
7. Choi JW, Kim BR, Seo E, Youn SW. Could psoriatic arthritis be easily diagnosed from current suspicious physical findings in the dermatology clinic? Ann Dermatol. 2017; 29(1):48–54. PMID: 28223746.
8. Baek HJ, Yoo CD, Shin KC, Lee YJ, Kang SW, Lee EB, et al. Spondylitis is the most common pattern of psoriatic arthritis in Korea. Rheumatol Int. 2000; 19(3):89–94. PMID: 10776686.
9. Shin D, Kim HJ, Kim DS, Kim SM, Park JS, Park YB, et al. Clinical features of psoriatic arthritis in Korean patients with psoriasis: a cross-sectional observational study of 196 patients with psoriasis using psoriatic arthritis screening questionnaires. Rheumatol Int. 2016; 36(2):207–212. PMID: 26395992.
10. Saad AA, Ashcroft DM, Watson KD, Hyrich KL, Noyce PR, Symmons DP, et al. Persistence with anti-tumour necrosis factor therapies in patients with psoriatic arthritis: observational study from the British Society of Rheumatology Biologics Register. Arthritis Res Ther. 2009; 11(2):R52. PMID: 19356232.
11. Glintborg B, Østergaard M, Dreyer L, Krogh NS, Tarp U, Hansen MS, et al. Treatment response, drug survival, and predictors thereof in 764 patients with psoriatic arthritis treated with anti-tumor necrosis factor α therapy: results from the nationwide Danish DANBIO registry. Arthritis Rheum. 2011; 63(2):382–390. PMID: 21279995.
12. Heiberg MS, Kaufmann C, Rødevand E, Mikkelsen K, Koldingsnes W, Mowinckel P, et al. The comparative effectiveness of anti-TNF therapy and methotrexate in patients with psoriatic arthritis: 6 month results from a longitudinal, observational, multicentre study. Ann Rheum Dis. 2007; 66(8):1038–1042. PMID: 17213251.
13. Kim J, Koh JH, Choi SJ, Jeon CH, Kwok SK, Kim SK, et al. KOBIO, the first web-based Korean Biologics Registry operated with a unified platform among distinct disease entities. J Rheum Dis. 2021; 28(4):176–182.
14. Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H, et al. Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum. 2006; 54(8):2665–2673. PMID: 16871531.
15. van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum. 1984; 27(4):361–368. PMID: 6231933.
16. Yamamoto T, Ohtsuki M, Sano S, Igarashi A, Morita A, Okuyama R, et al. Epidemiological analysis of psoriatic arthritis patients in Japan. J Dermatol. 2016; 43(10):1193–1196. PMID: 26992450.
17. Song Z, Deng X, Xie W, Li B, Zhang Z. Clinical characteristics of psoriatic arthritis in Chinese patients: a cross-sectional study. Rheumatol Ther. 2021; 8(4):1845–1857. PMID: 34665456.
18. Dönmez S, Pamuk ON, Akker M, Ak R. Clinical features and types of articular involvement in patients with psoriatic arthritis. Clin Rheumatol. 2015; 34(6):1091–1096. PMID: 25066919.
19. Gunal EK, Kamali S, Gul A, Ocal L, Konice M, Aral O, et al. Clinical evaluation and comparison of different criteria for classification in Turkish patients with psoriatic arthritis. Rheumatol Int. 2009; 29(4):365–370. PMID: 18766345.
20. Nossent JC, Gran JT. Epidemiological and clinical characteristics of psoriatic arthritis in northern Norway. Scand J Rheumatol. 2009; 38(4):251–255. PMID: 19247847.
21. Salvarani C, Lo Scocco G, Macchioni P, Cremonesi T, Rossi F, Mantovani W, et al. Prevalence of psoriatic arthritis in Italian psoriatic patients. J Rheumatol. 1995; 22(8):1499–1503. PMID: 7473473.
22. Azevedo S, Santos-Faria D, Leite Silva J, Ramos Rodrigues J, Sousa Neves J, Peixoto D, et al. Obesity, metabolic syndrome and other comorbidities in rheumatoid arthritis and psoriatic arthritis: influence on disease activity and quality of life. Acta Reumatol Port. 2019; 44(4):322–324. PMID: 32281967.
23. Hackett S, Ogdie A, Coates LC. Psoriatic arthritis: prospects for the future. Ther Adv Musculoskelet Dis. 2022; 14:1759720X221086710.
24. Jamnitski A, Symmons D, Peters MJ, Sattar N, McInnes I, Nurmohamed MT. Cardiovascular comorbidities in patients with psoriatic arthritis: a systematic review. Ann Rheum Dis. 2013; 72(2):211–216. PMID: 22532629.
25. Horreau C, Pouplard C, Brenaut E, Barnetche T, Misery L, Cribier B, et al. Cardiovascular morbidity and mortality in psoriasis and psoriatic arthritis: a systematic literature review. J Eur Acad Dermatol Venereol. 2013; 27(Suppl 3):12–29. PMID: 23845149.
26. Oh EH, Ro YS, Kim JE. Epidemiology and cardiovascular comorbidities in patients with psoriasis: a Korean nationwide population-based cohort study. J Dermatol. 2017; 44(6):621–629. PMID: 28191654.
27. Zisman D, Eder L, Elias M, Laor A, Bitterman H, Rozenbaum M, et al. Clinical and demographic characteristics of patients with psoriatic arthritis in northern Israel. Rheumatol Int. 2012; 32(3):595–600. PMID: 21120489.
28. Husted JA, Thavaneswaran A, Chandran V, Eder L, Rosen CF, Cook RJ, et al. Cardiovascular and other comorbidities in patients with psoriatic arthritis: a comparison with patients with psoriasis. Arthritis Care Res (Hoboken). 2011; 63(12):1729–1735. PMID: 21905258.
29. Soriano ER, Acosta-Felquer ML, Luong P, Caplan L. Pharmacologic treatment of psoriatic arthritis and axial spondyloarthritis with traditional biologic and non-biologic DMARDs. Best Pract Res Clin Rheumatol. 2014; 28(5):793–806. PMID: 25488785.
30. Vivekanantham A, McGagh D, Coates LC. Current treatments and recommendations for psoriatic arthritis. Best Pract Res Clin Rheumatol. 2021; 35(2):101680. PMID: 33824068.
31. Rudwaleit M, Landewé R, van der Heijde D, Listing J, Brandt J, Braun J, et al. The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part I): classification of paper patients by expert opinion including uncertainty appraisal. Ann Rheum Dis. 2009; 68(6):770–776. PMID: 19297345.
32. Baraliakos X, Coates LC, Braun J. The involvement of the spine in psoriatic arthritis. Clin Exp Rheumatol. 2015; 33(5):Suppl 93. S31–S35.
33. Mease PJ, Palmer JB, Liu M, Kavanaugh A, Pandurengan R, Ritchlin CT, et al. Influence of axial involvement on clinical characteristics of psoriatic arthritis: analysis from the Corrona Psoriatic Arthritis/Spondyloarthritis Registry. J Rheumatol. 2018; 45(10):1389–1396. PMID: 29961691.
34. Queiro R, Sarasqueta C, Belzunegui J, Gonzalez C, Figueroa M, Torre-Alonso JC. Psoriatic spondyloarthropathy: a comparative study between HLA-B27 positive and HLA-B27 negative disease. Semin Arthritis Rheum. 2002; 31(6):413–418. PMID: 12077714.
35. Feld J, Ye JY, Chandran V, Inman RD, Haroon N, Cook R, et al. Is axial psoriatic arthritis distinct from ankylosing spondylitis with and without concomitant psoriasis? Rheumatology (Oxford). 2020; 59(6):1340–1346. PMID: 31593590.
36. Hanly JG, Russell ML, Gladman DD. Psoriatic spondyloarthropathy: a long term prospective study. Ann Rheum Dis. 1988; 47(5):386–393. PMID: 3260473.
37. Chandran V, Barrett J, Schentag CT, Farewell VT, Gladman DD. Axial psoriatic arthritis: update on a longterm prospective study. J Rheumatol. 2009; 36(12):2744–2750. PMID: 19884276.