Protective role of SARS-CoV-2 anti-S IgG against breakthrough infections among European healthcare workers during pre and post-Omicron surge—ORCHESTRA project

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Abstract

Purpose

Anti SARS-CoV-2 vaccination initially showed high effectiveness in preventing COVID-19. However, after the surge of variants of concern, the effectiveness dropped. Several studies investigated if this was related to the decrease of the humoral response over time; however, this issue is still unclear. The aim of this study was to understand whether SARS-CoV-2 anti-S IgG levels can be used to predict breakthrough infection risk and define the timing for further booster doses administration.

Method

Within the framework of the ORCHESTRA Project, over 20,000 health workers from 11 European centers were enrolled since December 2020. We performed two Cox proportional hazards survival analyses regarding pre-Omicron (from January to July 2021) and Omicron (December 2021–May 2022) periods. The serological response was classified as high (above the 75th percentile), medium (25th-75th), or low (< 25th).

Results

Seventy-four (0.33%) and 2122 (20%) health workers were infected during the first and second periods, respectively. Both Cox analyses showed that having high anti-S titer was linked to a significantly lower risk of infection as compared to having medium serological response [HR of high vs medium anti-S titer = 0.27 (95% CI 0.11–0.66) during the first phase, HR = 0.76 (95% CI 0.62–0.93) during the second phase].

Conclusion

Vaccine effectiveness wanes significantly after new variants surge, making anti-S titer unsuitable to predict optimal timing for further booster dose administration. Studies on other immunological indicators, such as cellular immunity, are therefore needed to better understand the mechanisms and duration of protection against breakthrough infection risk.

Supplementary Information

The online version contains supplementary material available at 10.1007/s15010-024-02189-x.

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Most cited references 30

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Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine

Lindsey Baden, Hana El Sahly, Brandon Essink … (2020)

Abstract Background Vaccines are needed to prevent coronavirus disease 2019 (Covid-19) and to protect persons who are at high risk for complications. The mRNA-1273 vaccine is a lipid nanoparticle–encapsulated mRNA-based vaccine that encodes the prefusion stabilized full-length spike protein of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes Covid-19. Methods This phase 3 randomized, observer-blinded, placebo-controlled trial was conducted at 99 centers across the United States. Persons at high risk for SARS-CoV-2 infection or its complications were randomly assigned in a 1:1 ratio to receive two intramuscular injections of mRNA-1273 (100 μg) or placebo 28 days apart. The primary end point was prevention of Covid-19 illness with onset at least 14 days after the second injection in participants who had not previously been infected with SARS-CoV-2. Results The trial enrolled 30,420 volunteers who were randomly assigned in a 1:1 ratio to receive either vaccine or placebo (15,210 participants in each group). More than 96% of participants received both injections, and 2.2% had evidence (serologic, virologic, or both) of SARS-CoV-2 infection at baseline. Symptomatic Covid-19 illness was confirmed in 185 participants in the placebo group (56.5 per 1000 person-years; 95% confidence interval [CI], 48.7 to 65.3) and in 11 participants in the mRNA-1273 group (3.3 per 1000 person-years; 95% CI, 1.7 to 6.0); vaccine efficacy was 94.1% (95% CI, 89.3 to 96.8%; P<0.001). Efficacy was similar across key secondary analyses, including assessment 14 days after the first dose, analyses that included participants who had evidence of SARS-CoV-2 infection at baseline, and analyses in participants 65 years of age or older. Severe Covid-19 occurred in 30 participants, with one fatality; all 30 were in the placebo group. Moderate, transient reactogenicity after vaccination occurred more frequently in the mRNA-1273 group. Serious adverse events were rare, and the incidence was similar in the two groups. Conclusions The mRNA-1273 vaccine showed 94.1% efficacy at preventing Covid-19 illness, including severe disease. Aside from transient local and systemic reactions, no safety concerns were identified. (Funded by the Biomedical Advanced Research and Development Authority and the National Institute of Allergy and Infectious Diseases; COVE ClinicalTrials.gov number, NCT04470427.)

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Nonparametric Estimation from Incomplete Observations

E. Kaplan, Paul Meier (1958)

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Duration of effectiveness of vaccines against SARS-CoV-2 infection and COVID-19 disease: results of a systematic review and meta-regression

Daniel Feikin, Melissa Higdon, Laith Abu-Raddad … (2022)

Background Knowing whether COVID-19 vaccine effectiveness wanes is crucial for informing vaccine policy, such as the need for and timing of booster doses. We aimed to systematically review the evidence for the duration of protection of COVID-19 vaccines against various clinical outcomes, and to assess changes in the rates of breakthrough infection caused by the delta variant with increasing time since vaccination. Methods This study was designed as a systematic review and meta-regression. We did a systematic review of preprint and peer-reviewed published article databases from June 17, 2021, to Dec 2, 2021. Randomised controlled trials of COVID-19 vaccine efficacy and observational studies of COVID-19 vaccine effectiveness were eligible. Studies with vaccine efficacy or effectiveness estimates at discrete time intervals of people who had received full vaccination and that met predefined screening criteria underwent full-text review. We used random-effects meta-regression to estimate the average change in vaccine efficacy or effectiveness 1–6 months after full vaccination. Findings Of 13 744 studies screened, 310 underwent full-text review, and 18 studies were included (all studies were carried out before the omicron variant began to circulate widely). Risk of bias, established using the risk of bias 2 tool for randomised controlled trials or the risk of bias in non-randomised studies of interventions tool was low for three studies, moderate for eight studies, and serious for seven studies. We included 78 vaccine-specific vaccine efficacy or effectiveness evaluations (Pfizer–BioNTech-Comirnaty, n=38; Moderna-mRNA-1273, n=23; Janssen-Ad26.COV2.S, n=9; and AstraZeneca-Vaxzevria, n=8). On average, vaccine efficacy or effectiveness against SARS-CoV-2 infection decreased from 1 month to 6 months after full vaccination by 21·0 percentage points (95% CI 13·9–29·8) among people of all ages and 20·7 percentage points (10·2–36·6) among older people (as defined by each study, who were at least 50 years old). For symptomatic COVID-19 disease, vaccine efficacy or effectiveness decreased by 24·9 percentage points (95% CI 13·4–41·6) in people of all ages and 32·0 percentage points (11·0–69·0) in older people. For severe COVID-19 disease, vaccine efficacy or effectiveness decreased by 10·0 percentage points (95% CI 6·1–15·4) in people of all ages and 9·5 percentage points (5·7–14·6) in older people. Most (81%) vaccine efficacy or effectiveness estimates against severe disease remained greater than 70% over time. Interpretation COVID-19 vaccine efficacy or effectiveness against severe disease remained high, although it did decrease somewhat by 6 months after full vaccination. By contrast, vaccine efficacy or effectiveness against infection and symptomatic disease decreased approximately 20–30 percentage points by 6 months. The decrease in vaccine efficacy or effectiveness is likely caused by, at least in part, waning immunity, although an effect of bias cannot be ruled out. Evaluating vaccine efficacy or effectiveness beyond 6 months will be crucial for updating COVID-19 vaccine policy. Funding Coalition for Epidemic Preparedness Innovations.

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Author and article information

Contributors

Marika D’Agostini: marika.dagostini2@unibo.it

Journal

Journal ID (nlm-ta): Infection

Journal ID (iso-abbrev): Infection

Title: Infection

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0300-8126

ISSN (Electronic): 1439-0973

Publication date (Electronic): 7 February 2024

Publication date PMC-release: 7 February 2024

Publication date (Print): 2024

Volume: 52

Issue: 4

Pages: 1347-1356

Affiliations

[1 ]GRID grid.411475.2, ISNI 0000 0004 1756 948X, Occupational Medicine Unit, , University Hospital of Verona, ; 37134 Verona, Italy

[2 ]Department of Medical and Surgical Sciences, University of Bologna, ( https://ror.org/01111rn36) 40138 Bologna, Italy

[3 ]Interdisciplinary Department of Medicine, University of Bari, ( https://ror.org/027ynra39) 70121 Bari, Italy

[4 ]Unit of Occupational Health and Industrial Hygiene, Department of Medical and Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, ( https://ror.org/02q2d2610) 25121 Brescia, Italy

[5 ]Unit of Occupational Health, Hygiene, Toxicology and Prevention, University Hospital ASST Spedali Civili, ( https://ror.org/015rhss58) 25123 Brescia, Italy

[6 ]Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, ( https://ror.org/02d4c4y02) 41125 Modena, Italy

[7 ]Department of Cardiac Thoracic Vascular Sciences and Public Health, University of Padova, ( https://ror.org/00240q980) 35128 Padua, Italy

[8 ]Occupational Medicine Unit, University Hospital of Padova, ( https://ror.org/05xrcj819) 35128 Padua, Italy

[9 ]Department of Medicine and Surgery, University of Perugia, ( https://ror.org/00x27da85) 06129 Perugia, Italy

[10 ]Occupational Medicine Unit, Perugia Hospital, 06129 Perugia, Italy

[11 ]Department of Medical Sciences, Unit of Occupational Medicine, University of Trieste, ( https://ror.org/02n742c10) 34129 Trieste, Italy

[12 ]GRID grid.452479.9, Unitat de Suport a la Recerca Metropolitana Nord, , Institut Universitari d’Investigació en Atenció Primària Jordi Gol (IDIAP Jordi Gol), ; 08303 Mataró, Barcelona, Spain

[13 ]GRID grid.429186.0, ISNI 0000 0004 1756 6852, Germans Trias i Pujol Research Institute (IGTP), ; 08916 Badalona, Spain

[14 ]Grup de REcerca en Impacte de les Malalties Cròniques i les Seves Trajectòries (GRIMTra), (2021 SGR 01537), Institut Universitari d’Investigació en Atenció Primària Jordi Gol (IDIAPJGol), ( https://ror.org/0370bpp07) 08303 Barcelona, Spain

[15 ]Network for Research on Chronicity, Primary Care, and Health Promotion (RICAPPS) (RD21/0016/0029), Insitituto de Salud Carlos III, ( https://ror.org/00ca2c886) 28029 Madrid, Spain

[16 ]GRID grid.22061.37, ISNI 0000 0000 9127 6969, Direcció d’Atenció Primària Metropolitana Nord Institut Català de Salut, ; 08204 Barcelona, Spain

[17 ]Universitat Autónoma de Barcelona, ( https://ror.org/052g8jq94) 08193 Bellaterra, Spain

[18 ]GRID grid.414928.2, ISNI 0000 0004 0500 8159, National Institute of Public Health, ; 050463 Bucharest, Romania

[19 ]Epidemiology Department, Regional Authority of Public Health, 97556 Banská Bystrica, Slovakia

[20 ]Section of Occupational Medicine, Department of Diagnostics and Public Health, University of Verona, ( https://ror.org/039bp8j42) 37134 Verona, Italy

[21 ]Unit of Epidemiology and Medical Statistics, Department of Diagnostics and Public Health, University of Verona, ( https://ror.org/039bp8j42) 37134 Verona, Italy

Article

Publisher ID: 2189

DOI: 10.1007/s15010-024-02189-x

PMC ID: 11289150

PubMed ID: 38326526

SO-VID: ec4b65d5-bb9f-4114-af00-6f239c11b044

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 9 December 2023

Date accepted : 16 January 2024

Funding

Funded by: European Commission, Horizon 2020 Program

Award ID: 101016167

Funded by: Alma Mater Studiorum - Università di Bologna

Open Access :

Open access funding provided by Alma Mater Studiorum - Università di Bologna within the CRUI-CARE Agreement.

Custom metadata

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: healthcare workers,covid-19,sars-cov-2,sars-cov-2 anti-s igg,covid-19 vaccination,breakthrough infections,omicron variant

Data availability:

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: healthcare workers, covid-19, sars-cov-2, sars-cov-2 anti-s igg, covid-19 vaccination, breakthrough infections, omicron variant

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Protective role of SARS-CoV-2 anti-S IgG against breakthrough infections among European healthcare workers during pre and post-Omicron surge—ORCHESTRA project

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Novel Coronavirus Disease COVID-19

Most cited references 30

Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine

Nonparametric Estimation from Incomplete Observations

Duration of effectiveness of vaccines against SARS-CoV-2 infection and COVID-19 disease: results of a systematic review and meta-regression

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