Low Risk of SARS-CoV-2 Reinfection for Fully or Boosted mRNA Vaccinated Subjects in Sicily: A Population-Based Study Using Real-World Data
Abstract
:1. Introduction
2. Materials and Methods
2.1. Eligibility Criteria
2.2. Methods
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hu, T.; Liu, Y.; Zhao, M.; Zhuang, Q.; Xu, L.; He, Q. A Comparison of COVID-19, SARS and MERS. PeerJ 2020, 8, e9725. [Google Scholar] [CrossRef] [PubMed]
- Zhu, N.; Zhang, D.; Wang, W.; Li, X.; Yang, B.; Song, J.; Zhao, X.; Huang, B.; Shi, W.; Lu, R.; et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. N. Engl. J. Med. 2020, 382, 727–733. [Google Scholar] [CrossRef] [PubMed]
- WHO Coronavirus (COVID-19) Dashboard. Available online: https://covid19.who.int (accessed on 13 November 2022).
- Graña, C.; Ghosn, L.; Evrenoglou, T.; Jarde, A.; Minozzi, S.; Bergman, H.; Buckley, B.S.; Probyn, K.; Villanueva, G.; Henschke, N.; et al. Efficacy and Safety of COVID-19 Vaccines. Cochrane Database Syst. Rev. 2022, 12, CD015477. [Google Scholar] [CrossRef] [PubMed]
- Amodio, E.; Genovese, D.; Mazzeo, L.; Martino, L.; Restivo, V.; Vella, G.; Calamusa, G.; Vitale, F. Effectiveness of mRNA COVID-19 Vaccines in Adolescents Over 6 Months. Pediatrics 2022, 150, e2022057394. [Google Scholar] [CrossRef] [PubMed]
- Prunas, O.; Weinberger, D.M.; Pitzer, V.E.; Gazit, S.; Patalon, T. Waning Effectiveness of the BNT162b2 Vaccine Against Infection in Adolescents. medRxiv 2022. [Google Scholar] [CrossRef]
- Tartof, S.Y.; Slezak, J.M.; Fischer, H.; Hong, V.; Ackerson, B.K.; Ranasinghe, O.N.; Frankland, T.B.; Ogun, O.A.; Zamparo, J.M.; Gray, S.; et al. Effectiveness of mRNA BNT162b2 COVID-19 Vaccine up to 6 Months in a Large Integrated Health System in the USA: A Retrospective Cohort Study. Lancet 2021, 398, 1407–1416. [Google Scholar] [CrossRef] [PubMed]
- Andrews, N.; Tessier, E.; Stowe, J.; Gower, C.; Kirsebom, F.; Simmons, R.; Gallagher, E.; Thelwall, S.; Groves, N.; Dabrera, G.; et al. Duration of Protection against Mild and Severe Disease by COVID-19 Vaccines. N. Engl. J. Med. 2022, 386, 340–350. [Google Scholar] [CrossRef]
- Olson, S.M.; Newhams, M.M.; Halasa, N.B.; Price, A.M.; Boom, J.A.; Sahni, L.C.; Pannaraj, P.S.; Irby, K.; Walker, T.C.; Schwartz, S.P.; et al. Effectiveness of BNT162b2 Vaccine against Critical Covid-19 in Adolescents. N. Engl. J. Med. 2022, 386, 713–723. [Google Scholar] [CrossRef]
- Tenforde, M.W.; Self, W.H.; Naioti, E.A.; Ginde, A.A.; Douin, D.J.; Olson, S.M.; Talbot, H.K.; Casey, J.D.; Mohr, N.M.; Zepeski, A.; et al. Sustained Effectiveness of Pfizer-BioNTech and Moderna Vaccines Against COVID-19 Associated Hospitalizations Among Adults—United States, March-July 2021. Morb. Mortal. Wkly. Rep. 2021, 70, 1156–1162. [Google Scholar] [CrossRef]
- Amicone, M.; Borges, V.; Alves, M.J.; Isidro, J.; Zé-Zé, L.; Duarte, S.; Vieira, L.; Guiomar, R.; Gomes, J.P.; Gordo, I. Mutation Rate of SARS-CoV-2 and Emergence of Mutators during Experimental Evolution. Evol. Med. Public Health 2022, 10, 142–155. [Google Scholar] [CrossRef]
- Wang, Z.; Schmidt, F.; Weisblum, Y.; Muecksch, F.; Barnes, C.O.; Finkin, S.; Schaefer-Babajew, D.; Cipolla, M.; Gaebler, C.; Lieberman, J.A.; et al. mRNA Vaccine-Elicited Antibodies to SARS-CoV-2 and Circulating Variants. Nature 2021, 592, 616–622. [Google Scholar] [CrossRef] [PubMed]
- Gaudreault, N.N.; Carossino, M.; Morozov, I.; Trujillo, J.D.; Meekins, D.A.; Madden, D.W.; Cool, K.; Artiaga, B.L.; McDowell, C.; Bold, D.; et al. Experimental Re-Infected Cats Do Not Transmit SARS-CoV-2. Emerg. Microbes Infect. 2021, 10, 638–650. [Google Scholar] [CrossRef] [PubMed]
- Brustolin, M.; Rodon, J.; Rodríguez de la Concepción, M.L.; Ávila-Nieto, C.; Cantero, G.; Pérez, M.; Te, N.; Noguera-Julián, M.; Guallar, V.; Valencia, A.; et al. Protection against Reinfection with D614- or G614-SARS-CoV-2 Isolates in Golden Syrian Hamster. Emerg. Microbes Infect. 2021, 10, 797–809. [Google Scholar] [CrossRef]
- To, K.K.-W.; Hung, I.F.-N.; Ip, J.D.; Chu, A.W.-H.; Chan, W.-M.; Tam, A.R.; Fong, C.H.-Y.; Yuan, S.; Tsoi, H.-W.; Ng, A.C.-K.; et al. Coronavirus Disease 2019 (COVID-19) Re-Infection by a Phylogenetically Distinct Severe Acute Respiratory Syndrome Coronavirus 2 Strain Confirmed by Whole Genome Sequencing. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2021, 73, e2946–e2951. [Google Scholar] [CrossRef] [PubMed]
- Prado-Vivar, B.; Becerra-Wong, M.; Guadalupe, J.J.; Márquez, S.; Gutierrez, B.; Rojas-Silva, P.; Grunauer, M.; Trueba, G.; Barragán, V.; Cárdenas, P. A Case of SARS-CoV-2 Reinfection in Ecuador. Lancet Infect. Dis. 2021, 21, e142. [Google Scholar] [CrossRef]
- Prado-Vivar, B.; Becerra-Wong, M.; Guadalupe, J.J.; Marquez, S.; Gutierrez, B.; Rojas-Silva, P.; Grunauer, M.; Trueba, G.; Barragan, V.; Cardenas, P. COVID-19 Re-Infection by a Phylogenetically Distinct SARS-CoV-2 Variant, First Confirmed Event in South America. 2020. Available online: https://papers.ssrn.com/sol3/papers.cfm?abstract_id=3686174 (accessed on 22 November 2023).
- Borgogna, C.; de Andrea, M.; Griffante, G.; Lai, A.; Bergna, A.; Galli, M.; Zehender, G.; Castello, L.; Ravanini, P.; Cattrini, C.; et al. SARS-CoV-2 Reinfection in a Cancer Patient with a Defective Neutralizing Humoral Response. J. Med. Virol. 2021, 93, 6444–6446. [Google Scholar] [CrossRef]
- Gupta, V.; Bhoyar, R.C.; Jain, A.; Srivastava, S.; Upadhayay, R.; Imran, M.; Jolly, B.; Divakar, M.K.; Sharma, D.; Sehgal, P.; et al. Asymptomatic Reinfection in 2 Healthcare Workers from India with Genetically Distinct Severe Acute Respiratory Syndrome Coronavirus 2. Clin. Infect. Dis. 2021, 73, e2823–e2825. [Google Scholar] [CrossRef]
- Larson, D.; Brodniak, S.L.; Voegtly, L.J.; Cer, R.Z.; Glang, L.A.; Malagon, F.J.; Long, K.A.; Potocki, R.; Smith, D.R.; Lanteri, C.; et al. A Case of Early Reinfection With Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). Clin. Infect. Dis. 2021, 73, e2827–e2828. [Google Scholar] [CrossRef]
- Yahav, D.; Yelin, D.; Eckerle, I.; Eberhardt, C.S.; Wang, J.; Cao, B.; Kaiser, L. Definitions for Coronavirus Disease 2019 Reinfection, Relapse and PCR Re-Positivity. Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 2021, 27, 315–318. [Google Scholar] [CrossRef]
- Shastri, J.; Parikh, S.; Agrawal, S.; Chatterjee, N.; Pathak, M.; Chaudhary, S.; Sharma, C.; Kanakan, A.; Vivekanand, A.; Srinivasa Vasudevan, J.; et al. Clinical, Serological, Whole Genome Sequence Analyses to Confirm SARS-CoV-2 Reinfection in Patients from Mumbai, India. Front. Med. 2021, 8, 215. [Google Scholar] [CrossRef]
- Flacco, M.E.; Acuti Martellucci, C.; Baccolini, V.; de Vito, C.; Renzi, E.; Villari, P.; Manzoli, L. Risk of Reinfection and Disease after SARS-CoV-2 Primary Infection: Meta-Analysis. Eur. J. Clin. Investig. 2022, 52, e13845. [Google Scholar] [CrossRef] [PubMed]
- Pecoraro, V.; Pirotti, T.; Trenti, T. Evidence of SARS-CoV-2 Reinfection: Analysis of 35,000 Subjects and Overview of Systematic Reviews. Clin. Exp. Med. 2022, 23, 1213–1224. [Google Scholar] [CrossRef] [PubMed]
- Flacco, M.E.; Soldato, G.; Acuti Martellucci, C.; di Martino, G.; Carota, R.; Caponetti, A.; Manzoli, L. Risk of SARS-CoV-2 Reinfection 18 Months After Primary Infection: Population-Level Observational Study. Front. Public Health 2022, 10, 884121. [Google Scholar] [CrossRef] [PubMed]
- Ren, X.; Zhou, J.; Guo, J.; Hao, C.; Zheng, M.; Zhang, R.; Huang, Q.; Yao, X.; Li, R.; Jin, Y. Reinfection in Patients with COVID-19: A Systematic Review. Glob. Health Res. Policy 2022, 7, 12. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. Common Investigation Protocol for Investigating Suspected SARS-CoV-2 Reinfection. Available online: https://www.cdc.gov/coronavirus/2019-ncov/php/reinfection.html (accessed on 20 November 2022).
- European Centre for Disease Prevention and Control (ECDC). Data on SARS-CoV-2 Variants in the EU/EEA. Available online: https://www.ecdc.europa.eu/en/publications-data/data-virus-variants-covid-19-eueea (accessed on 22 March 2023).
- Amodio, E.; Genovese, D.; Fallucca, A.; Ferro, P.; Sparacia, B.; D’Azzo, L.; Fertitta, A.; Maida, C.M.; Vitale, F. Clinical Severity in Different Waves of SARS-CoV-2 Infection in Sicily: A Model of Smith’s “Law of Declining Virulence” from Real-World Data. Viruses 2023, 15, 125. [Google Scholar] [CrossRef]
- Cavanaugh, A.M.; Spicer, K.B.; Thoroughman, D.; Glick, C.; Winter, K. Reduced Risk of Reinfection with SARS-CoV-2 after COVID-19 Vaccination—Kentucky, May–June 2021. Morb. Mortal. Wkly. Rep. 2021, 70, 1081–1083. [Google Scholar] [CrossRef]
- Hammerman, A.; Sergienko, R.; Friger, M.; Beckenstein, T.; Peretz, A.; Netzer, D.; Yaron, S.; Arbel, R. Effectiveness of the BNT162b2 Vaccine after Recovery from COVID-19. N. Engl. J. Med. 2022, 386, 1221–1229. [Google Scholar] [CrossRef] [PubMed]
- Cohen, J.I.; Burbelo, P.D. Reinfection With SARS-CoV-2: Implications for Vaccines. Clin. Infect. Dis. 2021, 73, e4223–e4228. [Google Scholar] [CrossRef]
- Bechmann, N.; Barthel, A.; Schedl, A.; Herzig, S.; Varga, Z.; Gebhard, C.; Mayr, M.; Hantel, C.; Beuschlein, F.; Wolfrum, C.; et al. Sexual Dimorphism in COVID-19: Potential Clinical and Public Health Implications. Lancet Diabetes Endocrinol. 2022, 10, 221–230. [Google Scholar] [CrossRef] [PubMed]
- Piazza, M.F.; Amicizia, D.; Marchini, F.; Astengo, M.; Grammatico, F.; Battaglini, A.; Sticchi, C.; Paganino, C.; Lavieri, R.; Andreoli, G.B.; et al. Who Is at Higher Risk of SARS-CoV-2 Reinfection? Results from a Northern Region of Italy. Vaccines 2022, 10, 1885. [Google Scholar] [CrossRef]
- Galasso, V.; Pons, V.; Profeta, P.; Becher, M.; Brouard, S.; Foucault, M. Gender Differences in COVID-19 Attitudes and Behavior: Panel Evidence from Eight Countries. Proc. Natl. Acad. Sci. USA 2020, 117, 27285–27291. [Google Scholar] [CrossRef]
- Wenham, C.; Smith, J.; Morgan, R. COVID-19: The Gendered Impacts of the Outbreak. Lancet 2020, 395, 846–848. [Google Scholar] [CrossRef] [PubMed]
- Bertocchi, G. COVID-19 Susceptibility, Women, and Work. Available online: https://cepr.org/voxeu/columns/covid-19-susceptibility-women-and-work (accessed on 14 March 2023).
- Ballering, A.V.; Oertelt-Prigione, S.; Olde Hartman, T.C.; Rosmalen, J.G.M.; Boezen, M.; Mierau, J.O.; Franke, L.H.; Dekens, J.; Deelen, P.; Lanting, P.; et al. Sex and Gender-Related Differences in COVID-19 Diagnoses and SARS-CoV-2 Testing Practices During the First Wave of the Pandemic: The Dutch Lifelines COVID-19 Cohort Study. J. Womens Health 2021, 30, 1686–1692. [Google Scholar] [CrossRef] [PubMed]
- Hawkes, S.; Pantazis, A.; Purdie, A.; Gautam, A.; Kiwuwa-Muyingo, S.; Buse, K.; Tanaka, S.; Borkotoky, K.; Sharma, S.; Verma, R. Sex-Disaggregated Data Matters: Tracking the Impact of COVID-19 on the Health of Women and Men. Econ. Polit. 2022, 39, 55–73. [Google Scholar] [CrossRef] [PubMed]
- Jang, E.J.; Choe, Y.J.; Yun, G.-W.; Wang, S.; Cho, U.J.; Yi, S.; Lee, S.; Park, Y.-J. Reinfection with SARS-CoV-2 in General Population, South Korea; Nationwide Retrospective Cohort Study. J. Med. Virol. 2022, 94, 5589–5592. [Google Scholar] [CrossRef] [PubMed]
- Pilz, S.; Theiler-Schwetz, V.; Trummer, C.; Krause, R.; Ioannidis, J.P.A. SARS-CoV-2 Reinfections: Overview of Efficacy and Duration of Natural and Hybrid Immunity. Environ. Res. 2022, 209, 112911. [Google Scholar] [CrossRef] [PubMed]
- Özüdoğru, O.; Bahçe, Y.G.; Acer, Ö. SARS CoV-2 Reinfection Rate Is Higher in the Omicron Variant than in the Alpha and Delta Variants. Ir. J. Med. Sci. 2023, 192, 751–756. [Google Scholar] [CrossRef]
- Pulliam, J.R.C.; van Schalkwyk, C.; Govender, N.; von Gottberg, A.; Cohen, C.; Groome, M.J.; Dushoff, J.; Mlisana, K.; Moultrie, H. Increased Risk of SARS-CoV-2 Reinfection Associated with Emergence of Omicron in South Africa. Science 2022, 376, eabn4947. [Google Scholar] [CrossRef]
- Iwasaki, A. What Reinfections Mean for COVID-19. Lancet Infect. Dis. 2021, 21, 3–5. [Google Scholar] [CrossRef]
- Van Elslande, J.; Vermeersch, P.; Vandervoort, K.; Wawina-Bokalanga, T.; Vanmechelen, B.; Wollants, E.; Laenen, L.; André, E.; van Ranst, M.; Lagrou, K.; et al. Symptomatic Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Reinfection by a Phylogenetically Distinct Strain. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2021, 73, 354–356. [Google Scholar] [CrossRef]
- Salton, F.; Confalonieri, P.; Campisciano, G.; Cifaldi, R.; Rizzardi, C.; Generali, D.; Pozzan, R.; Tavano, S.; Bozzi, C.; Lapadula, G.; et al. Cytokine Profiles as Potential Prognostic and Therapeutic Markers in SARS-CoV-2-Induced ARDS. J. Clin. Med. 2022, 11, 2951. [Google Scholar] [CrossRef] [PubMed]
Months | Overall Registered COVID-19 Cases | Proportion of Reinfections | |||
---|---|---|---|---|---|
n | % of Infections on the Entire Period | n | % of Infections on the Entire Period | ||
2020 | |||||
February | 8 | 0.00% | 0 | 0 | |
March | 1583 | 0.17% | 0 | 0 | |
April | 925 | 0.10% | 0 | 0 | |
May | 176 | 0.02% | 0 | 0 | |
June | 58 | 0.01% | 0 | 0 | |
July | 185 | 0.02% | 0 | 0 | |
August | 816 | 0.09% | 0 | 0 | |
September | 2417 | 0.27% | 0 | 0 | |
October | 14,160 | 1.56% | 0 | 0 | |
November | 36,648 | 4.05% | 0 | 0 | |
December | 23,890 | 2.64% | 0 | 0 | |
Subtotal | 80,866 | ||||
2021 | |||||
January | 34,206 | 3.78% | 3 | 0.01% | |
February | 12,107 | 1.34% | 2 | 0.01% | |
March | 18,223 | 2.01% | 2 | 0.01% | |
April | 26,072 | 2.88% | 8 | 0.02% | |
May | 11,543 | 1.27% | 0 | 0.00% | |
June | 3788 | 0.42% | 4 | 0.01% | |
July | 8813 | 0.97% | 52 | 0.13% | |
August | 25,753 | 2.84% | 117 | 0.30% | |
September | 14,313 | 1.58% | 84 | 0.21% | |
October | 6826 | 0.75% | 47 | 0.12% | |
November | 11,025 | 1.22% | 53 | 0.13% | |
December | 51,515 | 5.69% | 778 | 1.98% | |
Subtotal | 224,184 | 1150 | |||
2022 | |||||
January | 193,882 | 21.40% | 4532 | 11.53% | |
February | 106,833 | 11.79% | 3480 | 8.85% | |
March | 139,244 | 15.37% | 4367 | 11.11% | |
April | 99,188 | 10.95% | 3248 | 8.26% | |
May | 57,350 | 6.33% | 2287 | 5.82% | |
June | 4282 * | 0.47% * | 5028 | 12.79% | |
July | * | * | 12,798 | 32.56% | |
August | * | * | 2411 | 6.13% | |
Subtotal | 600,779 | 38,151 | |||
TOTAL | 905,829 | 100,00% | 39,301 | 4,34% |
Reinfection Incidence | ||||
---|---|---|---|---|
Total | No | Yes | p-Value | |
n = 905,829 (% by Column) | n = 866,528 (% by Row) | n = 39,301 (% by Row) | ||
Sex | ||||
Female | 500,154 (55.2%) | 476,766 (95.3%) | 23,388 (4.7%) | <0.001 |
Male | 405,675 (44.8%) | 389,762 (96.1%) | 15,913 (3.9%) | |
Age | ||||
18–29 | 175,388 (19.4%) | 167,117 (95.3%) | 8271 (4.7%) | <0.001 |
30–39 | 166,005 (18.3%) | 157,028 (94.6%) | 8977 (5.4%) | |
40–49 | 176,819 (19.5%) | 168,207 (95.1%) | 8612 (4.9%) | |
50–59 | 159,127 (17.6%) | 152,294 (95.7%) | 6833 (4.3%) | |
60–69 | 106,029 (11.7%) | 102,295 (96.5%) | 3734 (3.5%) | |
70–79 | 67,567 (7.5%) | 65,885 (97.5%) | 1682 (2.5%) | |
80+ | 54,894 (6.1%) | 53,703 (97.8%) | 1191 (2.2%) | |
Hospitalization | ||||
No | 879,253 (97.1%) | 841,414 (95.7%) | 37,839 (4.3%) | <0.001 |
Yes | 26,576 (2.9%) | 25,115 (94.5%) | 1461 (5.5%) | |
Vaccination status | ||||
Unvaccinated | 169,625 (18.7%) | 157,852 (93.1%) | 11,773 (6.9%) | <0.001 |
Incomplete vaccination | 77,098 (8.5%) | 67,581 (87.7%) | 9517 (12.3%) | |
Full vaccination cycle | 354,078 (39.1%) | 340,943 (96.2%) | 13,135 (3.8%) | |
Boosted | 305,028 (33.7%) | 300,152 (98.4%) | 4876 (1.6%) | |
Variant dominance | ||||
Wild type | 102,924 (11.4%) | 102,921 (100%) | 3 (0%) | <0.001 |
Wild-type–Alpha | 85,077 (9.4%) | 85,056 (100%) | 21 (0%) | |
Delta | 72,238 (8%) | 71,853 (99.5%) | 385 (0.5%) | |
Delta–Omicron | 106,443 (11.8%) | 104,453 (98.1%) | 1990 (1.9%) | |
Omicron | 539,147 (59.5%) | 502,245 (93.1%) | 36,902 (6.9%) |
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Maniscalco, L.; Genovese, D.; Ravazzolo, B.; Vella, G.; Sparacia, B.; Vitale, F.; Matranga, D.; Amodio, E. Low Risk of SARS-CoV-2 Reinfection for Fully or Boosted mRNA Vaccinated Subjects in Sicily: A Population-Based Study Using Real-World Data. Vaccines 2023, 11, 1757. https://doi.org/10.3390/vaccines11121757
Maniscalco L, Genovese D, Ravazzolo B, Vella G, Sparacia B, Vitale F, Matranga D, Amodio E. Low Risk of SARS-CoV-2 Reinfection for Fully or Boosted mRNA Vaccinated Subjects in Sicily: A Population-Based Study Using Real-World Data. Vaccines. 2023; 11(12):1757. https://doi.org/10.3390/vaccines11121757
Chicago/Turabian StyleManiscalco, Laura, Dario Genovese, Barbara Ravazzolo, Giuseppe Vella, Benedetta Sparacia, Francesco Vitale, Domenica Matranga, and Emanuele Amodio. 2023. "Low Risk of SARS-CoV-2 Reinfection for Fully or Boosted mRNA Vaccinated Subjects in Sicily: A Population-Based Study Using Real-World Data" Vaccines 11, no. 12: 1757. https://doi.org/10.3390/vaccines11121757
APA StyleManiscalco, L., Genovese, D., Ravazzolo, B., Vella, G., Sparacia, B., Vitale, F., Matranga, D., & Amodio, E. (2023). Low Risk of SARS-CoV-2 Reinfection for Fully or Boosted mRNA Vaccinated Subjects in Sicily: A Population-Based Study Using Real-World Data. Vaccines, 11(12), 1757. https://doi.org/10.3390/vaccines11121757