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Prevalence and Clinical Outcomes of COVID-19 in Patients with Autoimmune Diseases: a Systematic Review and Meta-Analysis

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Prevalence and Clinical Outcomes of COVID-19 in Patients with Autoimmune Diseases: a Systematic Review and Meta-Analysis Autoinflammatory disorders Ann Rheum Dis: first published as 10.1136/annrheumdis-2020-218946 on 13 October 2020. Downloaded from CLINICAL SCIENCE Prevalence and clinical outcomes of COVID-19 in patients with autoimmune diseases: a systematic review and meta- analysis Shintaro Akiyama ,1 Shadi Hamdeh,2 Dejan Micic,1 Atsushi Sakuraba1 Handling editor Josef S ABSTRACT Key messages Smolen Objectives The prevalence and clinical outcomes of COVID-19 in patients with autoimmune diseases who ► Additional material is What is already known about this subject? published online only. To view are frequently treated with disease modifying therapies ► The prevalence and clinical outcomes of please visit the journal online remains poorly understood. This meta-analysis aims to COVID-19 in patients with autoimmune (http:// dx. doi. org/ 10. 1136/ assess the prevalence and clinical outcomes of COVID-19 diseases who are frequently treated with annrheumdis- 2020- 218946). in autoimmune diseases. immunosuppressive or anticytokine drugs 1 Inflammatory Bowel Disease Methods Electronic databases were searched for remains poorly understood. Center, The University of observational and case–controlled studies. We sorted Chicago Medicine, Chicago, medications into glucocorticoids, conventional synthetic Illinois, USA What does this study add? 2 disease-modifying antirheumatic drugs (csDMARDs) and Department of Internal ► The prevalence of COVID-19 in autoimmune Medicine, Division of biologic or targeted synthetic DMARDs (b/tsDMARDs), diseases was 0.011 (95% CI: 0.005 to 0.025) Gastroenterology, Hepatology which was also divided into monotherapy and b/ which was significantly higher than in the and Motility, University of tsDMARDs–csDMARDs combination therapy. Kansas, Lawrence, Kansas, USA comparator population. Results We analysed 62 observational studies with a ► Glucocorticoids increased the risk of COVID-19 total of 319 025 patients with autoimmune diseases. The Correspondence to and its severe outcomes. Atsushi Sakuraba, Inflammatory prevalence of COVID-19 was 0.011 (95% CI: 0.005 to ► Conventional synthetic disease- modifying Bowel Disease Center, The 0.025). Meta- analysis of seven case–controlled studies antirheumatic drugs (csDMARDs) and biologic University of Chicago Medicine, demonstrated that the risk of COVID-19 in autoimmune or targeted synthetic DMARDs (b/tsDMARDs)– Chicago, Illinois, USA; diseases was significantly higher than in control asakurab@ medicine. bsd. csDMARDs combination therapy significantly uchicago. edu patients (OR: 2.19, 95% CI: 1.05 to 4.58, p=0.038). increased the risk of severe outcomes, whereas Meta- regression analysis showed glucocorticoids were b/tsDMARDs monotherapy, in particular anti- Received 21 August 2020 significantly associated with the risk of COVID-19. For tumour necrosis factor therapy, reduced the risk Revised 30 September 2020 clinical outcomes, we assessed 65 studies with 2766 of severe COVID-19. Accepted 30 September 2020 patients with autoimmune diseases diagnosed with COVID-19. The rates of hospitalisation and mortality How might this impact on clinical practice or were 0.35 (95% CI: 0.23 to 0.50) and 0.066 (95% CI: future developments? 0.036 to 0.12), respectively. Glucocorticoids, csDMARDs ► Unlike glucocorticoids, csDMARDs and b/ http://ard.bmj.com/ and b/tsDMARDs–csDMARDs combination therapy tsDMARDs–csDMARDs combination therapy, increased the risk of these outcomes, whereas b/ b/tsDMARDs monotherapy can be safely used tsDMARDs monotherapy, particularly antitumour necrosis during COVID-19 pandemic. factor agents, were associated with a lower risk of hospitalisation and death. Conclusions Our meta-analysis demonstrated that To understand the incidence and prognosis on October 1, 2021 by guest. Protected copyright. patients with autoimmune diseases had an increased risk of COVID-19 in ADs, international registries of COVID-19, primarily attributed to glucocorticoid use. of patients with inflammatory bowel disease b/tsDMARDs monotherapy was associated with a lower 2 (SECURE- IBD registry ) or rheumatic diseases risk of severe COVID-19 suggesting its safety in the (C19- GRA3) diagnosed with COVID-19 have been COVID-19 pandemic. developed and analysed their COVID-19 outcomes. These data have demonstrated that similar to the general population, age and underlying comor- bidities are poor prognostic factors of COVID-19 © Author(s) (or their INTRODUCTION in ADs.4 In terms of treatments, both registries employer(s)) 2020. No The outbreak of COVID-19 caused by the novel demonstrated that patients treated with glucocorti- commercial re- use. See rights SARS- CoV-2 has spread worldwide leading to large coids (GCs) had poor clinical outcomes of COVID- and permissions. Published 1 by BMJ. number of infections and deaths. Patients with 19, whereas those treated with antitumour necrosis autoimmune diseases (ADs) are frequently treated factor (TNF) therapies, particularly when used as a To cite: Akiyama S, with immunosuppressive or anticytokine drugs, monotherapy, had a decreased risk of hospitalisa- Hamdeh S, Micic D, et al. 2 3 Ann Rheum Dis Epub ahead which raises concern for infectious complications, tion due to COVID-19. These findings suggest of print: [please include Day placing patients and physicians at a crossroads with that anti- TNF monotherapy may be protective Month Year]. doi:10.1136/ respect to continuation or cessation of these disease against severe COVID-19. However, each study or annrheumdis-2020-218946 modifying therapies. registry has a limited sample size. Therefore, there Akiyama S, et al. Ann Rheum Dis 2020;0:1–8. doi:10.1136/annrheumdis-2020-218946 1 Autoinflammatory disorders Ann Rheum Dis: first published as 10.1136/annrheumdis-2020-218946 on 13 October 2020. Downloaded from is a need to integrate findings across studies to better understand or deceased patients were excluded. The search strategy is the risk of COVID-19 in ADs. described in figure 1. This systematic review and meta-analysis aimed to determine the prevalence of COVID-19 and investigate its clinical outcomes Data extraction and quality assessment in ADs. We also assessed how individual risk factors, including All data were independently abstracted in duplicate by two comorbidities and medical therapies, influence the prevalence authors (SA and AS) by using a data extraction form. Data on the and clinical outcomes in ADs. study characteristics, such as author name, year of publication, study design, duration, study location, sample size, diagnosis of ADs, type of medications, age and gender of patients, comor- METHODS bidities including hypertension, diabetes and obesity, prevalence Search strategy and study selection and clinical outcomes of COVID-19 were collected. We rated This meta- analysis was conducted according to a priori defined the quality of evidence according to the Grades of Recommen- protocol that is in accordance with Preferred Reporting Items dation, Assessment, Development and Evaluation (GRADE) for Systematic Reviews and Meta- Analyses guideline.5 The approach to assess the certainty of evidence obtained from the protocol of this meta- analysis has been submitted to the Interna- present meta- analysis.10 tional Prospective Register of Systematic Reviews.6 We searched PubMed/MEDLINE, Scopus, EMBASE, medRxiv (https://www. medrxiv. org/) from inception to 31 July 2020 to identify studies Outcome assessment assessing the prevalence and clinical outcomes of COVID-19 in The primary outcome was the prevalence of suspected or ADs. confirmed COVID-19 with a positive PCR test for SARS- CoV-2 As for inclusion criteria, we considered observational or in ADs. The numbers of patients with COVID-19 and confirmed case–controlled studies reporting the prevalence and clinical cases in each of studies are shown in online supplemental table outcomes of COVID-19 in ADs. There were no restrictions S1. To conduct subgroup analyses with each diagnosis, we classi- regarding age, sex or duration of the study. We imposed no fied ADs based on the digestive, musculoskeletal and integumen- geographic or language restrictions. Three authors (SA, SH tary systems. Diseases of the digestive system were categorised and AS) independently screened each of the potential studies into IBD and autoimmune hepatic diseases (AHD). Rheumatic to determine whether they were eligible for inclusion. Areas of diseases (RD) included rheumatoid arthritis, systemic lupus disagreement or uncertainty were resolved by consensus among erythematosus (SLE), psoriatic arthritis, spondyloarthritis, anky- the authors. Studies were identified with the following terms: losing spondylitis, vasculitis, polymyalgia rheumatica, Sjögren’s ‘COVID-19’, ‘inflammatory bowel disease’, ‘psoriasis’, ‘rheu- syndrome (SjS), systemic sclerosis (SSc) and other autoimmune- matic diseases’, ‘systemic lupus erythematosus’ and ‘autoim- mediated diseases (including Behcet’s syndrome, sarcoidosis and mune diseases’. inflammatory myopathies). Given that several studies of RD Single case reports were excluded. Given several studies used focused only on patients with SLE, SjS or SSc, these studies were initial data from C19- GRA registry, we included a study with categorised into ‘SLE/SjS/SSc’. Diseases of the skin were catego- data of the first 600 patients submitted to C19- GRA registry3 rised as ‘psoriasis/autoimmune skin diseases (AISD)’. Two studies and excluded other studies with preliminary data.7–9 For an included various ADs and were classified as ‘immune-mediated 11 12 analysis
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