Determinants of Anti-S Immune Response at 9 Months after COVID-19 Vaccination in a Multicentric European Cohort of Healthcare Workers—ORCHESTRA Project
Abstract
:1. Introduction
2. Methods
3. Results
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Venugopal, U.; Jilani, N.; Rabah, S.; Shariff, M.A.; Jawed, M.; Mendez Batres, A.; Abubacker, M.; Menon, S.; Pillai, A.; Shabarek, N.; et al. SARS-CoV-2 seroprevalence among health care workers in a New York City hospital: A cross-sectional analysis during the COVID-19 pandemic. Int. J. Infect. Dis. 2021, 102, 63–69. [Google Scholar] [CrossRef] [PubMed]
- Iversen, K.; Bundgaard, H.; Hasselbalch, R.B.; Kristensen, J.H.; Nielsen, P.B.; Pries-Heje, M.; Knudsen, A.D.; Christensen, C.E.; Fogh, K.; Norsk, J.B.; et al. Risk of COVID-19 in health-care workers in Denmark: An observational cohort study. Lancet Infect. Dis. 2020, 20, 1401–1408. [Google Scholar] [CrossRef] [PubMed]
- Joint Committee on Vaccination and Immunisation. Advice on Priority Groups for COVID-19 Vaccination, 30 December 2020. London, Department of Health and Social Care. 2020. Available online: https://www.gov.uk/government/publications/priority-groups-for-coronavirus-covid-19-vaccination-advice-from-the-jcvi-30-december-2020/joint-committee-on-vaccination-and-immunisation-advice-on-priority-groups-for-covid-19-vaccination-30-december-2020 (accessed on 1 September 2022).
- Polack, F.P.; Thomas, S.J.; Kitchin, N.; Absalon, J.; Gurtman, A.; Lockhart, S.; Perez, J.L.; Marc, G.P.; Moreira, E.D.; Zerbini, C.; et al. Safety and Efficacy of the BNT162b2 mRNA COVID-19 Vaccine. N. Engl. J. Med. 2020, 383, 2603–2615. [Google Scholar] [CrossRef] [PubMed]
- Baden, L.R.; El Sahly, H.M.; Essink, B.; Kotloff, K.; Frey, S.; Novak, R.; Creech, C.B.; Gettigan, J.M.; Khetan, S.; Segall, N.; et al. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N. Engl. J. Med. 2021, 384, 403–416. [Google Scholar] [CrossRef] [PubMed]
- Bernal, J.L.; Andrews, N.; Gower, C.; Robertson, C.; Stowe, J.; Tessier, E.; Simmons, R.; Cottrell, S.; Roberts, R.; O’Doherty, M.; et al. Effectiveness of the Pfizer-BioNTech and Oxford-AstraZeneca vaccines on COVID-19 related symptoms, hospital admissions, and mortality in older adults in England: Test negative case-control study. BMJ 2021, 373, n1088. [Google Scholar] [CrossRef] [PubMed]
- Fiolet, T.; Kherabi, Y.; MacDonald, C.J.; Ghosn, J.; Peiffer-Smadja, N. Comparing COVID-19 vaccines for their characteristics, efficacy and effectiveness against SARS-CoV-2 and variants of concern: A narrative review. Clin. Microbiol. Infect. 2022, 28, 202–221. [Google Scholar] [CrossRef] [PubMed]
- Vallée, A.; Vasse, M.; Mazaux, L.; Bonan, B.; Amiel, C.; Zia-Chahabi, S.; Chan-Hew-Wai, A.; Farfour, E.; Camps, E.; Touche, P.; et al. An Immunogenicity Report for the Comparison between Heterologous and Homologous Prime-Boost Schedules with ChAdOx1-S and BNT162b2 Vaccines. J. Clin. Med. 2021, 10, 3817. [Google Scholar] [CrossRef]
- Cabezas, C.; Coma, E.; Mora-Fernandez, N.; Li, X.; Martinez-Marcos, M.; Fina, F.; Fabregas, M.; Hermosilla, E.; Jover, A.; Contel, J.C.; et al. Associations of BNT162b2 vaccination with SARS-CoV-2 infection and hospital admission and death with COVID-19 in nursing homes and healthcare workers in Catalonia: Prospective cohort study. BMJ 2021, 374, n1868. [Google Scholar] [CrossRef]
- Gilbert, P.B.; Montefiori, D.C.; McDermott, A.B.; Fong, Y.; Benkeser, D.; Deng, W.; Zhou, H.; Houchens, C.R.; Martins, K.; Jayashankar, L.; et al. Immune correlates analysis of the mRNA-1273 COVID-19 vaccine efficacy clinical trial. Science 2022, 375, 43–50. [Google Scholar] [CrossRef]
- Cho, A.; Wrammert, J. Implications of broadly neutralizing antibodies in the development of a universal influenza vaccine. Curr. Opin. Virol. 2016, 17, 110–115. [Google Scholar] [CrossRef]
- Turkkan, A.; Saglik, I.; Turan, C.; Sahin, A.; Akalin, H.; Ener, B.; Kara, A.; Celebi, S.; Sahin, E.; Hacimustafaoglu, M. Nine-month course of SARS-CoV-2 antibodies in individuals with COVID-19 infection. Ir. J. Med. Sci. 2022, 191, 2803–2811. [Google Scholar] [CrossRef] [PubMed]
- Lumley, S.F.; O’Donnell, D.; Stoesser, N.E.; Matthews, P.C.; Howarth, A.; Hatch, S.B.; Marsden, B.D.; Cox, S.; James, T.; Warren, F.; et al. Antibody Status and Incidence of SARS-CoV-2 Infection in Health Care Workers. N. Engl. J. Med. 2021, 384, 533–540. [Google Scholar] [CrossRef]
- Available online: https://orchestra-cohort.eu (accessed on 1 September 2022).
- Visci, G.; Zunarelli, C.; Mansour, I.; Porru, S.; De Palma, G.; Duval, X.; Monaco, M.G.L. Serological response after SARS-CoV2 vaccination in healthcare workers: A multicenter study. Med. Lav. 2022, 113, e2022022. [Google Scholar]
- Collatuzzo, G.; Visci, G.; Violante, F.S.; Porru, S.; Spiteri, G.; Monaco, M.G.L.; Fillon, F.L.; Negro, C.; Janke, C.; Castelletti, N.; et al. Determinants of anti-S immune response at 6 months after COVID-19 vaccination in a multicentric European cohort of healthcare workers—ORCHESTRA project. Front. Immunol. 2022, 13. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.; Zhu, J.; Liu, Z.; Li, C.; Guo, Y.; Wang, Y.; Chen, K. Kinetics of severe acute respiratory syndrome coronavirus 2 infection antibody responses. Front. Immunol. 2022, 13, 864278. [Google Scholar] [CrossRef] [PubMed]
- Li, Z.; Xiang, T.; Liang, B.; Deng, H.; Wang, H.; Feng, X.; Monaco, M.G.L.; Spiteri, G.; Carta, A.; Lippi, G.; et al. Characterization of SARS-CoV-2-Specific Humoral and Cellular Immune Responses Induced by Inactivated COVID-19 Vaccines in a Real-World Setting. Front. Immunol. 2021, 12, 802858. [Google Scholar] [CrossRef]
- Yalçın, T.Y.; Topçu, D.I.; Doğan, Ö.; Aydın, S.; Sarı, N.; Erol, Ç.; Kuloğlu, Z.E.; Azap, K.; Can, F.; Arslan, H.; et al. Immunogenicity after two doses of inactivated virus vaccine in healthcare workers with and without previous COVID-19 infection: Prospective observational study. J. Med. Virol. 2022, 94, 279–286. [Google Scholar] [CrossRef] [PubMed]
- Cervantes-Luevano, K.; Espino-Vazquez, A.N.; Flores-Acosta, G.; Bernaldez-Sarabia, J.; Cabanillas-Bernal, O.; Gasperin-Bulbarela, J.; Gonzalez-Sanchez, R.; Comas-Garcia, A.; Licea-Navarro, A.F. Neutralizing antibodies levels are increased in individuals with heterologous vaccination and hybrid immunity with Ad5-nCoV in the north of Mexico. PLoS ONE 2022, 17, e0269032. [Google Scholar] [CrossRef]
- Violán, C.; Torán-Monserrat, P.; Quirant, B.; Lamonja-Vicente, N.; Carrasco-Ribelles, L.A.; Chacón, C.; Manresa-Dominguez, J.M.; Ramos-Roure, F.; Dacosta-Aguayo, R.; Palacios-Fernández, C.; et al. Kinetics of humoral immune response over 17 months of COVID-19 pandemic in a large cohort of healthcare workers in Spain: The ProHEpiC-19 study. BMC Infect. Dis. 2022, 22, 721. [Google Scholar] [CrossRef]
- Wolszczak-Biedrzycka, B.; Bieńkowska, A.; Dorf, J. Assessment of Post-Vaccination Antibody Response Eight Months after the Administration of BNT1622b2 Vaccine to Healthcare Workers with Particular Emphasis on the Impact of Previous COVID-19 Infection. Vaccines 2021, 9, 1508. [Google Scholar] [CrossRef]
- Wolszczak-Biedrzycka, B.; Bieńkowska, A.; Zaborowska, J.E.; Smolińska-Fijołek, E.; Biedrzycki, G.; Dorf, J. Anti-SARS-CoV-2S Antibody Levels in Healthcare Workers 10 Months after the Administration of Two BNT162b2 Vaccine Doses in View of Demographic Characteristic and Previous COVID-19 Infection. Vaccines 2022, 10, 741. [Google Scholar] [CrossRef]
- Dimeglio, C.; Herin, F.; Martin-Blondel, G.; Miedougé, M.; Izopet, J. Antibody Titers and Protection against a SARS-CoV-2 Infection. J. Infect. 2021, 2, 67–72. [Google Scholar] [CrossRef] [PubMed]
- Zimmermann, P.; Curtis, N. Factors That Influence the Immune Response to Vaccination. Clin. Microbiol. Rev. 2019, 32, e00084-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, X.; Shaw, R.H.; Stuart, A.S.V.; Greenland, M.; Aley, P.K.; Andrews, N.J.; Cameron, J.C.; Charlton, S.; Clutterbuck, E.A.; Collins, A.M.; et al. Safety and immunogenicity of heterologous versus homologous prime-boost schedules with an adenoviral vectored and mRNA COVID-19 vaccine (Com-COV): A single-blind, randomised, non-inferiority trial. Lancet 2021, 398, 856–869. [Google Scholar] [CrossRef] [PubMed]
- Lu, S. Heterologous prime-boost vaccination. Curr. Opin. Immunol. 2009, 21, 346–351. [Google Scholar] [CrossRef] [Green Version]
- Torres, I.; Poujois, S.; Albert, E.; Colomina, J.; Navarro, D. Evaluation of a rapid antigen test (Panbio™ COVID-19 Ag rapid test device) for SARS-CoV-2 detection in asymptomatic close contacts of COVID-19 patients. Clin. Microbiol. Infect. 2021, 27, e1–e636. [Google Scholar] [CrossRef]
- Dinnes, J.; Deeks, J.J.; Berhane, S.; Taylor, M.; Adriano, A.; Davenport, C.; Dittrich, S.; Emperador, D.; Takwoingi, Y.; Cunningham, J.; et al. Cochrane COVID-19 Diagnostic Test Accuracy Group. Rapid, point-of-care antigen and molecular-based tests for diagnosis of SARS-CoV-2 infection. Cochrane Database Syst Rev. 2021, 3, CD013705. [Google Scholar]
- Böger, B.; Fachi, M.M.; Vilhena, R.O.; Cobre, A.F.; Tonin, F.S.; Pontarolo, R. Systematic review with meta-analysis of the accuracy of diagnostic tests for COVID-19. Am. J. Infect. Control. 2021, 49, 21–29. [Google Scholar] [CrossRef]
- Parry, H.M.; Bruton, R.; Stephens, C.; Brown, K.; Amirthalingam, G.; Hallis, B.; Otter, A.; Zuo, J.; Moss, P. Extended interval BNT162b2 vaccination enhances peak antibody generation in older people. medRxiv 2021, 5, 1–20. [Google Scholar]
Variables | Observed | Percent | Mean | Std. Error |
---|---|---|---|---|
Cohort | ||||
Italy—Bologna | 4.402 | 21.5 | 6.46 | 0.02 |
Italy—Brescia | 6.250 | 30.5 | 5.79 | 0.01 |
Italy—Trieste | 1995 | 9.7 | 5.83 | 0.03 |
Italy—Verona | 3250 | 15.9 | 6.23 | 0.02 |
Germany—Munich | 3473 | 17.0 | 2.48 | 0.01 |
Slovakia—Multicenter | 567 | 2.8 | 5.75 | 0.05 |
Spain—Northern Barcelona region | 412 | 2.0 | 5.61 | 0.06 |
Spain—Oviedo | 127 | 0.6 | 5.20 | 0.16 |
Gender | 3473 | |||
Male | 5515 | 27.2 | 5.41 | 0.02 |
Female | 14,750 | 72.8 | 5.35 | 0.02 |
Age group | ||||
≤29 | 2667 | 13.0 | 5.53 | 0.03 |
30–39 | 4555 | 22.2 | 5.42 | 0.02 |
40–49 | 4825 | 23.6 | 5.36 | 0.02 |
≥50 | 8429 | 41.2 | 5.30 | 0.02 |
Job title | ||||
Administration | 1364 | 8.1 | 5.75 | 0.03 |
Technician | 1349 | 8.0 | 5.97 | 0.03 |
Nurses | 6314 | 37.7 | 6.02 | 0.01 |
Physician (including residents) | 4363 | 26.0 | 6.04 | 0.01 |
Other HCW (including auxiliary workers) | 3376 | 20.1 | 5.93 | 0.02 |
Previous COVID-19 infection (PCR) | ||||
Never infected | 17,889 | 87.4 | 5.21 | 0.01 |
Infected before vaccination | 2069 | 10.1 | 6.55 | 0.03 |
Infected after 1st dose | 462 | 2.3 | 6.31 | 0.07 |
Infected at both times | 48 | 0.2 | 6.07 | 0.11 |
Previous COVID-19 infection (anti-N ser. test) * | ||||
Never infected | 8313 | 82.1 | 4.17 | 0.02 |
Infected at least once | 1808 | 17.9 | 6.43 | 0.03 |
Type of vaccine | ||||
Comirnaty | 19,824 | 97.1 | 5.39 | 0.01 |
Spikevax | 446 | 2.2 | 4.91 | 0.10 |
Vaxzevria | 47 | 0.2 | 3.21 | 0.31 |
Mixed vaccines | 108 | 0.5 | 3.50 | 0.15 |
Number of doses | ||||
One dose received | 260 | 1.3 | 5.82 | 0.12 |
Two doses received | 20,216 | 98.7 | 5.36 | 0.01 |
Variables | Obs | Mean | Std. dev | Minimum | Maximum |
---|---|---|---|---|---|
Days since previous serology test to 9-month serology test | 14,541 | 141 | 43.48 | 1 | 277 |
Days since 1st vaccine dose to 9-month serology test | 20,476 | 250 | 25.60 | 210 | 330 |
Days since last vaccine dose to 9-month serology test | 20,476 | 227 | 28.14 | 0 | 331 |
RR | 95% CI | |
---|---|---|
Cohorts | ||
Italy—Bologna | ref | |
Italy—Brescia | 0.42 | 0.41–0.44 |
Italy—Trieste | 0.59 | 0.57–0.62 |
Italy—Verona | 0.72 | 0.69–0.75 |
Germany—Munich | 0.02 | 0.02–0.02 |
Slovakia—Multicentre | 0.40 | 0.37–0.43 |
Spain—Northern Barcelona region | 0.21 | 0.19–0.23 |
Spain—Oviedo | 0.31 | 0.27–0.36 |
Sex | ||
Male | ref | |
Female | 1.05 | 1.03–1.08 |
Age group | ||
10 years increase | 0.87 | 0.86–0.88 |
<29 | - | |
30–39 | - | |
40–49 | - | |
≥50 | - | |
Days since last vaccine dose to 9-month serology | ||
10 days increase | 0.97 | 0.97–0.98 |
Previous COVID-19 infection (detection: PCR/antiN serology test) | ||
Never infected | ref | |
Infected at least once | 3.03 | 2.92–3.13 |
Number of doses | ||
1 dose received | ref | |
2 doses received | 1.22 | 1.09–1.36 |
Type of vaccine received | ||
Pfizer | ref | |
Moderna | 1.51 | 1.39–1.64 |
AstraZeneca | 0.57 | 0.44–0.73 |
Mixed vaccines | 1.33 | 1.12–1.57 |
Previous COVID-19 infection (detection: PCR) | ||
Never infected | ref | |
Infected before vaccination | 2.64 | 2.53–2.76 |
Infected after 1st dose | 2.68 | 2.47–2.92 |
Infected at both times | 2.87 | 2.19–3.77 |
Previous COVID-19 infection (detection: antiN) * | ||
Never infected | ref | |
Infected at least once | 4.02 | 3.86–4.19 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Collatuzzo, G.; Lodi, V.; Feola, D.; De Palma, G.; Sansone, E.; Sala, E.; Janke, C.; Castelletti, N.; Porru, S.; Spiteri, G.; et al. Determinants of Anti-S Immune Response at 9 Months after COVID-19 Vaccination in a Multicentric European Cohort of Healthcare Workers—ORCHESTRA Project. Viruses 2022, 14, 2657. https://doi.org/10.3390/v14122657
Collatuzzo G, Lodi V, Feola D, De Palma G, Sansone E, Sala E, Janke C, Castelletti N, Porru S, Spiteri G, et al. Determinants of Anti-S Immune Response at 9 Months after COVID-19 Vaccination in a Multicentric European Cohort of Healthcare Workers—ORCHESTRA Project. Viruses. 2022; 14(12):2657. https://doi.org/10.3390/v14122657
Chicago/Turabian StyleCollatuzzo, Giulia, Vittorio Lodi, Daniela Feola, Giuseppe De Palma, Emanuele Sansone, Emma Sala, Christian Janke, Noemi Castelletti, Stefano Porru, Gianluca Spiteri, and et al. 2022. "Determinants of Anti-S Immune Response at 9 Months after COVID-19 Vaccination in a Multicentric European Cohort of Healthcare Workers—ORCHESTRA Project" Viruses 14, no. 12: 2657. https://doi.org/10.3390/v14122657