Assessment of enthesitis in patients with psoriasis: relationships with clinical features, screening questionnaires results, and quality of life – An ultrasound study

  • Dragan Dulović Military Medical Academy, Institute of Radiology
  • Nemanja Rančić Military Medical Academy, Center for Clinical Pharmacology
  • Ksenija Božić Military Medical Academy, Clinic for Rheumatology
  • Ratko Stamatović Military Medical Academy, Institute of Radiology
  • Željko Mijušković Military Medical Academy, Clinic for Dermatovenerology
  • Jasna Pešić Military Medical Academy, Institute of Radiology
  • Zorana Kremić Military Medical Academy, Clinic for Dermatovenerology
  • Radiša Vojinović University of Kragujevac, Faculty of Medical Sciences, Department of Radiology, Kragujevac
  • Milan Petronijević Military Medical Academy, Clinic for Rheumatology
Keywords: arthritis, psoriatic;, psoriasis;, surveys and questionnaires;, tendons;, ultrasonography;, quality of life

Abstract


Background/Aim. Often asymptomatic, enthesitis can be an integral feature of the wide clinical spectrum in psoriasis as well as an early sign of development of psoriatic arthritis (PsA). It may be difficult to clinically recognize enthesitis in patients with psoriasis or distinguish it from other causes of extraarticular pain. Ultrasound (US) expanding use with the development of accurate assessments through standardized US algorithms as the Glasgow Ultrasound Enthesis Scoring System (GUESS) and the Madrid Sonographic Enthesitis Index Scoring System (MASEI) scores made the US the dominant imaging technique in diagnosing enthesitis. The aims of this study were to establish the prevalence of US signs of enthesitis, compare it with screening questionnaires results, and estimate possible connections of US verified enthesitis with quality of life (QOL) of patients with psoriasis without PsA diagnosis. Methods. A cross-sectional study was performed on 67 patients with psoriasis who were without systemic therapy. The clinical presence of enthesitis was examined by an experienced rheumatologist, and systemic inflammation was estimated through serum level of C-reactive protein (CRP). The Psoriasis Area Severity Index (PASI) and Body Surface Area-Psoriasis (BSA-PsO) were calculated by a dermatologist. Visual analogue scale (VAS) for pain, screening questionnaires – the Toronto Psoriatic Arthritis Screening (ToPAS), Psoriasis Epidemiology Screening Tool (PEST), Psoriatic Arthritis Screening and Evaluation (PASE), Early Psoriatic Arthritis Screening Questionnaire (EARP), and Psoriasis and Arthrosis Screening Questionnaire (PASQ) – were filled by patients. GUESS and MASEI scores were determined by US. The QOL was estimated by the Dermatology Life Quality Index (DLQI). Results. The presence of clinical enthesitis was recorded in 8.7% of patients. According to US signs of enthesitis using GUESS and MASEI scores, only 7% and 2% of patients, respectively, had no sign of enthesitis. Duration of psoriasis and age of subjects were in a significant correlation with GUESS and MASEI scores, while systemic inflammation, VAS value, PASI, and BSA-PsO scores were not. GUESS and MASEI scores  significantly correlated with scores of all screening questionnaires as well as with DLQI. Conclusion. US can detect subclinical enthesitis better than clinical examination and widely used screening questionnaires, even though the correlations between MASEI and/or GUESS scores and results of screening questionnaires were positive. US examination is important in the multidisciplinary approach in diagnosing and managing psoriasis.

References

Menter A. Psoriasis and psoriatic arthritis overview. Am J Manag Care 2016; 22(8 Suppl): s216−24.

Alinaghi F, Calov M, Kristensen LE, Gladman DD, Coates LC, Jullien D, et al. Prevalence of psoriatic arthritis in patients with psoriasis: A systematic review and meta-analysis of ob-servational and clinical studies. J Am Acad Dermatol 2019; 80(1): 251−65.e19.

Helliwell PS, Taylor WJ. Classification and diagnostic criteria for psoriatic arthritis. Ann Rheum Dis 2005; 64 (Suppl 2): ii3−ii8.

Coates LC, Murphy R, Helliwell PS. New GRAPPA recommen-dations for the management of psoriasis and psoriatic arthritis: process, challenges and implementation. Br J Dermatol 2016; 174(6): 1174−8.

Bagel J, Schwartzman S. Enthesitis and Dactylitis in Psoriatic Disease: A Guide for Dermatologists. Am J Clin Dermatol 2018; 19(6): 839−52.

Sakkas LI, Alexiou I, Simopoulou T, Vlychou M. Enthesitis in psoriatic arthritis. Semin Arthritis Rheum 2013; 43(3): 325−34.

Iragorri N, Hazlewood G, Manns B, Danthurebandara V, Spack-man E. Psoriatic arthritis screening: a systematic review and meta-analysis. Rheumatology (Oxford) 2019; 58(4): 692−707.

Calabresi E, Monti S, Governato G, Carli L. One year in review 2018: psoriatic arthritis. Clin Exp Rheumatol 2019; 37(2): 167−78.

Coates LC, Hodgson R, Conaghan PG, Freeston JE. MRI and ul-trasonography for diagnosis and monitoring of psoriatic arthri-tis. Best Pract Res Clin Rheumatol 2012; 26(6): 805−22.

Balint PV, Kane D, Wilson H, McInnes IB, Sturrock RD. Ultra-sonography of entheseal insertions in the lower limb in spon-dyloarthropathy. Ann Rheum Dis 2002; 61(10): 905−10.

de Miguel E, Cobo T, Muñoz-Fernández S, Naredo E, Usón J, Ace-bes JC, et al. Validity of enthesis ultrasound assessment in spondyloarthropathy. Ann Rheum Dis 2009; 68(2): 169−74.

Elalouf O, Bakirci Ureyen S, Touma Z, Anderson M, Kaeley GS, Aydin SZ, et al. Psoriatic Arthritis Sonographic Enthesitis In-struments: A Systematic Review of the Literature. J Rheu-matol 2019; 46(1): 43−56.

Finlay AY, Khan GK. Dermatology Life Quality Index (DLQI)--a simple practical measure for routine clinical use. Clin Exp Dermatol 1994; 19(3): 210−6.

Finlay AY, Basra MKA, Piguet V, Salek MS. Dermatology life quality index (DLQI): a paradigm shift to patient-centered outcomes. J Invest Dermatol 2012; 132(10): 2464−5.

Gisondi P, Tinazzi I, El-Dalati G, Gallo M, Biasi D, Barbara LM, et al. Lower limb enthesopathy in patients with psoriasis without clinical signs of arthropathy: a hospital-based case-control study. Ann Rheum Dis 2008; 67(1): 26−30.

Polachek A, Li S, Chandran V, Gladman DD. Clinical enthesitis in a prospective longitudinal psoriatic arthritis cohort: inci-dence, prevalence, characteristics, and outcome. Arthritis Care Res (Hoboken) 2017; 69(11): 1685–91.

Ranza R, Carneiro S, Qureshi AA, Martins G, Joaquim JR, Romiti R, et al. Prevalence of psoriatic arthritis in a large cohort of Brazilian patients with psoriasis. J Rheumatol 2015; 42(5): 829–34.

Shbeeb M, Uramoto KM, Gibson LE, O’Fallon WM, Gabriel SE. The epidemiology of psoriatic arthritis in Olmsted County, Minnesota, USA, 1982–1991. J Rheumatol 2000; 27(5): 1247–50.

Lehtinen A, Leirisalo-Repo M, Taavitsainen M. Persistence of en-thesopathic changes in patients with spondylarthropathy dur-ing a 6-month followup. Clin Exp Rheumatol 1995, 13: 733−6.

Love TJ, Gudbjpornsson B, Gudjonsson JE, Valdimarsson H. Pso-riatic arthritis in Reykjavik, Iceland: prevalence, demographics and disease course. J Rheumatol 2007; 34(10): 2082–8.

Macıa-Villa C, De Miguel E. Updating the use of the Madrid Sonographic Enthesis Index (MASEI): a systematic review of the literature. Rheumatology (Oxford) 2020; 59(5): 1031−40.

Pistone G, La Vecchia M, Pistone A, Bongiorno MR. Achilles ten-don ultrasonography may detect early features of psoriatic ar-thropathy in patients with cutaneous psoriasis. Br J Dermatol 2014; 171(5): 1220−2.

Macchioni P, Salvarani C, Possemato N, Gutierrez M, Grassi W, Gasparini S, et al. Ultrasonographic and Clinical Assessment of Peripheral Enthesitis in Patients with Psoriatic Arthritis, Pso-riasis, and Fibromyalgia Syndrome: The ULISSE study. J Rheumatol 2019; 46(8): 904−11.

Perrotta FM, Astorri D, Zappia M, Reginelli A, Brunese L, Lu-brano E. An ultrasonographic study of enthesis in early psoriat-ic arthritis patients naive to traditional and biologic DMARDs treatment. Rheumatol Int 2016; 36(11): 1579−83.

Eder L, Jayakar J, Thavaneswaran A, Haddad A, Chandran V, Sa-lonen D, et al. Is the Madrid Sonographic Enthesitis Index Useful for Differentiating Psoriatic Arthritis from Psoriasis Alone and Healthy Controls? J Rheumatol 2014; 41(3); 466−72.

Hamdy M, Omar G, Elshereef RR, Ellaban AS, Amin M. Early detection of spondyloarthropathy in patients with psoriasis by using the ultrasonography and magnetic resonance image. Eur J Rheumatol 2015; 2(1): 10−5.

Van der Ven M, Karreman MC, Weel AE. Adding ultrasound to clinical examination reduced frequency of enthesitis in pri-mary care psoriasis patients with musculoskeletal complaints. Clin Exp Rheumatol 2016; 34(6): 1020−5.

Tinazzi I, McGonagle D, Biasi D, Confente S, Caimmi C, Girolo-moni G, et al. Preliminary evidence that subclinical enthesopa-thy may predict psoriatic arthritis in patients with psoriasis. J Rheumatol. 2011; 38(12): 2691−2.

El Miedany Y, El Gaafary M, Youssef S, Ahmed I, Nasr A. Tai-lored approach to early psoriatic arthritis patients: clinical and ultrasonographic predictors for structural joint damage. Clin Rheumatol 2015; 34(2): 307−13.

Falcao S, Castillo-Gallego C, Peiteado D. Can we use enthesis ul-trasound as an outcome measure of disease activity in spondy-loarthritis? A study at the Achilles level. Rheumatology (Ox-ford) 2015; 54(9): 1557−62.

Gisondi P, Tinazzi I, El-Dalati G, Gallo M, Biasi D, Barbara LM, et al. Lower limb enthesopathy in patients with psoriasis without clinical signs of arthropathy: a hospital-based case-control study. Ann Rheum Dis 2008; 67(1): 26−30.

Girolomoni G, Gisondi P. Psoriasis and systemic inflammation: underdiagnosed enthesopathy. J Eur Acad Dermatol Venereol 2009; 23(Suppl. 1): 3–8.

Rezvani A, Bodur H, Ataman S, Kaya T, Bugdaycı DS, Demir SE. Correlations among enthesitis, clinical, radiographic and quali-ty of life parameters in patients with ankylosing spondylitis. Mod Rheumatol 2014; 24(4): 651–6.

Salaffi F, Di Carlo M, Luchetti MM, Di Donato E, Campanati A, Benfaremo D, et al. A validation study of the Simple Psoriatic Arthritis Screening (SiPAS) questionnaire to screen psoriasis patients for psoriatic arthritis. Clin Exp Rheumatol 2018; 36(1): 127−35.

Langenbruch A, Radtke MA, Gutknecht M, Augustin M. Does the Dermatology Life Quality Index (DLQI) underestimate the disease-specific burden of psoriasis patients. Eur Acad Derma-tol Venereol 2019; 33(1): 123−7.

Kaufman BP, Alexis AF. Psoriasis in skin of color: insights into the epidemiology, clinical presentation, genetics, quality-of-life impact, and treatment of psoriasis in non-white ra-cial/ethnic groups. Am J Clin Dermatol 2018; 19(3): 405−23.

Published
2022/01/25
Section
Original Paper