SpringerLink
Log in

Breakthrough SARS-CoV-2 infection and disease flares in patients with rheumatoid arthritis: result from COVAD e-survey study

  • Observational Research
  • Published:
Rheumatology International Aims and scope Submit manuscript

Abstract

COVID-19 has been suggested as a possible trigger of disease flares in patients with rheumatoid arthritis (RA). However, factors associated with disease flares remain unknown. This study aimed to identify factors associated with breakthrough infection (BIs) and disease flares in patients with RA following COVID-19. We analysed data from RA patients who participated in the COVID-19 vaccination in autoimmune diseases (COVAD) study. Demographic data, patient-reported outcomes, comorbidities, pharmacologic treatment and details regarding disease flares were extracted from the COVAD database. Factors associated with disease flare-ups were determined by multivariate logistic regression analysis. The analysis comprised 1928 patients with RA who participated in the COVAD study. Younger age, Caucasian ethnicity, comorbidities with obstructive chronic pulmonary disease and asthma were associated with COVID-19 breakthrough infection. Moreover, younger age (odds ratio (OR): 0.98, 95% CI 0.96–0.99, p < 0.001), ethnicity other than Asian, past history of tuberculosis (OR: 3.80, 95% CI 1.12–12.94, p = 0.033), treatment with methotrexate (OR: 2.55, 95% CI: 1.56–4.17, p < 0.001), poor global physical health (OR: 1.07, 95% CI 1.00–1.15, p = 0.044) and mental health (OR: 0.91, 95% CI 0.87–0.95, p < 0.001) were independent factors associated disease flares in patients with RA. Our study highlights the impact of socio-demographic factors, clinical characteristics and mental health on disease flares in patients with RA. These insights may help determine relevant strategies to proactively manage RA patients at risk of flares.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

The datasets generated and/or analyzed during the current study are not publicly available but are available from the corresponding author upon reasonable request.

References

  1. Petrilli CM, Jones SA, Yang J, Rajagopalan H, O’Donnell L, Chernyak Y, Tobin KA, Cerfolio RJ, Francois F, Horwitz LI (2022) Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. BMJ 369:m1966. https://doi.org/10.1136/bmj.m1966.PMID:32444366;PMCID:PMC7243801

    Article  Google Scholar 

  2. Listing J, Gerhold K, Zink A (2013) The risk of infections associated with rheumatoid arthritis, with its comorbidity and treatment. Rheumatology (Oxford) 52(1):53–61. https://doi.org/10.1093/rheumatology/kes305

    Article  CAS  PubMed  Google Scholar 

  3. Conway R, Grimshaw AA, Konig MF, Putman M, Duarte-García A, Tseng LY, Cabrera DM, Chock YPE, Degirmenci HB, Duff E, Egeli BH, Graef ER, Gupta A, Harkins P, Hoyer BF, Jayatilleke A, ** S, Kasia C, Khilnani A, Kilian A, Kim AHJ, Lin CMA, Low C, Proulx L, Sattui SE, Singh N, Sparks JA, Tam H, Ugarte-Gil MF, Ung N, Wang K, Wise LM, Yang Z, Young KJ, Liew JW, Grainger R, Wallace ZS, Hsieh E, COVID-19 Global Rheumatology Alliance (2022) SARS-CoV-2 Infection and COVID-19 outcomes in rheumatic diseases: a systematic literature review and meta-analysis. Arthritis Rheumatol 74(5):766–775. https://doi.org/10.1002/art.42030

  4. Sun J, Zheng Q, Madhira V, Olex AL, Anzalone AJ, Vinson A, Singh JA, French E, Abraham AG, Mathew J, Safdar N, Agarwal G, Fitzgerald KC, Singh N, Topaloglu U, Chute CG, Mannon RB, Kirk GD, Patel RC, National COVID Cohort Collaborative (N3C) Consortium (2022) Association between immune dysfunction and COVID-19 breakthrough infection after SARS-CoV-2 vaccination in the US. JAMA Intern Med 182(2):153–162. https://doi.org/10.1001/jamainternmed.2021.7024

  5. Paik JJ, Sparks JA, Kim AHJ (2022) Immunogenicity, breakthrough infection, and underlying disease flare after SARS-CoV-2 vaccination among individuals with systemic autoimmune rheumatic diseases. Curr Opin Pharmacol 65:102243. https://doi.org/10.1016/j.coph.2022.102243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jena A, Mishra S, Deepak P, Kumar-M P, Sharma A, Patel YI, Kennedy NA, Kim AHJ, Sharma V, Sebastian S (2022) Response to SARS-CoV-2 vaccination in immune mediated inflammatory diseases: systematic review and meta-analysis. Autoimmun Rev 21(1):102927. https://doi.org/10.1016/j.autrev.2021.102927

    Article  CAS  PubMed  Google Scholar 

  7. Liew J, Gianfrancesco M, Harrison C et al (2022) SARS-CoV-2 breakthrough infections among vaccinated individuals with rheumatic disease: results from the COVID-19 global rheumatology alliance provider registry. RMD Open 8:e002187. https://doi.org/10.1136/rmdopen-2021-002187

    Article  PubMed  Google Scholar 

  8. Li H, Wallace ZS, Sparks JA, Lu N, Wei J, **e D, Wang Y, Zeng C, Lei G, Zhang Y (2023) Risk of COVID-19 among unvaccinated and vaccinated patients with rheumatoid arthritis: a general population study. Arthritis Care Res (Hoboken) 75(5):956–966. https://doi.org/10.1002/acr.25028

    Article  CAS  PubMed  Google Scholar 

  9. Torres-Aguilar H, Sosa-Luis SA, Aguilar-Ruiz SR (2019) Infections as triggers of flares in systemic autoimmune diseases: novel innate immunity mechanisms. Curr Opin Rheumatol 31(5):525–531. https://doi.org/10.1097/BOR.0000000000000630

    Article  CAS  PubMed  Google Scholar 

  10. Zheng Q, Lin R, Chen Y, Lv Q, Zhang J, Zhai J, Xu W, Wang W (2022) SARS-CoV-2 induces “cytokine storm” hyperinflammatory responses in RA patients through pyroptosis. Front Immunol 13:1058884. https://doi.org/10.3389/fimmu.2022.1058884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Pham A, Brook J, Elashoff DA, Ranganath VK (2022) Impact of perceived stress during the SARS-CoV-2 pandemic on rheumatoid arthritis patients’ disease activity: an online survey. J Clin Rheumatol 28(7):333–337. https://doi.org/10.1097/RHU.0000000000001861

    Article  PubMed  PubMed Central  Google Scholar 

  12. Fazal ZZ, Sen P, Joshi M, Ravichandran N, Lilleker JB, Agarwal V, et al. COVAD survey 2 long-term outcomes: unmet need and protocol. Rheumatol Int. 2022;42(12), 2151–2158, doi: 10.1007/s00296-022-05157-6

  13. Sun J, Zheng Q, Madhira V et al (2022) Association between immune dysfunction and COVID-19 breakthrough infection after SARS-CoV-2 vaccination in the US. JAMA Intern Med 182(2):153–162. https://doi.org/10.1001/jamainternmed.2021.7024

    Article  CAS  PubMed  Google Scholar 

  14. Schiff AE, Wang X, Patel NJ, Kawano Y, Kowalski EN, Cook CE, Vanni KMM, Qian G, Bade KJ, Saavedra AA, Srivatsan S, Williams ZK, Venkat RK, Wallace ZS, Sparks JA (2023) Immunomodulators and risk for breakthrough infection after third COVID-19 mRNA vaccine among patients with rheumatoid arthritis: a cohort study. medRxiv. https://doi.org/10.1101/2023.10.08.23296717

    Article  PubMed  PubMed Central  Google Scholar 

  15. Friedman MA, Curtis JR, Winthrop KL (2021) Impact of disease-modifying antirheumatic drugs on vaccine immunogenicity in patients with inflammatory rheumatic and musculoskeletal diseases. Ann Rheum Dis 80(10):1255–1265. https://doi.org/10.1136/annrheumdis-2021-221244

    Article  CAS  PubMed  Google Scholar 

  16. Patel NJ, Wang X, Fu X, Kawano Y, Cook C, Vanni KMM et al (2023) Factors associated with COVID-19 breakthrough infection among vaccinated patients with rheumatic diseases: a cohort study. Semin Arthritis Rheum 58:152108

    Article  CAS  PubMed  Google Scholar 

  17. Boekel L, Stalman EW, Wieske L et al (2022) Breakthrough SARS-CoV-2 infections with the delta (B.1.617.2) variant in vaccinated patients with immune-mediated inflammatory diseases using immunosuppressants: a sub study of two prospective cohort studies. Lancet Rheumatol 4:e417–e429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Yamal J, Appana S, Wang M, Bakota E, Ye Y, Sharma S, Morrison AC, Marko D, Linder SH, Rector A, Jetelina KK, Boerwinkle E (2022) Trends and correlates of breakthrough infections with SARS-CoV-2. Front Public Health 10:856532. https://doi.org/10.3389/fpubh.2022.856532

    Article  PubMed  PubMed Central  Google Scholar 

  19. Maza MD, Úbeda M, Delgado P, Horndler L, Llamas MA, Van Santen HM, Alarcón B, Abia D, Bastolla U, Fresno M (2022) ACE2 serum levels as predictor of infectability and outcome in COVID-19. Front Immunol 13:836516. https://doi.org/10.3389/fimmu.2022.836516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lamacchia C, Gilbert B, Studer O, Lauper K, Finckh A (2023) Brief report: Can COVID-19 infection trigger rheumatoid arthritis-associated autoimmunity in individuals at risk for the disease? A nested cohort study. Front Med 10:1201425. https://doi.org/10.3389/fmed.2023.1201425

    Article  Google Scholar 

  21. Fong W, Woon TH, Chew LC, Low A, Law A, Poh YJ, Yeo SI, Leung YY, Ma M, Santosa A, Kong KO, Xu C, Teng GG, Mak A, Tay SH, Chuah TY, Roslan NE, Angkodjojo S, Phang KF, Sriranganathan M, Tan TC, Cheung P, Lahiri M (2023) Prevalence and factors associated with flares following COVID-19 mRNA vaccination in patients with rheumatoid arthritis, psoriatic arthritis and spondyloarthritis: a national cohort study. Adv Rheumatol 63(1):38. https://doi.org/10.1186/s42358-023-00316-0

    Article  PubMed  Google Scholar 

  22. Terracina KA, Tan FK (2021) Flare of rheumatoid arthritis after COVID-19 vaccination. Lancet Rheumatol 3(7):e469–e470. https://doi.org/10.1016/S2665-9913(21)00108-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zavala-Flores E, Salcedo-Matienzo J, Quiroz-Alva A, Berrocal-Kasay A (2021) Side effects and flares risk after SARS-CoV-2 vaccination in patients with systemic lupus erythematosus. Clin Rheumatol 16:1–9. https://doi.org/10.1007/s10067-021-05980-5

    Article  Google Scholar 

  24. Cherian S, Paul A, Ahmed S, Alias B, Manoj M, Santhosh AK et al (2021) Safety of the ChAdOx1 Ncov-19 and the BBV152 vaccines in 724 patients with rheumatic diseases: a post-vaccination cross-sectional survey. Rheumatol Int 41(8):1441–1445. https://doi.org/10.1007/s00296-021-04917-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rotondo C, Cantatore FP, Fornaro M, Colia R, Busto G, Rella V et al (2021) Preliminary data on post market safety profiles of COVID 19 vaccines in rheumatic diseases: assessments on various vaccines in use, different rheumatic disease subtypes, and immunosuppressive therapies: a twocenters study. Vaccines (Basel) 9(7):730. https://doi.org/10.3390/vaccines9070730

    Article  CAS  PubMed  Google Scholar 

  26. **e Y, Liu Y, Liu Y (2022) The flare of rheumatic disease after SARS-CoV-2 vaccination: a review. Front Immunol 13:919979. https://doi.org/10.3389/fimmu.2022.919979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Fan Y, Geng Y, Wang Y, Deng X, Li G, Zhao J et al (2022) Safety and disease flare of autoimmune inflammatory rheumatic diseases: a large real-world survey on inactivated COVID-19 vaccines. Ann Rheum Dis 81(3):443–445. https://doi.org/10.1136/annrheumdis-2021-221736

    Article  CAS  PubMed  Google Scholar 

  28. Rider LG, Parks CG, Wilkerson J, Schiffenbauer AI, Kwok RK, Noroozi Farhadi P et al (2022) Baseline factors associated with self-reported disease flares following COVID-19 vaccination among adults with systemic rheumatic disease: results from the COVID-19 global rheumatology alliance vaccine survey. Rheumatol (Oxford) 23:keac249. https://doi.org/10.1093/rheumatology/keac249

    Article  Google Scholar 

  29. Connolly CM, Ruddy JA, Boyarsky BJ, Barbur I, Werbel WA, Geetha D et al (2022) Disease flare and reactogenicity in patients with rheumatic and musculoskeletal diseases following two-dose SARS-CoV-2 messenger RNA vaccination. Arthritis Rheumatol 74(1):28–32. https://doi.org/10.1002/art.41924

    Article  CAS  PubMed  Google Scholar 

  30. Naveen R, Sen P, Griger Z, Day J, Joshi M, Nune A, Nikiphorou E, Saha S, Tan AL, Shinjo SK, Ziade N, Velikova T, Milchert M, Jagtap K, Parodis I, Edgar Gracia-Ramos A, Cavagna L, Kuwana M, Knitza J, Chen YM, Makol A, Agarwal V, Patel A, Pauling JD, Wincup C, Barman B, Zamora Tehozol EA, Serrano JR, García-De La Torre I, Colunga-Pedraza IJ, Merayo-Chalico J, Chibuzo OC, Katchamart W, Goo PA, Shumnalieva R, Hoff LS, Kibbi EL, Halabi H, Vaidya B, Shaharir SS, Hasan ATMT, Dey D, Gutiérrez CET, Caballero-Uribe CV, Lilleker JB, Salim B, Gheita T, Chatterjee T, Distler O, Saavedra MA; COVAD study group Chinoy H, Agarwal V, Aggarwal R, Gupta L (2023) Flares in IIMs and the timeline following COVID-19 vaccination: a combined analysis of the COVAD-1 and 2 surveys. Rheumatology (Oxford). https://doi.org/10.1093/rheumatology/kead180

  31. Bauer ME (2020) Accelerated immunosenescence in rheumatoid arthritis: impact on clinical progression. Immun Ageing 17:6. https://doi.org/10.1186/s12979-020-00178-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Geng Y, Fan Y, Wang Y, Deng X, Ji L, Zhang X, Song Z, Huang H, Gui Y, Zhang H, Sun X, Li G, Zhao J, Zhang Z (2023) Flare and change in disease activity among patients with stable rheumatoid arthritis following coronavirus disease 2019 vaccination: a prospective Chinese cohort study. Chin Med J (Engl) 136(19):2324–2329. https://doi.org/10.1097/CM9.0000000000002562

    Article  PubMed  Google Scholar 

  33. Yılmaz V, Umay E, Gündoğdu İ, Karaahmet ZÖ, Öztürk AE (2017) Rheumatoid arthritis: are psychological factors effective in disease flare? Eur J Rheumatol 4(2):127–132. https://doi.org/10.5152/eurjrheum.2017.16100

    Article  PubMed  PubMed Central  Google Scholar 

  34. Furst D, Morris NT, Pham AQ et al (2022) POS0609 stress-associated increases in rheumatoid arthritis disease activity and flares during the covid-19 pandemic. Ann Rheum Dis 81:573–574

    Article  Google Scholar 

  35. Hsieh E, Dey D, Grainger R, Li M, Machado PM, Ugarte-Gil MF, Yazdany J (2023) Global perspective on the impact of the COVID-19 pandemic on rheumatology and health equity. Arthritis Care Res (Hoboken). https://doi.org/10.1002/acr.25169

    Article  PubMed  Google Scholar 

  36. Hua C, Barnetche T, Combe B, Morel J (2014) Effect of methotrexate, anti–tumor necrosis factor α, and rituximab on the immune response to influenza and pneumococcal vaccines in patients with rheumatoid arthritis: a systematic review and meta-analysis. Arthritis Care Res 66(7):1016–1026

    Article  CAS  Google Scholar 

  37. Al-Haideri MT, Mannani R, Kaboli R, Gharebakhshi F, Darvishzadehdeldari S, Tahmasebi S, Faramarzi F, Cotrina-Aliaga JC, Khorasani S, Alimohammadi M, Darvishi M, Akhavan-Sigari R (2023) The effects of methotrexate on the immune responses to the COVID-19 vaccines in the patients with immune-mediated inflammatory disease: a systematic review of clinical evidence. Transpl Immunol 79:101858. https://doi.org/10.1016/j.trim.2023.101858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sieiro Santos C, Calleja Antolin S, Moriano Morales C et al (2022) Immune responses to mRNA vaccines against SARS-CoV-2 in patients with immune-mediated inflammatory rheumatic diseases. RMD Open 8:e001898. https://doi.org/10.1136/rmdopen-2021-001898

    Article  PubMed  Google Scholar 

  39. Curtis JR, Johnson SR, Anthony DD, Arasaratnam RJ, Baden LR, Bass AR, Calabrese C, Gravallese EM, Harpaz R, Kroger A, Sadun RE, Turner AS, Williams EA, Mikuls TR (2023) American College of Rheumatology Guidance for COVID-19 vaccination in patients with rheumatic and musculoskeletal diseases: version 5. Arthritis Rheumatol 75(1):E1–E16. https://doi.org/10.1002/art.42372

    Article  PubMed  Google Scholar 

  40. Sen P, Gupta L, Lilleker JB et al (2022) COVID-19 vaccination in autoimmune disease (COVAD) survey protocol. Rheumatol Int 42:23–29. https://doi.org/10.1007/s00296-021-05046-4

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to all respondents for completing the questionnaire. The authors also thank the Myositis Association, Myositis India, Myositis UK, Myositis Support and Understanding, the Myositis Global Network, Deutsche Gesellschaft für Muskelkranke e.V. (DGM), Dutch and Swedish Myositis patient support groups, Cure JM, Cure IBM, Sjögren’s India Foundation, Patients Engage, Scleroderma India, Lupus UK, Lupus Sweden, Emirates Arthritis Foundation, EULAR PARE, ArLAR research group, AAAA patient group, Myositis Association of Australia, APLAR myositis special interest group, Thai Rheumatism association, PANLAR, AFLAR NRAS, Anti-Synthetase Syndrome support group, and various other patient support groups and organizations for their contribution to the dissemination of this survey. Finally, the authors wish to thank all members of the COVAD study group for their invaluable role in the data collection.

Funding

This research was supported by the NIHR Manchester Biomedical Research Centre (NIHR203308) and the National Science and Technology Council, Taiwan (NSTC 111-2314-B-005-007-MY3).

Author information

Author notes

  1. Vikas Agarwal and Yi-Ming Chen co-senior authors.

Authors and Affiliations

  1. Rheumatologist at Complejo Asistencial Universitario de León, Castilla and Leon, Spain

    Cristiana Sieiro Santos

  2. Department of Medical Research, Taichung Veterans General Hospital, Taichung City, Taiwan

    Jun-Peng Chen & Yi-Ming Chen

  3. Centre for Rheumatic Diseases, King’s College London, London, UK

    Elena Nikiphorou

  4. Rheumatology Department, King’s College Hospital, London, UK

    Elena Nikiphorou

  5. Division of Allergy, Immunology and Rheumatology, Department of Medical Research, Department of Internal Medicine, Taichung Veterans General Hospital, Taichung City, Taiwan

    Chi-Wei Tseng & Yi-Ming Chen

  6. Reference Center for Osteoporosis, Rheumatology and Dermatology, Pontifica Universidad Javeriana Cali, Cali, Colombia

    Carlos Enrique Toro Gutiérrez

  7. NIHR Leeds Biomedical Research Centre, Leeds Teaching Hospitals Trust, Leeds, UK

    Ai Lyn Tan

  8. Leeds Institute of Rheumatic and Musculoskeletal Medicine, University of Leeds, Leeds, UK

    Ai Lyn Tan

  9. Southport and Ormskirk Hospital NHS Trust, Southport, PR8 6PN, UK

    Arvind Nune

  10. Seth Gordhandhas Sunderdas Medical College and King Edwards Memorial Hospital, Mumbai, Maharashtra, India

    Esha Kadam

  11. Department of Allergy and Rheumatology, Nippon Medical School Graduate School of Medicine, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8602, Japan

    Masataka Kuwana

  12. Department of Rheumatology, Royal Melbourne Hospital, Parkville, VIC, 3050, Australia

    Jessica Day

  13. Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, 3052, Australia

    Jessica Day

  14. Department of Medical Biology, University of Melbourne, Parkville, VIC, 3052, Australia

    Jessica Day

  15. Mymensingh Medical College, Mymensingh, Bangladesh

    Sreoshy Saha

  16. Medical Faculty, Sofia University St. Kliment Ohridski, 1 Kozyak Str., 1407, Sofia, Bulgaria

    Tsvetelina Velikova

  17. Division of Musculoskeletal and Dermatological Sciences, Centre for Musculoskeletal Research, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre The University of Manchester, Manchester, UK

    James B. Lilleker, Hector Chinoy & Latika Gupta

  18. Manchester Centre for Clinical Neurosciences, Salford Royal NHS Foundation Trust, Salford, UK

    James B. Lilleker

  19. Department of Medicine, Hospital Universidad del Norte, Barranquilla, Atlantico, Colombia

    Carlo V. Caballero-Uribe

  20. Maulana Azad Medical College, 2-Bahadurshah Zafar Marg, New Delhi, Delhi, 110002, India

    Parikshit Sen

  21. National Institute for Health Research Manchester Biomedical Research Centre, Manchester University NHS Foundation Trust, The University of Manchester, Manchester, UK

    Hector Chinoy

  22. Department of Rheumatology, Salford Royal Hospital, Northern Care Alliance NHS Foundation Trust, Salford, UK

    Hector Chinoy

  23. Division of Rheumatology and Clinical Immunology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA

    Rohit Aggarwal

  24. Department of Clinical Immunology and Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India

    Vikas Agarwal

  25. Department of Rheumatology, Royal Wolverhampton Hospitals NHS Trust, Wolverhampton, UK

    Latika Gupta

  26. Department of Rheumatology, City Hospital, Sandwell and West Birmingham Hospitals NHS Trust, Birmingham, UK

    Latika Gupta

  27. Division of Allergy, Immunology and Rheumatology, Department of Medical Research, Taichung Veterans General Hospital, Taichung City, Taiwan

    Yi-Ming Chen

  28. Department of Post-Baccalaureate Medicine, College of Medicine, National Chung-Hsing University, Taichung City, Taiwan

    Yi-Ming Chen

  29. Precision Medicine Research Center, College of Medicine, National Chung Hsing University, Taichung City, Taiwan

    Yi-Ming Chen

  30. School of Medicine, National Yang-Ming Chiao Tung University, Taipei, Taiwan

    Yi-Ming Chen

Authors
  1. Cristiana Sieiro Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun-Peng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elena Nikiphorou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chi-Wei Tseng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carlos Enrique Toro Gutiérrez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ai Lyn Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Arvind Nune
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Esha Kadam
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Masataka Kuwana
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jessica Day
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Sreoshy Saha
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Tsvetelina Velikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. James B. Lilleker
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Carlo V. Caballero-Uribe
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Parikshit Sen
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Hector Chinoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Rohit Aggarwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Vikas Agarwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Latika Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Yi-Ming Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

COVAD study group

  • Mahnoor Javaid
  • , Naitica Darooka
  • , Samuel Katsuyuki Shinjo
  • , Ioannis Parodis
  • , Abraham Edgar Gracia-Ramos
  • , Johannes Knitza
  • , Aarat Patel
  • , Chris Wincup
  • , Bhupen Barman
  • , Erick Adrian Zamora Tehozol
  • , Jorge Rojas Serrano
  • , Ignacio García-De La Torre
  • , Iris J. Colunga-Pedraza
  • , Javier Merayo-Chalico
  • , Okwara Celestine Chibuzo
  • , Russka Shumnalieva
  • , Leonardo Santos Hoff
  • , Lina El Kibbi
  • , Hussein Halabi
  • , Binit Vaidya
  • , ATMTanveer Hasan
  • , Babur Salim
  • , Tamer Gheita
  • , Miguel A. Saavedra
  • , Sinan Kardes
  • , Laura Andreoli
  • , Daniele Lini
  • , Karen Schreiber
  • , Melinda Nagy Vince
  • , Yogesh Preet Singh
  • , Rajiv Ranjan
  • , Avinash Jain
  • , Sapan C. Pandya
  • , Rakesh Kumar Pilania
  • , Aman Sharma
  • , MManesh Manoj
  • , Vikas Gupta
  • , Chengappa G. Kavadichanda
  • , Pradeepta Sekhar Patro
  • , Sajal Ajmani
  • , Sanat Phatak
  • , Rudra Prosad Goswami
  • , Abhra Chandra Chowdhury
  • , Ashish Jacob Mathew
  • , Padnamabha Shenoy
  • , Ajay Asranna
  • , Keerthi Talari Bommakanti
  • , Anuj Shukla
  • , Arunkumar R. Pande
  • , Kunal Chandwar
  • , Akanksha Ghodke
  • , Hiya Boro
  • , Zoha Zahid Fazal
  • , Döndü Üsküdar Cansu
  • , Reşit Yıldırım
  • , Armen Yuri Gasparyan
  • , Nicoletta Del Papa
  • , Gianluca Sambataro
  • , Atzeni Fabiola
  • , Marcello Govoni
  • , Simone Parisi
  • , Elena Bartoloni Bocci
  • , Gian Domenico Sebastiani
  • , Enrico Fusaro
  • , Marco Sebastiani
  • , Luca Quartuccio
  • , Franco Franceschini
  • , Pier Paolo Sainaghi
  • , Giovanni Orsolini
  • , Rossella De Angelis
  • , Maria Giovanna Danielli
  • , Vincenzo Venerito
  • , Silvia Grignaschi
  • , Alessandro Giollo
  • , Alessia Alluno
  • , Florenzo Ioannone
  • , Marco Fornaro
  • , Lisa S. Traboco
  • , Suryo Anggoro Kusumo Wibowo
  • , Jesús Loarce-Martos
  • , Sergio Prieto-González
  • , Raquel Aranega Gonzalez
  • , Ran Nakashima
  • , Shinji Sato
  • , Naoki Kimura
  • , Yuko Kaneko
  • , Takahisa Gono
  • , Stylianos Tomaras
  • , Fabian Nikolai Proft
  • , Marie-Therese Holzer
  • , Margarita Aleksandrovna Gromova
  • , Or Aharonov
  • , Zoltán Griger
  • , Ihsane Hmamouchi
  • , Imane El bouchti
  • , Zineb Baba
  • , Margherita Giannini
  • , François Maurier
  • , Julien Campagne
  • , Alain Meyer
  • , Daman Langguth
  • , Vidya Limaye
  • , Merrilee Needham
  • , Nilesh Srivastav
  • , Marie Hudson
  • , Océane Landon-Cardinal
  • , Wilmer Gerardo Rojas Zuleta
  • , Álvaro Arbeláez
  • , Javier Cajas
  • , José António Pereira Silva
  • , João Eurico Fonseca
  • , Olena Zimba
  • , Uyi Ima-Edomwonyi
  • , Ibukunoluwa Dedeke
  • , Emorinken Airenakho
  • , Nwankwo Henry Madu
  • , Abubakar Yerima
  • , Hakeem Olaosebikan
  • , A. Becky
  • , Oruma Devi Koussougbo
  • , Elisa Palalane
  • , Ho So
  • , Manuel Francisco Ugarte-Gil
  • , Lyn Chinchay
  • , José Proaño Bernaola
  • , Victorio Pimentel
  • , Hanan Mohammed Fathi
  • , Reem Hamdy A. Mohammed
  • , Ghita Harifi
  • , Yurilís Fuentes-Silva
  • , Karoll Cabriza
  • , Jonathan Losanto
  • , Nelly Colaman
  • , Antonio Cachafeiro-Vilar
  • , Generoso Guerra Bautista
  • , Enrique Julio Giraldo Ho
  • , Lilith Stange Nunez
  • , MCristian Vergara
  • , Jossiell Then Báez
  • , Hugo Alonzo
  • , Carlos Benito Santiago Pastelin
  • , Rodrigo García Salinas
  • , Alejandro Quiñónez Obiols
  • , Nilmo Chávez
  • , Andrea Bran Ordóñez
  • , Gil Alberto Reyes Llerena
  • , Radames Sierra-Zorita
  • , Dina Arrieta
  • , Eduardo Romero Hidalgo
  • , Ricardo Saenz
  • , MIdania Escalante
  • , Wendy Calapaqui
  • , Ivonne Quezada
  • , Gabriela Arredondo
  • , Akira Yoshida
  • , Keina Yomono
  • , John D. Pauling
  • , Ashima Makol
  • , Tulika Chatterjee
  • , Wanruchada Katchamart
  • , Phonpen Akarawatcharangura Goo
  • , Dzifa Dey
  • , Lorenzo Cavagna
  • , Marcin Milchert
  • , Nelly Ziade
  •  & Oliver Distler

Contributions

Conceptualization: LG, VA, YMC and CSS. Data curation: All authors. Formal analysis: YMC; Funding acquisition: N/A. Investigation: YMC, VA, LG. Methodology: YMC, LG, VA; Software: LG. Validation: VA, RA, JBL, and HC. Visualization: CSS, YMC, VA and LG. Writing-original draft: CSS, YMC, VA and LG. Writing-review and editing: all authors.

Corresponding author

Correspondence to Yi-Ming Chen.

Ethics declarations

Conflict of interest

ALT has received honoraria for advisory boards and speaking for Abbvie, Gilead, Janssen, Lilly, Novartis, Pfizer, and UCB. EN has received speaker honoraria/participated in advisory boards for Celltrion, Pfizer, Sanofi, Gilead, Galapagos, AbbVie, and Lilly, and holds research grants from Pfizer and Lilly. HC has received grant support from Eli Lilly and UCB, consulting fees from Novartis, Eli Lilly, Orphazyme, Astra Zeneca, speaker for UCB, and Biogen. JBL has received speaker honoraria/participated in advisory boards for Sanofi Genzyme, Roche, and Biogen. None is related to this manuscript. JD has received research funding from CSL Limited. RA has a consultancy relationship with and/or has received research funding from the following companies: Bristol Myers-Squibb, Pfizer, Genentech, Octapharma, CSL Behring, Mallinckrodt, AstraZeneca, Corbus, Kezar, Abbvie, Janssen, Kyverna Alexion, Argenx, Q32, EMD-Serono, Boehringer Ingelheim, Roivant, Merck, Galapagos, Actigraph, Scipher, Horizon Therepeutics, Teva, Beigene, ANI Pharmaceuticals, Biogen, Nuvig, Capella Bioscience, and CabalettaBio. TV has received speaker honoraria from Pfizer and AstraZeneca, non-related to the current manuscript. Rest of the authors have no conflict of interest relevant to this manuscript.

Consent for publication

No part of this manuscript has been copied or published elsewhere either in whole or in part.

Ethical approval

Ethical approval was obtained from the Institutional Ethics Committee of the Sanjay Gandhi Postgraduate Institute of Medical Sciences, Raebareli Road, Lucknow, 226014.

Human or animal rights

It was not appropriate or possible to involve patients or the public in the design, or conduct, or reporting, or dissemination plans of our research.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 41 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santos, C.S., Chen, JP., Nikiphorou, E. et al. Breakthrough SARS-CoV-2 infection and disease flares in patients with rheumatoid arthritis: result from COVAD e-survey study. Rheumatol Int 44, 805–817 (2024). https://doi.org/10.1007/s00296-024-05542-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00296-024-05542-3

Keywords

Search

Navigation