Evaluation of clinical efficacy of tumor necrosis factor‑α inhibitors in treatment of distal extremity swelling with pitting edema in psoriatic arthritis of inadequate response to conventional therapy: A 10‑year retrospective study

Zhao,Chenyang; Liu,Bingqian; Yao,Yuan; Yang,Kevin; Zang,Bo; Liu,Bin

doi:10.3892/etm.2023.11962

Evaluation of clinical efficacy of tumor necrosis factor‑α inhibitors in treatment of distal extremity swelling with pitting edema in psoriatic arthritis of inadequate response to conventional therapy: A 10‑year retrospective study

Authors:
- Chenyang Zhao
- Bingqian Liu
- Yuan Yao
- Kevin Yang
- Bo Zang
- Bin Liu
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Affiliations: Department of Rheumatology, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266003, P.R. China
Published online on: April 19, 2023 https://doi.org/10.3892/etm.2023.11962
Article Number: 263
Copyright: © Zhao et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Distal extremity swelling with pitting edema in psoriatic arthritis (PsA) is a rare rheumatological condition, whose management presents a challenge. The aim of the present study was to identify the clinical characteristics of, and formulate a standardized management strategy for, patients with distal extremity swelling with pitting edema in PsA. The medical records of consecutive patients with PsA, with or without distal extremity swelling with pitting edema, were systematically analyzed over a ~10‑year period (between September 2008 and September 2018) in a single center and a comprehensive review (pathogenic mechanisms, clinical manifestations, and treatments) was undertaken. A total of 167 patients with PsA were evaluated, and distal extremity swelling with pitting edema was recorded in 16 of these patients. In three of the 16 patients, distal extremity swelling with pitting edema occurred as the first, isolated manifestation of PsA. The upper and lower extremities were affected, predominantly asymmetrically. Female patients with PsA were more likely to be affected with pitting edema and the blood test results revealed that the patients with PsA and pitting edema also presented with a significantly higher erythrocyte sedimentation rate and concentration of C‑reactive protein. The onset of pitting edema was associated with the activity of the disease. Lymphoscintigraphy and magnetic resonance imaging (MRI) scans revealed that edema might have resulted from inflammation of the tenosynovial structures. Furthermore, treatment with tumor necrosis factor‑α inhibitor (TNFi) elicited improvements in patients with pitting edema that were not responsive to conventional synthetic disease‑modifying antirheumatic drug therapy. In conclusion, distal extremity swelling with pitting edema, also termed atypical remitting seronegative symmetrical synovitis with pitting edema (RS3PE) syndrome, may represent the initial isolated manifestation of PsA. The atypical RS3PE syndrome in PsA was attributable to inflammation of the tenosynovial structures, and TNFi may serve as a potential treatment.

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1	Kalliomaki JL and Vastamaki M: Chronic diffuse oedema of the rheumatoid hand: A sign of local lymphatic involvement. Ann Rheum Dis. 27:167–169. 1968.PubMed/NCBI View Article : Google Scholar
2	Salvarani C, Macchioni PL, Veneziani M, Rossi F, Lodi L, Baricchi R, Boiardi L and Portioli I: Upper limb lymphedema in psoriatic arthritis. J Rheumatol. 17:273–274. 1990.PubMed/NCBI
3	Mulherin DM, FitzGerald O and Bresnihan B: Lymphedema of the upper limb in patients with psoriatic arthritis. Semin Arthritis Rheum. 22:350–356. 1993.PubMed/NCBI View Article : Google Scholar
4	Kiely PD, Bland JM, Joseph AE, Mortimer PS and Bourke BE: Upper limb lymphatic function in inflammatory arthritis. J Rheumatol. 22:214–217. 1995.PubMed/NCBI
5	Salvarani C, Cantini F, Olivieri I, Niccoli L, Senesi C, Macchioni L, Boiardi L and Padula A: Distal extremity swelling with pitting edema in psoriatic arthritis: Evidence of 2 pathological mechanisms. J Rheumatol. 26:1831–1834. 1999.PubMed/NCBI
6	Bohm M, Riemann B, Luger TA and Bonsmann G: Bilateral upper limb lymphoedema associated with psoriatic arthritis: A case report and review of the literature. Br J Dermatol. 143:1297–1301. 2000.PubMed/NCBI View Article : Google Scholar
7	Diez-Porres L, Munoz-Fernandez S, Aguado P, Alonso M and Martin-Mola E: Remitting seronegative symmetrical synovitis with pitting oedema as the first manifestation of psoriatic arthropathy. Rheumatology (Oxford). 41:1333–1335. 2002.PubMed/NCBI
8	Yamamoto T and Nishioka K: Psoriasis arthropathy and lymphedema. J Dermatol. 29:812–814. 2002.PubMed/NCBI View Article : Google Scholar
9	Quarta L, Corrado A, d'Onofrio F, Maruotti N and Cantatore FP: Two cases of distal extremity swelling with pitting oedema in psoriatic arthritis: The different pathological mechanisms. Rheumatol Int. 30:1367–1370. 2010.PubMed/NCBI View Article : Google Scholar
10	Almodovar R, Zarco P, Quiros FJ and Mazzucchelli R: Infliximab treatment efficacy in lymphoedema associated with ankylosing spondylitis. Rheumatology (Oxford). 43(1456)2004.PubMed/NCBI View Article : Google Scholar
11	Lubrano E, Perrotta FM, Scriffignano S, Coates LC and Helliwell P: Sustained very low disease activity and remission in psoriatic arthritis patients. Rheumatol Ther. 6:521–528. 2019.PubMed/NCBI View Article : Google Scholar
12	Lekpa FK, Economu-Dubosc A, Fevre C, Claudepierre P and Chevalier X: Efficacy of etanercept in lymphedema associated with psoriatic arthritis. J Rheumatol. 36:207–208. 2009.PubMed/NCBI View Article : Google Scholar
13	Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H and Group CS: Classification criteria for psoriatic arthritis: Development of new criteria from a large international study. Arthritis Rheum. 54:2665–2673. 2006.PubMed/NCBI View Article : Google Scholar
14	Helliwell PS, FitzGerald O, Fransen J, Gladman DD, Kreuger GG, Callis-Duffin K, McHugh N, Mease PJ, Strand V, Waxman R, et al: The development of candidate composite disease activity and responder indices for psoriatic arthritis (GRACE project). Ann Rheum Dis. 72:986–991. 2013.PubMed/NCBI View Article : Google Scholar
15	Gan Y, Sun Y, Jin J, Wang Y, Chen J, Chung Y, Li X and Ye H: bFGF could be a biomarker of malignancy in RS₃PE syndrome: An ambispective single-center cohort analysis of 51 patients. Arthritis Res Ther. 23(261)2021.PubMed/NCBI View Article : Google Scholar
16	Kerschbaumer A, Fenzl KH, Erlacher L and Aletaha D: An overview of psoriatic arthritis-epidemiology, clinical features, pathophysiology and novel treatment targets. Wien Klin Wochenschr. 128:791–795. 2016.PubMed/NCBI View Article : Google Scholar
17	Gladman DD and Brockbank J: Psoriatic arthritis. Expert Opin Investig Drugs. 9:1511–1522. 2000.PubMed/NCBI View Article : Google Scholar
18	Gottlieb AB, Bakewell C and Merola JF: Musculoskeletal imaging for dermatologists: Techniques in the diagnosis and management of psoriatic arthritis. Dermatol Ther (Heidelb). 11:1199–1216. 2021.PubMed/NCBI View Article : Google Scholar
19	Szczerkowska-Dobosz A, Krasowska D, Bartosinska J, StawczykMacieja M, Walczak A, Owczarczyk-Saczonek A, Reich A, Batycka-Baran A, Czajkowski R, Dobrucki IT, et al: Pathogenesis of psoriasis in the ‘omic’ era. Part IV. Epidemiology, genetics, immunopathogenesis, clinical manifestation and treatment of psoriatic arthritis. Postepy Dermatol Alergol. 37:625–634. 2020.PubMed/NCBI View Article : Google Scholar
20	Kenzaka T: The relationship between remitting seronegative symmetrical synovitis with pitting edema and vascular endothelial growth factor and matrix metalloproteinase 3. Intern Med. 59:1021–1022. 2020.PubMed/NCBI View Article : Google Scholar
21	Fearon U, Griosios K, Fraser A, Reece R, Emery P, Jones PF and Veale DJ: Angiopoietins, growth factors, and vascular morphology in early arthritis. J Rheumatol. 30:260–268. 2003.PubMed/NCBI
22	Veale DJ and Fearon U: The pathogenesis of psoriatic arthritis. Lancet. 391:2273–2284. 2018.PubMed/NCBI View Article : Google Scholar
23	Bucaloiu ID, Olenginski TP and Harrington TM: Remitting seronegative symmetrical synovitis with pitting edema syndrome in a rural tertiary care practice: A retrospective analysis. Mayo Clin Proc. 82:1510–1515. 2007.PubMed/NCBI View Article : Google Scholar
24	Kimura M, Tokuda Y, Oshiawa H, Yoshida K, Utsunomiya M, Kobayashi T, Deshpande GA, Matsui K and Kishimoto M: Clinical characteristics of patients with remitting seronegative symmetrical synovitis with pitting edema compared to patients with pure polymyalgia rheumatica. J Rheumatol. 39:148–153. 2012.PubMed/NCBI View Article : Google Scholar
25	Gisserot O, Cremades S, Landais C, Leyral G, Bernard P and de Jaureguiberry JP: RS3PE revealing recurrent non-Hodgkin's lymphoma. Joint Bone Spine. 71:424–426. 2004.PubMed/NCBI View Article : Google Scholar
26	Chiappetta N and Gruber B: Remitting seronegative symmetrical synovitis with pitting edema associated with acute myeloid leukemia. J Rheumatol. 32:1613–1614. 2005.PubMed/NCBI
27	Tunc SE, Arslan C, Ayvacioglu NB, Sahin M, Akkus S and Yorgancigil H: Paraneoplastic remitting seronegative symmetrical synovitis with pitting edema (RS3PE syndrome): A report of two cases and review of the literature. Rheumatol Int. 24:234–237. 2004.PubMed/NCBI View Article : Google Scholar
28	Schaeverbeke T, Fatout E, Marce S, Vernhes JP, Halle O, Antoine JF, Lequen L, Bannwarth B and Dehais J: Remitting seronegative symmetrical synovitis with pitting oedema: Disease or syndrome? Ann Rheum Dis. 54:681–684. 1995.PubMed/NCBI View Article : Google Scholar
29	Olivieri I, Padula A, Favaro L, Pierro A, Oranges GS and Ferri S: Dactylitis with pitting oedema of the hand in longstanding ankylosing spondylitis. Clin Rheumatol. 14:701–704. 1995.PubMed/NCBI View Article : Google Scholar
30	Cantini F, Niccoli L, Olivieri I, Barozzi L, Pavlica P, Bozza A, Macchioni PL, Padula AA and Salvarani C: Remitting distal lower extremity swelling with pitting oedema in acute sarcoidosis. Ann Rheum Dis. 56:565–566. 1997.PubMed/NCBI View Article : Google Scholar
31	Okumura T, Tanno S, Ohhira M and Nozu T: The rate of polymyalgia rheumatica (PMR) and remitting seronegative symmetrical synovitis with pitting edema (RS3PE) syndrome in a clinic where primary care physicians are working in Japan. Rheumatol Int. 32:1695–1699. 2012.PubMed/NCBI View Article : Google Scholar
32	Joseph AD, Kumanan T, Aravinthan N and Suganthan N: An unusual case of remitting seronegative symmetrical synovitis with pitting edema: Case report and literature review. SAGE Open Med Case Rep. 8(2050313X20910920)2020.PubMed/NCBI View Article : Google Scholar
33	Cantini F, Salvarani C, Olivieri I, Macchioni L, Niccoli L, Padula A, Falcone C, Boiardi L, Bozza A, Barozzi L and Pavlica P: Distal extremity swelling with pitting edema in psoriatic arthritis: A case-control study. Clin Exp Rheumatol. 19:291–296. 2001.PubMed/NCBI
34	Ku DD, Zaleski JK, Liu S and Brock TA: Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am J Physiol. 265:H586–H592. 1993.PubMed/NCBI View Article : Google Scholar
35	Arima K, Origuchi T, Tamai M, Iwanaga N, Izumi Y, Huang M, Tanaka F, Kamachi M, Aratake K, Nakamura H, et al: RS3PE syndrome presenting as vascular endothelial growth factor associated disorder. Ann Rheum Dis. 64:1653–1655. 2005.PubMed/NCBI View Article : Google Scholar
36	Baumgartner I, Rauh G, Pieczek A, Wuensch D, Magner M, Kearney M, Schainfeld R and Isner JM: Lower-extremity edema associated with gene transfer of naked DNA encoding vascular endothelial growth factor. Ann Intern Med. 132:880–884. 2000.PubMed/NCBI View Article : Google Scholar
37	Eder L, Aydin SZ, Kaeley GS, Maksymowych WP and Ostergaard M: Options for Assessing Joints and Entheses in Psoriatic Arthritis by Ultrasonography and Magnetic Resonance Imaging: How to Move Forward. J Rheumatol Suppl. 94:44–47. 2018.PubMed/NCBI View Article : Google Scholar
38	Crespo-Rodriguez AM, Sanz Sanz J, Freites D, Rosales Z, Abasolo L and Arrazola J: Role of diagnostic imaging in psoriatic arthritis: How, when, and why. Insights Imaging. 12(121)2021.PubMed/NCBI View Article : Google Scholar
39	Szuba A, Shin WS, Strauss HW and Rockson S: The third circulation: Radionuclide lymphoscintigraphy in the evaluation of lymphedema. J Nucl Med. 44:43–57. 2003.PubMed/NCBI
40	Kleinert S, Feuchtenberger M, Kneitz C and Tony HP: Psoriatic arthritis: Clinical spectrum and diagnostic procedures. Clin Dermatol. 25:519–523. 2007.PubMed/NCBI View Article : Google Scholar
41	Kohm M, Burkhardt H and Behrens F: Anti-TNFalpha-therapy as an evidence-based treatment option for different clinical manifestations of psoriatic arthritis. Clin Exp Rheumatol. 33 (Suppl 5):S109–S114. 2015.PubMed/NCBI