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Factors associated with hospitalizations for Covid-19 in patients with rheumatoid arthritis: data from the Reumacov Brazil registry

Advances in Rheumatology volume 62, Article number: 13 (2022) Cite this article

Abstract

Background

Patients using immunosuppressive drugs may have unfavorable results after infections. However, there is a lack of information regarding COVID-19 in these patients, especially in patients with rheumatoid arthritis (RA). Therefore, the aim of this study was to evaluate the risk factors associated with COVID-19 hospitalizations in patients with RA.

Methods

This multicenter, prospective cohort study is within the ReumaCoV Brazil registry and included 489 patients with RA. In this context, 269 patients who tested positive for COVID-19 were compared to 220 patients who tested negative for COVID-19 (control group). All patient data were collected from the Research Electronic Data Capture database.

Results

The participants were predominantly female (90.6%) with a mean age of 53 ± 12 years. Of the patients with COVID-19, 54 (20.1%) required hospitalization. After multiple adjustments, the final regression model showed that heart disease (OR = 4.61, 95% CI 1.06–20.02. P < 0.001) and current use of glucocorticoids (OR = 20.66, 95% CI 3.09–138. P < 0.002) were the risk factors associated with hospitalization. In addition, anosmia was associated with a lower chance of hospitalization (OR = 0.26; 95% CI 0.10–0.67, P < 0.005).

Conclusion

Our results demonstrated that heart disease and the use of glucocorticoids were associated with a higher number of hospital admissions for COVID-19 in patients with RA.

Trial registration: Brazilian Registry of Clinical Trials - RBR-33YTQC.

Background

The COVID-19 pandemic has raised additional concerns for rheumatologists, especially related to health care for patients with immune-mediated rheumatic diseases (IMRDs) [1, 2]. Notably, immunosuppression resulting from disease or treatment itself is considered a relevant risk factor for higher infection susceptibility and more severe outcomes [3].

Although some evidence on the course of SARS-CoV-2 infections in patients with IMRDs has already been demonstrated, such as a similar COVID-19 prevalence to that of the general population [4], there are some knowledge gaps and uncertainties regarding the peculiarities and possible unfavorable outcomes, including hospitalization rate, frequency of admission to intensive care centers and severity [5,6,7,8,9,10,11]. In addition, immunosuppressive treatments for underlying diseases, glucocorticoids, and cyclophosphamide may contribute to unfavorable outcomes [12, 13]. On the other hand, a hypothesis has been presented that some immunomodulatory drugs, such as conventional or biological disease-modifying anti-rheumatic drugs (DMARDs), can help to mitigate the inflammation and cytokine storm induced by SARS-CoV-2 [14, 15].

Considering the rheumatoid arthritis (RA) treatment scenario, which includes disease activity, low-dose prednisone, methotrexate, TNF blockers, IL-6 antagonists, JAK inhibitors, and anti-CD20 therapy, as a prototype for these findings, this study had the main aim of evaluating the risk factors associated with COVID-19 hospitalizations in patients with RA.

Methods

This was a cross-sectional analysis performed only in patients with RA who were enrolled in the ReumaCoV-Brazil Registry, a multicenter, prospective cohort study, used to evaluate and monitor patients with IMRDs during the COVID-19 pandemic. The complete methodology and initial data were published previously [12, 16]. Eligible patients were selected through a convenience sample after the researchers contacted patients with RA and COVID-19 via telephone calls and noted similar patients in outpatient care or hospitals. They then compared the patients with RA who had COVID-19 with patients with RA who did not have COVID-19.

The following inclusion criteria were considered: (a) an age older than 18 years; (b) a diagnosis of COVID-19, according to the Ministry of Health; and (c) a previous diagnosis of RA, according to the American College of Rheumatology or the European League against Rheumatism criteria. The exclusion criteria were patients with HIV or other immunodeficiency diseases, previous organ or bone marrow transplants, neoplasms in the last five years, current chemotherapy treatment and diseases of the thymus.

The Research Electronic Data Capture (REDCap) (https://www.project-redcap.org/) electronic database was used to collect and record the patients’ sociodemographic aspects and information on RA (time of disease, disease activity, laboratory data, use of DMARDs and other concomitant medications, comorbidities and details about the COVID-19 infection (clinical manifestations, treatment and outcomes)). Information was obtained by telephone or a face-to-face consultation, according to the local recommendations due to the pandemic, and through medical records in the event of hospitalization.

Statistical analysis

Initially, the data were analyzed descriptively. For categorical variables, absolute and relative frequencies were presented, and for numerical variables, summary measures (mean, median, minimum, maximum and standard deviation) were presented. For associations among categorical variables, the chi-square test was used, or Fisher’s exact test was used when cells had expected values of less than five counts. In cases of discrepancies, the standardized adjusted residue was used to identify local differences–cells with absolute values above 1.96 indicated significant deviations from expected values assignable only to random variations.

The comparisons of the means between two groups and more than two groups were performed using Student’s t-test for independent samples and analysis of variance (ANOVA), respectively. Normality in data distribution was verified by the Kolmogorov–Smirnov test. In the event of assumption violations to Student’s t-test and ANOVA, the Mann–Whitney and Kruskal–Wallis nonparametric tests were used, respectively. Once the Kruskal–Wallis test was significant, the location of paired differences was determined by Dunn Bonferroni tests, maintaining an overall significance level of 5%.

To assess the simultaneous effects of the demographic and clinical characteristics (e.g., predictor variables) on hospitalizations (e.g., dependent variable), univariate and multivariate logistic regressions were adjusted. For the initial multivariate models, predictor variables whose associations with the dependent variable were significant at 10% in the univariate logistic regression were selected. Then, a backward procedure was conducted by excluding the variables one by one in order of significance that were not found to be more significant at 5% in the multivariate regression than those in the final model. The final model fit was then evaluated by a Hosmer and Lemeshow test. Due to the large number of predictor variables and the small number of events, the variables whose associations with the dependent variable were significant amounted to 10% in the univariate logistic regression. Then, the variables that were not significant to 5% were excluded one by one in order of significance (backward method). In addition, the adjustment adequacy of the final model was evaluated by the Hosmer and Lemeshow test.

For all statistical tests, a significance level of 5% was used. Statistical analyses were performed using SPSS 20.0 statistical software.

This study was approved by the Brazilian Committee of Ethics in Human Research on April 5, 2020, (CAAE 30,186,820.2.1001.8807) and registered on the Brazilian Registry of Clinical Trials (RBR-33YTQC) on June 1, 2020. All patients signed informed consent forms, and the results of the study are presented in an aggregated form, guaranteeing confidentiality and ensuring that there are no risks to patients’ well-being and care.

Results

From May 24, 2020, to January 31, 2021, 489 patients with RA were included: 269 tested positive for COVID-19, and 220 tested negative for COVID-19 (control group). There was a female predominance (n = 442; 90.6%) with a mean age of 53 ± 12 years. Considering only the patients with COVID-19, 54 (20.1%) patients required hospitalization.

Comparing hospitalized patients with COVID-19 with outpatients, patients with COVID-19 were older, and had one, two or more comorbidities present. Diabetes mellitus and hypertension were significantly more prevalent in those who required hospital care (Table 1). In addition, patients with shortness of breath, cough and vomiting were significantly more likely to be hospitalized. On the other hand, patients with anosmia and dysgeusia had a lower hospitalization rate (Table 2).

Table 1 General characteristics and comorbidities of patients with rheumatoid arthritis and COVID-19
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Table 2 Symptoms related to COVID-19 in patients with rheumatoid arthritis
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Considering specific findings related to RA, including autoantibody status and cumulative damage (erosions), extra-articular manifestations, withdrawal therapy, and the current use of azathioprine and corticosteroids were associated with hospitalization. On the other hand, patients on TNF inhibitors had a significantly lower frequency of hospitalization (Tables 3 and 4).

Table 3 Characteristics of rheumatoid arthritis in the studied population
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Table 4 Disease-modifying antirheumatic or immunossupressive drugs used by patients with rheumatoid arthritis at the time of the study
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After multiple adjustments, the final regression model showed that the risk factors significantly associated with hospitalization were shortness of breath (OR 6.12; 95% CI 2.34–16.06, P < 0.001), vomiting (OR 4.06; 95% CI 1.4–11.79, P < 0.01), heart disease (OR 4.61; 95% CI 1.06–20.02, P < 0.001), and the current use of glucocorticoids (OR 20.66; 95% CI 3.09–138, P < 0.002). Moreover, anosmia was associated with a lower chance of hospitalization (OR 0.26; 95% CI 0.10–0.67, P < 0.005) (Table 5). The results of the univariate logistic regression model are presented in the Additional file 1.

Table 5 Multivariate logistic regression models for the outcome variable hospitalization in patients with rheumatoid arthritis and covid-19”
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Discussion

Our data demonstrated that approximately 20% of patients with RA required hospitalization because of COVID-19, a rate lower than that in another large registry study (38%) [13] but similar to the second analysis from the same database (21%) [17]. The findings suggest that other details beyond disease alone could be involved, including genetic background and epidemiological differences (e.g., spreading time or viral community transmission) among the countries.

The main advantage of our study was the inclusion of a large sample of patients with RA. In addition, all data were preparametrized, prestandardized and captured by a trained rheumatologist and with laboratory test confirmation for those who tested positive for COVID-19.

Considering the traditional risk factors related to COVID-19 severity, our results did not find a significant association with age after multiple adjustments for cofounders, which is contrary to other studies from the general population and IMRD cohorts [13, 18,19,20,21].

However, heart disease, as a comorbidity, was significantly associated with hospitalization, which is in accordance with the current literature [22,23,24,25,26,27,28,29,30,31,32,33].

These results suggest that the comorbidity burden seems to be similar to several reports from the general population, regardless of underlying rheumatic disease [13, 31,32,33,34,35,36,37,38,39,40,41].

Although some clinical findings were associated with hospitalization in our cohort, such as shortness of breath and vomiting, these findings may be redundant because they are considered red flags or parameters for hospitalization [37,38,39,40,41,42,43,44,45,46,47,48]. Therefore, this particular result should be interpreted with caution, especially in a cross-sectional analysis.

Interestingly, anosmia, an important specific clinical marker for COVID-19 [48], had a protective behavior against hospitalization, as previously reported by other authors [44,45,46,47,48,49,50]. Thus, our data suggest that anosmia could be seen as a potential clinical marker of mild COVID-19 severity in patients with RA.

It is worth emphasizing that the clinical and laboratory characteristics of RA and DMARDs (e.g., conventional, biological and targeted synthetic medications) were not associated with hospitalization in the final analysis, except for the current use of glucocorticoids (dosage equal to or greater than 10 mg/day). This is a recurrent finding among the studies [12, 13].

Patients with RA on TNF inhibitors had a lower rate of hospitalizations in the initial analysis but this finding was not confirmed after multivariate analysis which is contrary to own findings when considering the entire sampling of patients with IMRDs [12] and the Global Alliance Rheumatology (GRA) database [13, 51] and another study published in the literature [52].

In addition, the second analysis of the GRA database that involved 2869 patients with RA found that rituximab (OR = 4.15; 95% CI 3.16–5.44) and JAK inhibitors (OR = 2.06; 95% CI 1.60–2.65) were significantly associated with COVID-19 severity [17]. Our data did not confirm the last reports.

Our study has some limitations, such as the convenience sample and small number of patients, cross-sectional analysis of an ongoing prospective cohort, the low number of rituximab users and specific DMARD targets and the lack of information on disease activity. On the other hand, our study included a national sample with a more homogeneous rate of community viral transmission, social distancing measures and immunization.

Conclusions

Our data showed traditional risk factors, including heart disease as a comorbidity, and the current use of glucocorticoids are more involved with hospitalizations for COVID-19 in patients with RA than the underlying IMRDs alone.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

RA:

Rheumatoid arthritis

IMRDS:

Immune-mediated rheumatic diseases

DMARDS:

Disease-modifying anti-rheumatic drugs

References

  1. D’Antiga L. Coronaviruses and immunosuppressed patients: the facts during the third epidemic. Liver Transpl. 2020;26:832–4.

    Article  PubMed  Google Scholar 

  2. Venerito V, Lopalco G, Iannone F. COVID-19, rheumatic diseases and immunosuppressive drugs: an appeal for medication adherence. Rheumatol Int. 2020;40:827–8.

    Article  CAS  PubMed  Google Scholar 

  3. Falagas ME, Manta KG, Betsi GI, Pappas G. Infection-related morbidity and mortality in patients with connective tissue diseases: a systematic review. Clin Rheumatol. 2007;26:663–70.

    Article  PubMed  Google Scholar 

  4. Favalli EG, Ingegnoli F, De Lucia O, Cincinelli G, Cimaz R, Caporali R. COVID-19 infection and rheumatoid arthritis: Faraway, so close! Autoimmun Rev. 2020;19:102523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. D’Silva KM, Serling-Boyd N, Wallwork R, Hsu T, Fu X, Gravallese EM, Clinical characteristics and outcomes of patients with coronavirus disease, et al. (COVID-19) and rheumatic disease: a comparative cohort study from a US ‘hot spot.’ Ann Rheum Dis. 2019;79:1156–62.

    Article  CAS  Google Scholar 

  6. Freites-Nuñez DD, Leon L, Mucientes A, Rodriguez-Rodriguez L, Font Urgelles J, Madrid García A, et al. Risk factors for hospital admissions related to COVID-19 in patients with autoimmune inflammatory rheumatic diseases. Ann Rheum Dis. 2020;79:1393–9.

    Article  CAS  PubMed  Google Scholar 

  7. Cheng C, Li C, Zhao T, Yue J, Yang F, Yan Y, Liu X. COVID-19 with rheumatic diseases: a report of 5 cases. Clin Rheumatol. 2020;39:2025–9.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Zhong J, Shen G, Yang H, Huang A, Chen X, Dong L, et al. COVID-19 in patients with rheumatic disease in Hubei province, China: a multicentre retrospective observational study. Lancet Rheumatol. 2020;2:e557–64.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Michelena X, Borrell H, López-Corbeto M, López-Lasanta M, Moreno E, Pascual-Pastor M, et al. Incidence of COVID-19 in a cohort of adult and paediatric patients with rheumatic diseases treated with targeted biologic and synthetic disease-modifying anti-rheumatic drugs. Semin Arthritis Rheum. 2020;50:564–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Murray K, Quinn S, Turk M, O’Rourke A, Molloy E, O’Neill L, et al. COVID-19 and rheumatic musculoskeletal disease patients: infection rates, attitudes and medication adherence in an Irish population. Rheumatology (Oxford). 2021;60:902–6.

    Article  CAS  Google Scholar 

  11. Ye C, Cai S, Shen G, Guan H, Zhou L, Hu Y, et al. Clinical features of rheumatic patients infected with COVID-19 in Wuhan. China Ann Rheum Dis. 2020;79:1007–13.

    Article  CAS  PubMed  Google Scholar 

  12. Marques CDL, Kakehasi AM, Pinheiro MM, Mota LMH, Albuquerque CP, Silva CR, et al. High levels of immunosuppression are related to unfavourable outcomes in hospitalised patients with rheumatic diseases and COVID-19: first results of ReumaCoV Brasil registry. RMD Open. 2021;7:e001461.

    Article  PubMed  Google Scholar 

  13. Gianfrancesco M, Hyrich KL, Al-Adely S, Carmona L, Danila MI, Gossec L, et al. Characteristics associated with hospitalisation for COVID-19 in people with rheumatic disease: data from the COVID-19 Global Rheumatology Alliance physician-reported registry. Ann Rheum Dis. 2020;79:859–66.

    Article  CAS  PubMed  Google Scholar 

  14. Nuño L, Novella Navarro M, Bonilla G, Franco-Gómez K, Aguado P, Peiteado D, et al. Clinical course, severity and mortality in a cohort of patients with COVID-19 with rheumatic diseases. Ann Rheum Dis. 2020;79:1659–61.

    Article  CAS  PubMed  Google Scholar 

  15. Haberman RH, Castillo R, Chen A, Yan D, Ramirez D, Sekar V, et al. COVID-19 in patients with inflammatory arthritis: a prospective study on the effects of comorbidities and disease-modifying antirheumatic drugs on clinical outcomes. Arthritis Rheumatol. 2020;72:1981–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Marques C, Kakehasi AM, Gomides APM, Paiva EDS, Dos Reis Neto ET, Pileggi GCS, et al. A Brazilian cohort of patients with immuno-mediated chronic inflammatory diseases infected by SARS-CoV-2 (ReumaCoV-Brasil Registry): protocol for a prospective. Observational Study. JMIR Res Protoc. 2020;9:e24357.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Klopfenstein T, Kadiane-Oussou NJ, Toko L, Royer PY, Lepiller Q, Gendrin V, et al. Features of anosmia in COVID-19. Med Mal Infect. 2020;50:436–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ilardi A, Politi C, Ciarambino T. COVID-19: could sex and age be a risk factor? Minerva Med. 2020. https://doi.org/10.23736/S0026-4806.20.06705-1.

    Article  PubMed  Google Scholar 

  19. Rod JE, Oviedo-Trespalacios O, Cortes-Ramirez J. A brief-review of the risk factors for covid-19 severity. Rev Saude Publica. 2020;54:60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gao YD, Ding M, Dong X, Zhang JJ, Kursat Azkur A, Azkur D, et al. Risk factors for severe and critically ill COVID-19 patients: a review. Allergy. 2021;76:428–55.

    Article  CAS  PubMed  Google Scholar 

  21. Freites Nuñez DD, Leon L, Mucientes A, Rodriguez-Rodriguez L, Font Urgelles J, Madrid García A, Colomer JI, Jover JA, Fernandez-Gutierrez B, Abasolo L. Risk factors for hospital admissions related to COVID-19 in patients with autoimmune inflammatory rheumatic diseases. Ann Rheum Dis. 2020;79(11):1393–9.

    Article  CAS  PubMed  Google Scholar 

  22. Ahmed S, Gasparyan AY, Zimba O. Comorbidities in rheumatic diseases need special consideration during the COVID-19 pandemic. Rheumatol Int. 2021;41:243–56.

    Article  CAS  PubMed  Google Scholar 

  23. Richardson S, Hirsch JS, Narasimhan M, Crawford JM, McGinn T, Davidson KW, et al. Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City Area. JAMA. 2020;323:2052–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Guan WJ, Liang WH, Zhao Y, Liang HR, Chen ZS, Li YM, et al. Comorbidity and its impact on 1590 patients with COVID-19 in China: a nationwide analysis. Eur Respir J. 2020;14(55):2000547.

    Article  CAS  Google Scholar 

  25. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395:1054–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zheng Z, Peng F, Xu B, Zhao J, Liu H, Peng J, et al. Risk factors of critical & mortal COVID-19 cases: a systematic literature review and meta-analysis. J Infect. 2020;81:e16–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hasseli R, Mueller-Ladner U, Schmeiser T, Hoyer BF, Krause A, Lorenz HM, et al. National registry for patients with inflammatory rheumatic diseases (IRD) infected with SARS-CoV-2 in Germany (ReCoVery): a valuable mean to gain rapid and reliable knowledge of the clinical course of SARS-CoV-2 infections in patients with IRD. RMD Open. 2020;6:e001332.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kang Y, Chen T, Mui D, Ferrari V, Jagasia D, Scherrer-Crosbie M, et al. Cardiovascular manifestations and treatment considerations in COVID-19. Heart. 2020;106:1132–41.

    Article  CAS  PubMed  Google Scholar 

  29. Yahia F, Zakhama L, Ben AA. COVID-19 and Cardiovascular diseases. Scoping review study. Tunis Med. 2020;98:283–94.

    PubMed  Google Scholar 

  30. Li B, Yang J, Zhao F, Zhi L, Wang X, Liu L, et al. Prevalence and impact of cardiovascular metabolic diseases on COVID-19 in China. Clin Res Cardiol. 2020;109:531–8.

    Article  CAS  PubMed  Google Scholar 

  31. Cancarevic I, Malik BH. SARS-CoV-2 (COVID 19) Infection in hypertensive patients and in patients with cardiac disease. Cureus. 2020;12:e8557.

    PubMed  PubMed Central  Google Scholar 

  32. Pinheiro MM, Pileggi GS, Kakehasi AM, Reis APMG, Reis-Neto ET, Abreu MM, et al. Incidence and risk factors for moderate/severe COVID-19 in rheumatic diseases patients on hydroxychloroquine: a 24-week prospective cohort. Clin Exp Rheumatol. 2021. https://doi.org/10.55563/clinexprheumatol/67oyux.

  33. Cacciapaglia F, Manfredi A, Erre G, Piga M, Sakellariou G, Viapiana O, et al. Correspondence on “Characteristics associated with hospitalisation for COVID-19 in people with rheumatic disease: data from the COVID-19 global rheumatology alliance physician-reported registry” by Gianfrancesco M et al. The impact of cardiovascular comorbidity on COVID-19 infection in a large cohort of rheumatoid arthritis patients. Ann Rheum Dis. 2020. https://doi.org/10.1136/annrheumdis-2020-218813.

    Article  PubMed  Google Scholar 

  34. Fredi M, Cavazzana I, Moschetti L, Andreoli L, Franceschini F. COVID-19 in patients with rheumatic diseases in northern Italy: a single-centre observational and case-control study. Lancet Rheumatol. 2020;2:e549–56.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Montero F, Martínez-Barrio J, Serrano-Benavente B, González T, Rivera J, Molina Collada J, et al. Coronavirus disease 2019 (COVID-19) in autoimmune and inflammatory conditions: clinical characteristics of poor outcomes. Rheumatol Int. 2020;40:1593–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pistone A, Tant L, Soyfoo MS. Clinical course of COVID-19 infection in inflammatory rheumatological patients: a monocentric Belgian experience. Rheumatol Adv Pract. 2020;4:55.

    Google Scholar 

  37. Santos CS, Morales CM, Álvarez ED, Castro CÁ, Robles AL, Sandoval TP. Determinants of COVID-19 disease severity in patients with underlying rheumatic disease. Clin Rheumatol. 2020;39:2789–96.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Pablos JL, Galindo M, Carmona L, Lledó A, Retuerto M, Blanco R, et al. Clinical outcomes of hospitalised patients with COVID-19 and chronic inflammatory and autoimmune rheumatic diseases: a multicentric matched cohort study. Ann Rheum Dis. 2020;79:1544–9.

    Article  CAS  PubMed  Google Scholar 

  39. Characteristics associated with Covid-19 in patients with Rheumatic Disease in Latin America: data from the Covid-19 Global Rheumatology Alliance physician-reported registry. Available at https://www.globalrheumpanlar.org/node/254. Accessed on 12/03/20222

  40. Gimeno-Miguel A, Bliek-Bueno K, Poblador-Plou B, Carmona-Pírez J, Poncel-Falcó A, González-Rubio F, et al. Chronic diseases associated with increased likelihood of hospitalization and mortality in 68, 913 COVID-19 confirmed cases in Spain: a population-based cohort study. PLoS ONE. 2021;16(11):e0259822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Korakas E, Ikonomidis I, Kousathana F, Balampanis K, Kountouri A, Raptis A, et al. Obesity and COVID-19: immune and metabolic derangement as a possible link to adverse clinical outcomes. Am J Physiol Endocrinol Metab. 2020;319(1):E105–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan. China Lancet. 2020;395:497–506.

    Article  CAS  PubMed  Google Scholar 

  43. Johnson KD, Harris C, Cain JK, Hummer C, Goyal H, Perisetti A. Pulmonary and extra-pulmonary clinical manifestations of COVID-19. Front Med (Lausanne). 2020;7:526.

    Article  Google Scholar 

  44. Du RH, Liu LM, Yin W, Wang W, Guan LL, Yuan ML, et al. Hospitalization and critical care of 109 decedents with COVID-19 pneumonia in Wuhan. China Ann Am Thorac Soc. 2020;17:839–46.

    Article  PubMed  Google Scholar 

  45. Zhang T, Liu D, Tian D, Xia L. The roles of nausea and vomiting in COVID-19: did we miss something? J Microbiol Immunol Infect. 2020. https://doi.org/10.1016/j.jmii.2020.10.005.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Zhong P, Xu J, Yang D, Shen Y, Wang L, Feng Y, et al. COVID-19-associated gastrointestinal and liver injury: clinical features and potential mechanisms. Signal Transduct Target Ther. 2020;5:256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Mao R, Qiu Y, He JS, Tan JY, Li XH, Liang J, et al. Manifestations and prognosis of gastrointestinal and liver involvement in patients with COVID-19: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2020;5:667–78.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Symptoms of Coronavirus, US Centers for Disease Control and Prevention. https://www.cdc.gov/coronavirus/2019-ncov/symptoms-testing/symptoms.html. Acessed 20 May 2021.

  49. Yan CH, Faraji F, Prajapati DP, Ostrander BT, De Conde AS. Self-reported olfactory loss associates with outpatient clinical course in COVID-19. Int Forum Allergy Rhinol. 2020;10:821–31.

    Article  PubMed  Google Scholar 

  50. Giacomelli A, Pezzati L, Conti F, Bernacchia D, Siano M, Oreni L, et al. Self-reported olfactory and taste disorders in patients with severe acute respiratory coronavirus 2 infection: a cross-sectional study. Clin Infect Dis. 2020;28(71):889–90.

    Article  CAS  Google Scholar 

  51. Sparks JA, Wallace ZS, Seet AM, Gianfrancesco MA, Izadi Z, Hyrich KL, et al. COVID-19 global rheumatology. Alliance Associations of baseline use of biologic or targeted synthetic DMARDs with COVID-19 severity in rheumatoid arthritis: results from the COVID-19 Global Rheumatology Alliance physician registry. Ann Rheum Dis. 2021;80:1137–46.

    Article  CAS  PubMed  Google Scholar 

  52. Izadi Z, Brenner EJ, Mahil SK, Dand N, Yiu ZZN, Yates M, et al. Association between tumor necrosis factor inhibitors and the risk of hospitalization or death among patients with immune-mediated inflammatory disease and COVID-19. JAMA Netw Open. 2021;4(10):e2129639.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Foster KJ, Jauregui E, Tajudeen B, Bishehsari F, Mahdavinia M. Smell loss is a prognostic factor for lower severity of coronavirus disease. Ann Allergy Asthma Immunol. 2020. https://doi.org/10.1016/j.anai.2020.07.023.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Talavera B, García-Azorín D, Martínez-Pías E, Trigo J, Hernández-Pérez I, Valle-Peñacoba G, et al. Anosmia is associated with lower in-hospital mortality in COVID-19. J Neurol Sci. 2020;419:117163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Xydakis MS, Dehgani-Mobaraki P, Holbrook EH, Geisthoff UW, Bauer C, Hautefort C, et al. Smell and taste dysfunction in patients with COVID-19. Lancet Infect Dis. 2020;20:1015–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank to the Brazilian Society of Rheumatology for technical support and rapid nationwide mobilization and to all collaborators on behalf of the ReumaCoV Brasil registry.

Funding

This work has been funded by the Research Funding of the Brazilian Society of Rheumatology and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico –MCTIC/CNPq/FNDCT/MS/SCTIE/Decit Nº 07/2020).

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Authors and Affiliations

  1. Faculdade de Ciências da Educação e Saúde, Centro Universitário de Brasília, Brasília, Brazil

    Ana Paula Monteiro Gomides, Cleandro Pires de Albuquerque, Licia Maria Henrique da Mota, Guilherme Devidé, Laiza Hombre Dias, Angela Luzia Branco Pinto Duarte, Raquel Altoé Giovelli, Thais Evelyn Karnopp, Hugo Deleon de Lima, Adriana Marinho, Marianne Schrader de Oliveira, Felipe Omura, Aline Ranzolin, Gustavo Resende, Francinne Machado Ribeiro, Sandra Lúcia Euzébio Ribeiro, Nathália de Carvalho Sacilotto, Wander Gonzaga dos Santos, Samuel Katsuyuki Shinjo, Samia Araujo de Sousa Studart, Flávia Patricia Sena Teixeira, Michel Alexandre Yazbek, Gilda Aparecida Ferreira, Odirlei A. Monticielo, Eduardo Paiva, Gecilmara Cristina Salviato Pileggi, Edgard Torres dos Reis-Neto, Marcelo de Medeiros Pinheiro & Claudia D. L. Marques

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Consortia

On behalf of ReumaCoV Brasil Registry

Contributions

MMP, LMHM, GAF, CDLM conceived the study and developed the protocol. APMG, and CPA wrote the manuscript with input from all other authors. All authors participated in data collection, critically read the manuscript and approved the final submitted version. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ana Paula Monteiro Gomides.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Brazilian Committee of Ethics in Human Research on April 5, 2020, (CAAE 30186820.2.1001.8807) and registered on the Brazilian Registry of Clinical Trials (RBR-33YTQC) on June 1, 2020. All patients signed informed consent forms.

Consent for publication

Not applicable.

Competing interests

APMG: Personal or institutional support: Pfizer, Abvie, Janssen. Advisory board: Pfizer. CPA: personal fees and/or non-financial support from Pfizer, AbbVie, AstraZeneca, Janssen, Bristol-Myers Squibb, Roche, Novartis and UCB. LMHM: Personal or institutional support from AbbVie, Janssen, Pfizer and Roche; delivered speeches at events related to this work and sponsored by AbbVie, Janssen, Pfizer, Roche and UCB. GR: received lecture fees from Abbvie, Janssen, Novartis, Pfizer, and UCB; advisory board from Abbvie, Janssen, and Novartis; Research support from Brazilian Society of Rheumatology, FAPEMIG and UCB; Clinical research payments from Abbvie and Pfizer; sponsorship for scientific events from Abbvie, Janssen, Lilly, Novartis, Pfizer, and UCB. SLER: speeches Abbvie e Novartis. OAM: speaker’s fees from Abbvie, Boehringer Ingelheim, GSK, Janssen, Novartis, Pfizer, UCB and Roche. GCSP: Speeches for Jansen, Novartis. ETRN: Speeches for Janssen e Apsen. MMP: Speeches for Abbvie, Novartis, Janssen, Lilly. Advisory board: Lilly, Novartis. CDLM: Personal or institutional support from Abbvie, Janssen, Novartis, Pfizer, UCB Speeches: Abbvie, Janssen, Novartis, UCB. The other authors have no conflict of interest to declare.

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Supplementary Information

Additional file 1.

Results of univariate logistic regression models - hospitalization in patients with rheumatoid arthritis.

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Gomides, A.P.M., de Albuquerque, C.P., da Mota, L.M.H. et al. Factors associated with hospitalizations for Covid-19 in patients with rheumatoid arthritis: data from the Reumacov Brazil registry. Adv Rheumatol 62, 13 (2022). https://doi.org/10.1186/s42358-022-00244-5

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  • DOI: https://doi.org/10.1186/s42358-022-00244-5

Keywords

  • COVID-19
  • Hospitalization
  • Immunosuppression
  • Outcomes
  • Rheumatoid arthritis

Advances in Rheumatology

ISSN: 2523-3106