COVID-19 prognosis in systemic lupus erythematosus compared with rheumatoid arthritis and spondyloarthritis: results from the CONTROL-19 Study by the Italian Society for Rheumatology
Chiara Scirocco, Sara Ferrigno, Laura Andreoli, Micaela Fredi, Claudia Lomater, Luca Moroni, Marta Mosca, Bernd Raffeiner, Greta Carrara, Gianpiero Landolfi, Davide Rozza, Anna Zanetti, Carlo Alberto Scirè, Gian Domenico Sebastiani
Lupus Science & Medicine, doi:10.1136/lupus-2023-000945
Introduction Data concerning SARS-CoV-2 in patients affected by SLE are contradicting. The aim of this study was to investigate disease-related differences in COVID-19 prognosis of patients affected by rheumatic diseases before vaccination; we tested the hypothesis that patients with SLE may have a different outcome compared with those with rheumatoid arthritis (RA) or spondyloarthritis (SPA). Methods We analysed data from the national CONTROL-19 Database with a retrospective, observational design, including rheumatic patients affected by COVID-19. The principal outcome measure was hospitalisation with death or mechanical ventilation. Differences between SLE, RA and SPA were analysed by univariable and multivariable logistic regression models. Results We included 103 patients with SLE (88.2% female, mean age 48.9 years, 50.4% active disease), 524 patients with RA (74.4% female, mean age 60.6 years, 59.7% active disease) and 486 patients with SPA (58.1% female, mean age 53.2 years, 58% active disease). Outcome prevalence was not different between patients with SLE and those with RA (SLE 24.5%, RA 25.6%), while patients with SPA showed a more favourable outcome compared with those with SLE (SPA 15.9%); data from the multivariable analysis confirmed this result. In SLE, age >65 years (OR 17.3, CI 5.51 to 63.16, p<0.001), hypertension (OR 6.2, CI 2.37 to 17.04, p<0.001) and prednisone (PDN) use (OR 3.8, CI 1.43 to 11.39, p=0.01) were associated with severe outcomes, whereas hydroxychloroquine use was found to be protective (OR 0.3, CI 0.14 to 0.91, p=0.03). Conclusion Our data suggest that patients with SLE and RA do not show a different COVID-19 outcome, while patients with SPA have a more favourable disease course compared with those with SLE. Risk of hospitalisation with ventilation or death was associated with age >65 years, hypertension and PDN use in patients with SLE. WHAT IS ALREADY KNOWN ON THIS TOPIC ⇒ COVID-19 expression in rheumatic diseases has been largely studied in the last 3 years. Some studies reported an increased risk of severe COVID-19 in these patients, while others did not confirm these data. Concerning patients with SLE, data on COVID-19 incidence and prognosis come mainly from case series, reports, observational and retrospective studies, and evidence is controversial. Moreover, little has been investigated about the comparison between SLE and other rheumatic diseases concerning COVID-19 outcome. WHAT THIS STUDY ADDS ⇒ We analysed the national surveillance study's data promoted by the Italian Society for Rheumatology (CONTROL-19 Database) including patients with rheumatic diseases and COVID-19. The principal outcome measure was hospitalisation with death or mechanical ventilation. We included 103 patients with SLE, 524 patients with rheumatoid arthritis (RA) and 486 patients with spondyloarthritis (SPA). According to our results, outcome prevalence was not different between patients with SLE and those with RA,..
Contributors CS, SF, DR, GL, AZ, MM, CAS and GDS were responsible for data analysis and interpretation and gave substantial contribution to the conception of the work. CS, SF, LA, MF, CL, LM, MM, BR, GC, GL, DR, AZ, CAS and GDS wrote the original draft and revised it. CS, SF, MM, CAS and GDS realised and validated the final revision and agreed about all the aspects of the work ensuring that questions related to the accuracy or integrity of it were appropriately investigated. GDS is responsible for the overall content as the guarantor. All authors reviewed and approved the manuscript's content before submission. Competing interests None declared. Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research. Patient consent for publication Not required. Ethics approval This study involves human participants and was approved by the Ethics Committee of Area Vasta Emilia Centrale on 24 March 2020 (288/2020/Oss/ AOUFe). Encrypted retrospective information was used. Provenance and peer review Not commissioned; externally peer reviewed.
References
Alarcón, Izadi, Characteristics associated with poor COVID-19 outcomes in individuals with systemic lupus erythematosus: data from the COVID-19 global rheumatology alliance, Ann Rheum Dis,
doi:10.1136/annrheumdis-2021-221636Bozzalla Cassione, Zanframundo, Biglia, COVID-19 infection in a northern-Italian cohort of systemic lupus erythematosus assessed by Telemedicine, Ann Rheum Dis,
doi:10.1136/annrheumdis-2020-217717Bruera, Lei, Zhao, Risks of mortality and severe Coronavirus disease 19 (COVID-19) outcomes in patients with or without systemic lupus erythematosus, Lupus Sci Med,
doi:10.1136/lupus-2022-000750Carbillon, Benbara, Boujenah, Clinical course of COVID-19 in patients with systemic lupus erythematosus under long-term treatment with hydroxychloroquine, Ann Rheum Dis,
doi:10.1136/annrheumdis-2020-217847Cho, Kandane-Rathnayake, Louthrenoo, COVID-19 infection in patients with systemic lupus erythematosus: data from the Asia Pacific lupus collaboration, Int J Rheum Dis,
doi:10.1111/1756-185X.13937Cordtz, Kristensen, Dalgaard, Incidence of COVID-19 Hospitalisation in patients with systemic lupus erythematosus: a nationwide cohort study from Denmark, J Clin Med,
doi:10.3390/jcm10173842Favalli, Bugatti, Klersy, Impact of corticosteroids and immunosuppressive therapies on symptomatic SARS-CoV-2 infection in a large cohort of patients with chronic inflammatory arthritis, Arthritis Res Ther,
doi:10.1186/s13075-020-02395-6Fernandez-Ruiz, Paredes, Niewold, COVID-19 in patients with systemic lupus erythematosus: lessons learned from the inflammatory disease, Transl Res,
doi:10.1016/j.trsl.2020.12.007Fredi, Cavazzana, Moschetti, COVID-19 in patients with rheumatic diseases in northern Italy: a single-centre observational and case-control study, Lancet Rheumatol,
doi:10.1016/S2665-9913(20)30169-7Gendebien, Frenckell, Ribbens, Systematic analysis of COVID-19 infection and symptoms in a systemic lupus erythematosus population: correlation with disease characteristics, hydroxychloroquine use and immunosuppressive treatments, Ann Rheum Dis,
doi:10.1136/annrheumdis-2020-218244Gianfrancesco, Hyrich, Gossec, Rheumatic disease and COVID-19: initial data from the COVID-19 global rheumatology alliance provider registries, Lancet Rheumatol,
doi:10.1016/S2665-9913(20)30095-3Gianfrancesco, Leykina, Izadi, Association of race and Ethnicity with COVID-19 outcomes in rheumatic disease: data from the COVID-19 global rheumatology alliance physician registry, Arthritis Rheumatol,
doi:10.1002/art.41567Jiang, Sparks, Wallace, Risk of COVID-19 among Unvaccinated and vaccinated patients with systemic lupus erythematosus: a general population study, RMD Open,
doi:10.1136/rmdopen-2022-002839Konig, Kim, Scheetz, Baseline use of hydroxychloroquine in sistemic lupus erythematosus does not preclude SARS-Cov-2 infection and severe COVID-19, Ann Rheum Dis,
doi:10.1136/annrheumdis-2020-217690Landewé, Machado, Kroon, EULAR provisional recommendations for the management of rheumatic and musculoskeletal diseases in the context of SARS-CoV-2, Ann Rheum Dis,
doi:10.1136/annrheumdis-2020-217877Manivannan, Karthikeyan, Moorthy, The rise and fall of chloroquine/hydroxychloroquine as compassionate therapy of COVID-19, Front Pharmacol,
doi:10.3389/fphar.2021.584940Marques, Kakehasi, Pinheiro, High levels of immunosuppression are related to unfavorable outcomes in hospitalized patients with rheumatic diseases and COVID-19: first results of Reumacovbrasil Registry, RMD Open,
doi:10.1136/rmdopen-2020-001461Mathian, Mahevas, Rohmer, Clinical course of Coronavirus disease 2019 (COVID-19) in a series of 17 patients with systemic lupus erythematosus under long-term treatment with hydroxychloroquine, Ann Rheum Dis,
doi:10.1136/annrheumdis-2020-217566Misra, Agarwal, Gasparyan, Rheumatologists' perspective on Coronavirus disease 19 (COVID-19) and potential therapeutic targets, Clin Rheumatol,
doi:10.1007/s10067-020-05073-9Montero, Martínez-Barrio, Serrano-Benavente, Coronavirus disease 2019 (COVID-19) in autoimmune and inflammatory conditions: clinical characteristics of poor outcomes, Rheumatol Int,
doi:10.1007/s00296-020-04676-4Ramirez, Argolini, Bellocchi, Impact of the COVID-19 pandemic in patients with systemic lupus erythematosus throughout one year, Clin Immunol,
doi:10.1016/j.clim.2021.108845Sakthiswary, Chuah, Chiang, COVID-19 in systemic lupus erythematosus: a pooled analysis and systematic review of case reports and series, Lupus,
doi:10.1177/09612033211045057Scirè, Carrara, Zanetti, COVID-19 in rheumatic diseases in Italy: first results from the Italian Registry of the Italian society for rheumatology (CONTROL-19), Lupus Science & Medicine
Silva, Serling-Boyd, Wallwork, Clinical characteristics and outcomes of patients with Coronavirus disease 2019 (COVID-19) and rheumatic disease: a comparative cohort study from a US 'hot spot, Ann Rheum Dis,
doi:10.1136/annrheumdis-2020-217888Team, Grr, The COVID-19 global rheumatology alliance | the global rheumatology community's response to the worldwide COVID-19 pandemic
Van Doremalen, Bushmaker, Morris, Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1, N Engl J Med,
doi:10.1056/NEJMc2004973Wu, Chen, Cai, Risk factors associated with acute respiratory distress syndrome and death in patients with Coronavirus disease 2019 pneumonia in Wuhan, China, JAMA Intern Med,
doi:10.1001/jamainternmed.2020.0994Yao, Ye, Zhang, In vitro antiviral activity and projection of Optimized dosing design of hydroxychloroquine for the treatment of severe acute respiratory syndrome Coronavirus 2, Clin Infect Dis,
doi:10.1093/cid/ciaa237Zanetti, Carrara, Landolfi, Increased COVID-19 mortality in patients with rheumatic diseases: results from the CONTROL-19 study by the Italian society for rheumatology, Clin and Exp Rheumatol,
doi:10.55563/clinexprheumatol/fmyozhZhang, Li, Zhang, Identifying airborne transmission as the dominant route for the spread of COVID-19, Proc Natl Acad Sci U S A,
doi:10.1073/pnas.2009637117Zhong, Shen, Yang, COVID-19 in patients with rheumatic disease in Hubei province, China: a multicentre retrospective observational study, Lancet Rheumatol,
doi:10.1016/S2665-9913(20)30227-7Zhou, Yu, Du, Clinical course and risk factors for mortality of adult Inpatients with COVID-19 in Wuhan, China: a retrospective cohort study, Lancet,
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'abstract': '<jats:sec><jats:title>Introduction</jats:title><jats:p>Data concerning SARS-CoV-2 in patients '
'affected by SLE are contradicting.</jats:p><jats:p>The aim of this study was to investigate '
'disease-related differences in COVID-19 prognosis of patients affected by rheumatic diseases '
'before vaccination; we tested the hypothesis that patients with SLE may have a different '
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'models.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>We included 103 '
'patients with SLE (88.2% female, mean age 48.9 years, 50.4% active disease), 524 patients '
'with RA (74.4% female, mean age 60.6 years, 59.7% active disease) and 486 patients with SPA '
'(58.1% female, mean age 53.2 years, 58% active disease).</jats:p><jats:p>Outcome prevalence '
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'doi-asserted-by': 'crossref',
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'of COVID-19 infection and symptoms in a systemic lupus erythematosus '
'population: correlation with disease characteristics, hydroxychloroquine '
'use and immunosuppressive treatments. Ann Rheum Dis 2021;80:e94. '
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'doi-asserted-by': 'crossref',
'unstructured': 'Goyal M , Patil P , Pathak H , et al . Impact of COVID-19 pandemic on '
'patients with SLE: results of a large multicentric survey from India. '
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'volume': '2',
'author': 'Gianfrancesco',
'year': '2020',
'journal-title': 'Lancet Rheumatol'},
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'volume': '40',
'author': 'Zanetti',
'year': '2022',
'journal-title': 'Clin and Exp Rheumatol'},
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'author': 'Scirè',
'year': '2020',
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'Coronavirus disease 19 (COVID-19) outcomes in patients with or without '
'systemic lupus erythematosus. Lupus Sci Med 2023;10:e000750. '
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'Hospitalisation in patients with systemic lupus erythematosus: a '
'nationwide cohort study from Denmark. J Clin Med 2021;10:3842. '
'doi:10.3390/jcm10173842',
'DOI': '10.3390/jcm10173842'},
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'doi-asserted-by': 'publisher',
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'doi-asserted-by': 'crossref',
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