1887
  1. Home
  2. Eurosurveillance
  3. Volume 28, Issue 13, 30/Mar/2023
  4. Article
Surveillance Open Access
Like 0
Download

Abstract

Background

Understanding the epidemiology of reinfections is crucial for SARS-CoV-2 control over a long period.

Aim

To evaluate the risk of SARS-CoV-2 reinfection by vaccination status, predominant variant and time after first infection.

Methods

We conducted a cohort study including all residents in the Reggio Emilia province on 31 December 2019, followed up until 28 February 2022 for SARS-CoV-2 first infection and reinfection after 90 days. Cox models were used to compare risk of first infection vs reinfection, adjusting for age, sex, vaccine doses and comorbidities.

Results

The cohort included 538,516 residents, 121,154 with first SARS-CoV-2 infections and 3,739 reinfections, most in the Omicron BA.1 period. In the pre-Omicron period, three doses of vaccine reduced risk of reinfection by 89% (95% CI: 87–90), prior infection reduced risk by 90% (95% CI: 88–91), while two doses and infection reduced risk by 98% (95% CI: 96–99). In the Omicron BA.1 period, protection estimates were 53% (95% CI: 52–55), 9% (95% CI: 4–14) and 76% (95% CI: 74–77). Before Omicron, protection from reinfection remained above 80% for up to 15 months; with Omicron BA.1, protection decreased from 71% (95% CI: 65–76) at 5 months to 21% (95% CI: 10–30) at 22 months from the first infection. Omicron BA.1 reinfections showed 48% (95% CI: 10–57) lower risk of severe disease than first infections.

Conclusions

Natural immunity acquired with previous variants showed low protection against Omicron BA.1. Combined vaccination and natural immunity seems to be more protective against reinfection than either alone. Vaccination of people with prior infection reduced the risk of severe disease.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.13.2200494
2023-03-30
2024-12-26
/content/10.2807/1560-7917.ES.2023.28.13.2200494
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/13/eurosurv-28-13-1.html?itemId=/content/10.2807/1560-7917.ES.2023.28.13.2200494&mimeType=html&fmt=ahah

References

  1. Dong E, Du H, Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis. 2020;20(5):533-4.  https://doi.org/10.1016/S1473-3099(20)30120-1  PMID: 32087114 
  2. Nachmias V, Fusman R, Mann S, Koren G. The first case of documented Covid-19 reinfection in Israel. IDCases. 2020;22:e00970.  https://doi.org/10.1016/j.idcr.2020.e00970  PMID: 33029476 
  3. European Centre for Disease Prevention and Control (ECDC). Reinfection with SARS-CoV: considerations for public health response. Stockholm: ECDC; 2020. Available at: https://www.ecdc.europa.eu/en/publications-data/threat-assessment-brief-reinfection-sars-cov-2
  4. Flacco ME, Soldato G, Acuti Martellucci C, Di Martino G, Carota R, Caponetti A, et al. Risk of SARS-CoV-2 reinfection 18 months after primary infection: population-level observational study. Front Public Health. 2022;10:884121.  https://doi.org/10.3389/fpubh.2022.884121  PMID: 35586006 
  5. Sacco C, Petrone D, Del Manso M, Mateo-Urdiales A, Fabiani M, Bressi M, et al. Risk and protective factors for SARS-CoV-2 reinfections, surveillance data, Italy, August 2021 to March 2022. Euro Surveill. 2022;27(20):2200372.  https://doi.org/10.2807/1560-7917.ES.2022.27.20.2200372  PMID: 35593164 
  6. Lumley SF, O’Donnell D, Stoesser NE, Matthews PC, Howarth A, Hatch SB, et al. Antibody status and incidence of SARS-CoV-2 infection in health care workers. N Engl J Med. 2021;384(6):533-40.  https://doi.org/10.1056/NEJMoa2034545  PMID: 33369366 
  7. Helfand M, Fiordalisi C, Wiedrick J, Ramsey KL, Armstrong C, Gean E, et al. Risk for reinfection after SARS-CoV-2: a living, rapid review for American College of Physicians practice points on the role of the antibody response in conferring immunity following SARS-CoV-2 infection. Ann Intern Med. 2022;175(4):547-55.  https://doi.org/10.7326/M21-4245  PMID: 35073157 
  8. Pilz S, Theiler-Schwetz V, Trummer C, Krause R, Ioannidis JPA. SARS-CoV-2 reinfections: Overview of efficacy and duration of natural and hybrid immunity. Environ Res. 2022;209:112911.  https://doi.org/10.1016/j.envres.2022.112911  PMID: 35149106 
  9. Hall V, Foulkes S, Insalata F, Kirwan P, Saei A, Atti A, et al. Protection against SARS-CoV-2 after Covid-19 Vaccination and Previous Infection. N Engl J Med. 2022;386(13):1207-20.  https://doi.org/10.1056/NEJMoa2118691  PMID: 35172051 
  10. Nordström P, Ballin M, Nordström A. Risk of SARS-CoV-2 reinfection and COVID-19 hospitalisation in individuals with natural and hybrid immunity: a retrospective, total population cohort study in Sweden. Lancet Infect Dis. 2022;22(6):781-90.  https://doi.org/10.1016/S1473-3099(22)00143-8  PMID: 35366962 
  11. Hansen CH, Michlmayr D, Gubbels SM, Mølbak K, Ethelberg S. Assessment of protection against reinfection with SARS-CoV-2 among 4 million PCR-tested individuals in Denmark in 2020: a population-level observational study. Lancet. 2021;397(10280):1204-12.  https://doi.org/10.1016/S0140-6736(21)00575-4  PMID: 33743221 
  12. United Kingdom Health Security Agency (UKHSA). SARS-CoV-2 variants of concern and variants under investigation in England: Technical briefing 34. London: UKHSA; 2022. Available at: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/1050236/technical-briefing-34-14-january-2022.pdf
  13. Ferguson N, Ghani A, Cori A, Hogan A, Hinsley W, Volz E. Report 49: Growth, population distribution and immune escape of Omicron in England. London: Imperial College London; 2021. Available at: https://www.imperial.ac.uk/media/imperial-college/medicine/mrc-gida/2021-12-16-COVID19-Report-49.pdf
  14. Bobrovitz N, Ware H, Ma X, et al. Protective effectiveness of previous SARS-CoV-2 infection and hybrid immunity against the omicron variant and severe disease: a systematic review and meta-regression. Lancet Infect Dis. 2023;S1473-3099(22)00801-5. doi: 10.1016/S1473-3099(22)00801-5. Epub ahead of print. PMID: 36681084
  15. Riccardo F, Ajelli M, Andrianou XD, Bella A, Del Manso M, Fabiani M, et al. Epidemiological characteristics of COVID-19 cases and estimates of the reproductive numbers 1 month into the epidemic, Italy, 28 January to 31 March 2020. Euro Surveill. 2020;25(49):2000790.  https://doi.org/10.2807/1560-7917.ES.2020.25.49.2000790  PMID: 33303064 
  16. Task force COVID-19 del Dipartimento Malattie Infettive e Servizio di Informatica. Report Esteso ISS. COVID-19: Sorveglianza, impatto delle infezioni ed efficacia vaccinale. [Extended Report ISS. COVID-19: Surveillance, impact of infections and vaccination effectiveness]. Rome: Istituto Superiore di Sanità; 2022. Available at: https://www.epicentro.iss.it/coronavirus/bollettino/Bollettino-sorveglianza-integrata-COVID-19_2-marzo-2022.pdf
  17. Mangone L, Gioia F, Mancuso P, Bisceglia I, Ottone M, Vicentini M, et al. Cumulative COVID-19 incidence, mortality and prognosis in cancer survivors: A population-based study in Reggio Emilia, Northern Italy. Int J Cancer. 2021;149(4):820-6.  https://doi.org/10.1002/ijc.33601  PMID: 33861870 
  18. European Centre for Disease Prevention and Control. Reinfection with SARS-CoV-2: implementation of a surveillance case definition within the EU/EEA. ECDC: Stockholm, 2021. Available at: https://www.ecdc.europa.eu/en/publications-data/reinfection-sars-cov-2-implementation-surveillance-case-definition-within-eueea
  19. Italian Ministry of Health. Nota ministeriale n. 0037911 20/08/2021. Rome: Ministero della Salute; 2021. Available from: https://www.seremi.it/sites/default/files/GR3917-000127.pdf
  20. Mancuso P, Venturelli F, Vicentini M, Perilli C, Larosa E, Bisaccia E, et al. Temporal profile and determinants of viral shedding and of viral clearance confirmation on nasopharyngeal swabs from SARS-CoV-2-positive subjects: a population-based prospective cohort study in Reggio Emilia, Italy. BMJ Open. 2020;10(8):e040380.  https://doi.org/10.1136/bmjopen-2020-040380  PMID: 32878768 
  21. Italian National Institute of Health. Rapporto ISS COVID-19 n. 49/2020. Rome: Istituto Superiore di Sanità; 2020. Available from: https://www.istat.it/it/files/2020/06/Rapporto-ISS-Istat-cause-di-morte-COVID-19-49_2020.pdf
  22. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373-83.  https://doi.org/10.1016/0021-9681(87)90171-8  PMID: 3558716 
  23. Kojima N, Klausner JD. Protective immunity after recovery from SARS-CoV-2 infection. Lancet Infect Dis. 2022;22(1):12-4.  https://doi.org/10.1016/S1473-3099(21)00676-9  PMID: 34762853 
  24. Official Gazzette of Italian Republic. D.L. 23 July 2021, n. 105. Misure urgenti per fronteggiare l'emergenza epidemiologica da COVID-19 e per l'esercizio in sicurezza di attivita' sociali ed economiche. [Urgent measures to deal with the epidemiological emergency from COVID-19 and for the safe exercise of social and economic activities.] Rome: Italian government. [Accessed: 13 Jun 2022]. Italian. Available from: https://www.gazzettaufficiale.it/eli/id/2021/07/23/21G00117/sg
  25. Official Gazzette of Italian Republic. Decree of the president of the council of ministers 12 October 2021. Adoption of the guidelines on the conduct of public administrations for the application of the regulations on the obligation to possess and exhibit the COVID-19 green certification by personnel. Rome: Italian government. [Accessed: 15 Jun 2022]. Italian. Available at: https://www.gazzettaufficiale.it/eli/id/2021/10/14/21A06125/sg
  26. Kahn F, Bonander C, Moghaddassi M, Rasmussen M, Malmqvist U, Inghammar M, et al. Risk of severe COVID-19 from the Delta and Omicron variants in relation to vaccination status, sex, age and comorbidities - surveillance results from southern Sweden, July 2021 to January 2022. Euro Surveill. 2022;27(9):2200121.  https://doi.org/10.2807/1560-7917.ES.2022.27.9.2200121  PMID: 35241215 
  27. Crotty S. Hybrid immunity. Science. 2021;372(6549):1392-3.  https://doi.org/10.1126/science.abj2258 
  28. Stamatatos L, Czartoski J, Wan YH, Homad LJ, Rubin V, Glantz H, et al. mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection. Science. 2021;372(6549):1413-8.  https://doi.org/10.1126/science.abg9175  PMID: 33766944 
  29. Reynolds CJ, Pade C, Gibbons JM, Butler DK, Otter AD, Menacho K, et al. Prior SARS-CoV-2 infection rescues B and T cell responses to variants after first vaccine dose. Science. 2021;372(6549):1418-23.  https://doi.org/10.1126/science.abh1282  PMID: 33931567 
  30. Rodda LB, Morawski PA, Pruner KB, Fahning ML, Howard CA, Franko N, et al. Imprinted SARS-CoV-2-specific memory lymphocytes define hybrid immunity. Cell. 2022;185(9):1588-1601.e14.  https://doi.org/10.1016/j.cell.2022.03.018  PMID: 35413241 
  31. Minervina AA, Pogorelyy MV, Kirk AM, Crawford JC, Allen EK, Chou CH, et al. SARS-CoV-2 antigen exposure history shapes phenotypes and specificity of memory CD8+ T cells. Nat Immunol. 2022;23(5):781-90.  https://doi.org/10.1038/s41590-022-01184-4  PMID: 35383307 
Risk of SARS-CoV-2 reinfection by vaccination status, predominant variant and time from prior infection: a cohort study, Reggio Emilia province, Italy, February 2020 to February 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Massimo+Vicentini&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Vicentini Massimo</a>, <a href="/search?value1=Francesco+Venturelli&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Venturelli Francesco</a>, <a href="/search?value1=Pamela+Mancuso&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mancuso Pamela</a>, <a href="/search?value1=Eufemia+Bisaccia&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bisaccia Eufemia</a>, <a href="/search?value1=Alessandro+Zerbini&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zerbini Alessandro</a>, <a href="/search?value1=Marco+Massari&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Massari Marco</a>, <a href="/search?value1=Andrea+Cossarizza&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cossarizza Andrea</a>, <a href="/search?value1=Sara+De+Biasi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">De Biasi Sara</a>, <a href="/search?value1=Patrizio+Pezzotti&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pezzotti Patrizio</a>, <a href="/search?value1=Emanuela+Bedeschi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bedeschi Emanuela</a>, <a href="/search?value1=Paolo+Giorgi+Rossi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Giorgi Rossi Paolo</a>, <a href="/search?value1=Reggio+Emilia+COVID-19+Working+Group&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Reggio Emilia COVID-19 Working Group</a></span>. Risk of SARS-CoV-2 reinfection by vaccination status, predominant variant and time from prior infection: a cohort study, Reggio Emilia province, Italy, February 2020 to February 2022. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(13):pii=2200494. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.13.2200494" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.13.2200494</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 13 Jun 2022;&nbsp;&nbsp; <span class="generated">Accepted</span>: 10 Jan 2023 </span> </p>
/content/10.2807/1560-7917.ES.2023.28.13.2200494
/content/10.2807/1560-7917.ES.2023.28.13.2200494
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error