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Rheumatoid arthritis and COVID-19 outcomes: a systematic review and Meta-analysis

BMC Rheumatology volume 8, Article number: 61 (2024) Cite this article

Abstract

Objectives

This study aimed to conduct a comprehensive systematic literature review and meta-analysis to assess the risk and outcomes of coronavirus disease 2019 (COVID-19) in patients with rheumatoid arthritis.

Methods

A systematic search was performed across four electronic databases. The quality of the studies was assessed using the Newcastle‒Ottawa quality assessment scale and the Joanna Briggs Institute critical appraisal checklist. Statistical analyses were conducted using STATA 14 software.

Results

A total of 62 studies were included in the analysis. First, the meta-analysis revealed the following prevalence rates among rheumatoid arthritis patients: COVID-19, 11%; severe COVID-19, 18%; COVID-19-related hospitalization, 29%; admission to the intensive care unit (ICU) due to COVID-19, 10%; and death from COVID-19, 8%. Second, rheumatoid arthritis was associated with an increased risk of COVID-19 infection (OR 1.045(0.969–1.122), p = 0.006), COVID-19-related hospitalization (OR 1.319(1.055–1.584), p = 0.006), admission to the ICU due to COVID-19 (OR 1.498(1.145–1.850), p = 0.002), and death from COVID-19 (OR 1.377(1.168–1.587), p = 0.001). Third, no statistically significant association was found between rheumatoid arthritis and severe COVID-19 (OR 1.354(1.002–1.706), p = 0.135).

Conclusions

Rheumatoid arthritis patients have a significantly greater risk of COVID-19 infection, hospitalization, ICU admission, and death than individuals without rheumatoid arthritis. However, rheumatoid arthritis did not show a significant association with the risk of severe COVID-19. These findings underscore the need for tailored management strategies and vigilant monitoring of COVID-19 outcomes in rheumatoid arthritis patients.

Systematic Review Registration

The study has been registered on PROSPERO [https://www.crd.york.ac.uk/PROSPERO/], and the registration number is CRD42024528119.

Peer Review reports

Introduction

The global impact of coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has been profound over the past four years, significantly affecting global health and mortality [1]. Initially, identified in China in December 2019, COVID-19 swiftly spread worldwide, resulting in substantial morbidity and mortality. As of April 13, 2024, there were 704,753,890 confirmed cases globally, with 7,010,681 reported deaths [2]. Risk factors for severe disease include advanced age, male sex, ethnicity, obesity, and underlying conditions such as hypertension, diabetes mellitus, and cardiovascular diseases [3,4,5,6,7,8].

Rheumatoid arthritis (RA) is a chronic inflammatory disorder characterized by progressive joint damage and synovial inflammation, often leading to debilitating physical impairments and increased mortality [9,10,11,12,13]. Globally, rheumatoid arthritis incidence estimates indicate a pooled prevalence of 0.46% (95% CI 0.37–0.57%) between 1986 and 2014, with an estimated prevalence of approximately 460 per 100,000 people as of 2019 [14]. Studies have consistently shown that rheumatoid arthritis patients are at increased risk for various infections, which can be attributed to immune dysregulation and immunosuppressive therapies [15,16,17,18,19,20,21,22,23].

Given these considerations, it is hypothesized that rheumatoid arthritis patients may encounter the increased susceptibility to SARS-CoV-2 infection and more severe COVID-19 outcomes than the general population. However, the literature presents conflicting findings. While some clinical trials have suggested that certain immunosuppressive treatments for rheumatoid arthritis might improve COVID-19 outcomes [24], other studies have reported no significant differences in COVID-19 incidence or hospitalization rates between rheumatoid arthritis patients and the general population [25,26,27]. Previous studies had been performed in the initial stages of the pandemic and there are additional studies published after the two reviews [28, 29], so it is important and necessary to include new studies for systematic review on this topic. Accordingly, our study aimed to comprehensively review the reported literatures, perform a meta-analysis, and assess the incidence and outcomes of COVID-19 in rheumatoid arthritis patients to clarify this important clinical issue.

Materials and methods

The review and meta-analysis adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [30, 31] and employed a Population, Exposure, Control, Outcome, and Study Design (PECOS) framework to guide study inclusion. Two authors independently conducted comprehensive searches across multiple databases, extracted data, and assessed methodological quality. Discrepancies were resolved through consensus or consultation with a third author.

Criteria for considering the studies for this review

Participants

Only adult patients diagnosed with rheumatoid arthritis were considered.

Exposure

Studies focusing on individuals diagnosed with rheumatoid arthritis were included.

Control

Cohort studies included participants without rheumatoid arthritis, while case‒control studies included non-COVID-19 patients.

Outcomes

Primary outcomes included incidence, risk, severe COVID-19(Severe COVID was defined as a condition where symptoms were worse than normal COVID but did not require hospitalization), hospitalization rates, admission to the ICU, and COVID-19 mortality. Studies lacking specific outcomes for rheumatoid arthritis patients were excluded.

Study design

Quantitative observational studies such as cohort, cross-sectional (descriptive and analytical), and case–control studies were considered, with descriptive cross-sectional studies reporting only prevalence grouped separately. Only studies published in full text in English were eligible.

Search Strategy and Study Selection

A systematic review of PubMed, EMBASE, Scopus, and the Cochrane Library was conducted from inception to March 17, 2024, using Boolean operators and truncation symbols to combine search terms. The detailed search strategy is provided in Supplementary Information S1. Additional studies were identified by screening reference lists and contacting authors for supplementary data as needed.

Study selection involved initial screening by two authors, who evaluated titles and abstracts followed by full-text reviews to determine final inclusion.

Data extraction and management

Data extraction was independently performed by two authors using a structured spreadsheet (available on request). The extracted information included the study characteristics (authors, publication year, design, settings, participants), outcomes, and event and sample sizes. When necessary, clarification was sought from the original study authors.

Quality of evidence

The risk of bias among the included studies was assessed using the Newcastle‒Ottawa Scale (NOS) [32], with studies scoring six or more stars considered high quality. Methodological quality and bias risk were evaluated independently by two authors using the NOS and the Joanna Briggs Institute critical appraisal checklist [33]. Funnel plots and statistical tests (Begg’s and Egger’s) were employed to assess publication bias, with sensitivity analysis conducted to gauge bias impact.

Statistical analysis

Data synthesis and statistical analyses were performed using STATA14 software. Prevalence rates were calculated with 95% CIs, and ORs/RRs were computed for risk outcomes. Statistical heterogeneity was assessed using Cochran’s Q statistic and Higgins and Thompson’s I², with the fixed-effect model used for meta-analysis when p ≥ 0.10 and I² ≤ 50%. Substantial heterogeneity prompted subgroup and sensitivity analyses. A p value < 0.05 indicated statistical significance.

Results

Results of literature search

A total of 17,490 relevant citations were initially identified through electronic databases and other search sources (PubMed 1195, EMBASE 3289, Cochrane Library 115, Scopus 12891 and other search sources 0), with 2286 duplicates removed. Ultimately, 62 studies [25,26,27, 34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92] were included in the qualitative synthesis after all ineligible articles were excluded, and all studies were included in the meta-analysis. All studies were published in English, and the details of the study selection process are illustrated in the flowchart (Fig. 1).

Fig. 1
figure 1

Flowchart

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Characteristics of the included studies

There were 3 case‒control studies, 31 cohort studies (retrospective or prospective cohort studies, population-based cohort studies), 15 cross-sectional studies (direct or web-based cross-sectional studies), and 13 prevalence studies. The studies spanned various years, with publications ranging from 2020 to 2024. Predominantly, studies originated from the USA (n = 8), followed by Italy (n = 6), Spain (n = 6), India (n = 5), and several other countries. The total sample included 690,191 patients with rheumatoid arthritis. The detailed characteristics of the studies are presented in Table 1.

Table 1 Characteristics of the included studies and patients
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Quality Assessment of the included studies

All studies underwent rigorous quality and bias assessment using the Joanna Briggs Institute guidelines. Supplementary Information S2 provides detailed results. In prevalence studies, some studies failed to report on the methods used to identify the disease and their reliability. In cross-sectional studies and cohort studies, the risk of bias was attributed to factors such as the identification and handling of confounders. For case‒control studies, cross-sectional studies, and cohort studies, we also used the Newcastle–Ottawa Scale (NOS) for scoring, and all studies scored above six stars, indicating good overall quality with acceptable bias risk (Supplementary Information S3). Overall, most studies were observed to be of good quality with an acceptable risk of bias.

Results of the Meta-analysis

Prevalence of COVID-19 and Risk of COVID-19

Thirty-six studies reported on the incidence of COVID-19 among rheumatoid arthritis patients. According to a random-effects model, due to significant heterogeneity (I² = 99.96%, p = 0.00), the pooled prevalence was 11% (95% CI 6–17%) (Fig. 2a).

Fig. 2
figure 2

(a)Prevalence of COVID-19 in RA patients; (b) Risk of COVID-19 among RA patients

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Twelve studies assessed the association between rheumatoid arthritis and COVID-19 risk. Moderate heterogeneity (I² = 63.3%, p = 0.002) warranted a random-effects model, revealing a pooled OR of 1.045 (95% CI 0.969, 1.122) (z = 2.76, p = 0.006) (Fig. 2b).

Severe COVID-19 in patients with rheumatoid arthritis

Eleven studies examined severe COVID-19 among rheumatoid arthritis patients with COVID-19. The significant heterogeneity (I² = 97.79%, p = 0.00) led to the use of a random-effects model, which estimated a pooled prevalence of 18% (95% CI 11–26%) (Fig. 3a).

Fig. 3
figure 3

(a) Severe COVID-19 among RA patients; (b) Risk of severe COVID-19 among RA patients

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Eight studies investigated the association between rheumatoid arthritis and severe COVID-19. Significant heterogeneity (I² = 98.3%, p = 0.000) was observed, with a pooled OR of 1.354 (95% CI 1.002, 1.706) (z = 1.49, p = 0.135) (Fig. 3b).

COVID-19-related hospitalization and ICU admission

Fourteen studies reported on COVID-19-related hospitalization in rheumatoid arthritis patients. The significant heterogeneity (I² = 99.61%, p = 0.00) led to the use of a random-effects model, which estimated a pooled prevalence of 29% (95% CI 20–39%) (Fig. 4a). Thirteen studies assessed this association, revealing a pooled OR of 1.319 (95% CI 1.055, 1.584) (z = 2.74, p = 0.006) (Fig. 4b).

Fig. 4
figure 4

(a) COVID-19 hospitalization among RA patients; (b) Risk of COVID-19 hospitalization among RA patients

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Seven studies reported COVID-19-related ICU admissions in rheumatoid arthritis patients. The significant heterogeneity (I² = 99.23%, p = 0.00) necessitated a random-effects model, which estimated a pooled prevalence of 10% (95% CI 5–16%) (Fig. 5a). The pooled OR was 1.498 (95% CI 1.145, 1.850) (z = 3.06, p = 0.002) across the five studies (Fig. 5b).

Fig. 5
figure 5

(a) ICU admission due to COVID-19 among RA patients; (b) Risk of ICU admission due to COVID-19 among RA patients

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Mortality in COVID-19 rheumatoid arthritis patients

Sixteen studies reported COVID-19-related mortality among rheumatoid arthritis patients. Significant heterogeneity (I² = 97.48%, p = 0.00) was detected with a random-effects model, which estimated an overall mortality rate of 8% (95% CI 5–11%) (Fig. 6a). For the association between rheumatoid arthritis and COVID-19 mortality, the pooled OR from thirteen studies was 1.377 (95% CI 1.168, 1.587) (z = 3.31, p = 0.001) (Fig. 6b).

Fig. 6
figure 6

(a)Morality rate in COVID-19 RA patients; (b) Risk of dying from COVID-19 in RA patients

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All the results of the above meta-analysis are shown in Table 2.

Table 2 The results of the meta-analysis. Note: **p < 0.01, △p > 0.05.ICU: intensive care unit
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Sensitivity analysis and publication bias

Sensitivity analysis using STATA 14 confirmed the stability of the meta-analysis results, with no significant deviations noted upon removal of influential studies. Publication bias assessments revealed potential bias in COVID-19 and severe COVID-19 incidence studies by examining funnel plots (Supplementary File S4a, c), supported by Begg’s and Egger’s tests (p = 0.001 and p = 0.016, respectively) (Table 3). Other outcomes showed no significant publication bias (Supplementary File S4b, d, e, f, g, h, i, j), reinforcing the robustness of the findings. All the results of Begg’s and Egger’s tests are shown in Table 3.

Table 3 Results of Begg’s test and Egger’s test. Note: *p < 0.05, **p < 0.01, △p > 0.05. ICU: intensive care unit
Full size table

Discussion

Summary of the main results

This meta-analysis aimed to comprehensively assess COVID-19 outcomes in patients with rheumatoid arthritis, addressing gaps left by previous reviews with limited study inclusion [29]. Most studies were from the USA, Italy, and Spain, highlighting potential underreporting in other regions due to resource constraints.

Our findings indicated a greater prevalence of COVID-19 among rheumatoid arthritis patients (12%) than among the global average (approximately 8%) (based on data provided on the WHO website(https://data.who.int/dashboards/covid19/cases?n=c)).

In addition, a statistically significant association between rheumatoid arthritis and COVID-19 was found in the risk estimate, which suggested that patients with rheumatoid arthritis were more susceptible to COVID-19 than the general population. This was consistent with the results of prior studies highlighting rheumatoid arthritis patients’ elevated infection risk [93]. Factors such as immunosuppression, chronic inflammatory states, and comorbidities might also be causes [94]. Notably, certain rheumatoid arthritis treatments, such as DMARDs, glucocorticoids and etanercept, are associated with increased COVID-19 risk. For example, Assar et al. reported that patients treated with > 20 mg/d prednisolone were at increased risk of getting COVID-19 [56]. Gracia et al. reported that anti-TNF-alpha treatment was associated with a more than 3-fold increased risk of contracting COVID-19 [62]. A study conducted by Valladales et al. suggested that the incidence of COVID-19 was greater among patients with rheumatoid arthritis who received DMARDs and glucocorticoids simultaneously than among patients with rheumatoid arthritis who did not receive these drug combinations [68]. Bagheri et al. provided evidence that etanercept therapy might increase the risk of developing COVID-19 in patients with rheumatoid arthritis [83]. Apparently, the mechanism might stem from the suppression of a protective immune state in rheumatoid arthritis patients.

Our meta-analysis revealed that the incidence of severe COVID-19 among rheumatoid arthritis patients was 18%. For the risk of severe COVID-19, some studies have reported that patients with rheumatoid arthritis have an increased risk of severe COVID-19 [44, 60, 70, 80]. In contrast, other studies have suggested that COVID-19 severity is not associated with rheumatoid arthritis [25, 51, 55]. Overall, the pooled results indicated that rheumatoid arthritis was not a risk factor for severe COVID-19. This discrepancy underscores the need for standardized severity definitions and more data to clarify these findings.

The hospitalization and ICU admission rates for COVID-19 in rheumatoid arthritis patients were notably high, at 29% and 13%, respectively. Similarly, the pooled mortality rate of 9% among rheumatoid arthritis patients due to COVID-19 starkly contrasted with the global mortality rate of approximately 1% (roughly calculated according to data provided on the WHO website)1. In addition, rheumatoid arthritis patients might be more likely to be hospitalized due to COVID-19, and a similar trend was observed in terms of the risk of ICU admission for COVID-19. Moreover, compared with control patients, rheumatoid arthritis patients had a greater risk of dying from COVID-19. These outcomes suggest that compared with the general population, rheumatoid arthritis patients are more likely to experience severe COVID-19 and have worse clinical outcomes.

Figueroa et al. reported that rheumatoid arthritis with interstitial lung disease might be a substantial contributor to severe COVID-19 in patients with rheumatoid arthritis [60]. A study conducted by Gomides et al. demonstrated that heart disease and the use of glucocorticoids were associated with a greater number of hospital admissions for COVID-19 in patients with rheumatoid arthritis [61]. Singh et al. reported that rituximab was associated with hospitalization and ICU admission for COVID-19 in patients with rheumatoid arthritis [79]. Similarly, Tsai et al. reported that patients with rheumatoid arthritis caused by the use of Janus-associated kinase inhibitors (JAKis) had a significant risk for hospitalization, mortality or composite adverse outcomes, especially mortality, among those without COVID-19 vaccination [81]. In addition, advanced age, comorbid conditions (such as hypertension and diabetes), and a history of previous serious infections might be associated with a more severe COVID-19 disease course [73, 79, 84, 85, 89]. Some treatment options for rheumatoid arthritis might contribute to severe COVID-19 outcomes in patients with rheumatoid arthritis. However, compared with the comparator cohort, patients with rheumatoid arthritis were at a greater risk of severe or critical COVID-19, while non-TNFi biologics and systemic therapies did not further increase the risk [58]. These results might guide the development or modification of treatment plans for rheumatoid arthritis patients infected with SARS-CoV-2 or other similar viruses [83].

Potential biases in the review process

There was a significant level of heterogeneity observed in the pooled analysis of all outcomes, such as the prevalence of COVID-19, the risk of severe COVID-19, the prevalence and the risk of COVID-19-related hospitalization, the prevalence of admission to the ICU due to COVID-19 and the risk of admission to the ICU due to COVID-19, and the mortality and the risk of death from COVID-19, except for the risk of COVID-19 and the prevalence of severe COVID-19. Heterogeneity might stem from varying follow-up durations, disparate pandemic control measures, and regional differences in healthcare protocols. Subgroup analyses were not conducted due to insufficient data granularity. In addition, different treatments for rheumatoid arthritis and disease activity might also result in heterogeneity. However, publication bias was minimal, suggesting that the included studies were generally of high quality. Sensitivity analysis confirmed the robustness of our findings.

Limitations

Limitations include potential underreporting of data, especially from regions with limited resources. Variability in outbreak severity and control measures between countries also introduced inevitable heterogeneity. And due to the lack of relevant details, it was difficult to analyze some important points such as drug combination and disease activity in patients with RA. Additionally, the inclusion of single-center and small-scale studies might have influenced the overall results.

Conclusion

In conclusion, our meta-analysis revealed that compared with non- rheumatoid arthritis patients, rheumatoid arthritis patients are at greater risk of COVID-19 infection, hospitalization, ICU admission, and mortality. However, no significant association was found between rheumatoid arthritis and severe COVID-19. Future research should focus on standardizing severity definitions and assessing the impact of specific rheumatoid arthritis treatments on COVID-19 outcomes to optimize patient management strategies.

Data availability

Data is provided within the manuscript or supplementary information files.

Abbreviations

COVID-19:

Coronavirus disease 2019

ICU:

Intensive care unit

SARS-CoV-2:

Severe acute respiratory syndrome coronavirus 2

PRISMA:

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses

NOS:

The Newcastle‒Ottawa Scale

JAKis:

Janus-associated kinase inhibitors

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Acknowledgements

We would like to thank all the patients and researchers who have contributed to the related studies.

Funding

The funding project number is [cstc2019jscx-dxwtBX0023].

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Author notes

  1. Liang Jin and Jianping Gan contributed equally to this work.

Authors and Affiliations

  1. Faculty of Chinese Medicine, Macau University of Science and Technology, Macau, China

    Liang Jin, Yue Wang & Vincent Kam Wai Wong

  2. Department of Rheumatology, Chongqing Hospital of Chinese Medicine, Chongqing, 400021, China

    Liang Jin & Jianping Gan

  3. The First School of Clinical Medicine, Nanjing University of Chinese Medicine, Nanjing, 210046, China

    Yun Lu & Yue Wang

  4. Sichuan Vocational College of Health and Rehabilitation, Zigong, 643000, China

    Xuewei Li

  5. Jiangsu Province Hospital of Chinese Medicine, Affiliated Hospital of Nanjing University of Chinese Medicine, 155 Hanzhong Rd, Nanjing, 210029, Jiangsu, China

    Yue Wang

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Contributions

V.K.W.W and WY designed the study. JL, GJP, LXW, and LY collected the data. JL and GJP drafted the manuscript. V.K.W.W, and WY contributed to revise the manuscript. All authors reviewed the manuscript.

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Correspondence to Liang Jin, Yue Wang or Vincent Kam Wai Wong.

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Jin, L., Gan, J., Li, X. et al. Rheumatoid arthritis and COVID-19 outcomes: a systematic review and Meta-analysis. BMC Rheumatol 8, 61 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s41927-024-00431-5

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s41927-024-00431-5

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BMC Rheumatology

ISSN: 2520-1026

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