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Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study

BACKGROUND: High rates of vaccination and natural infection drive immunity and redirect selective viral adaptation. Updated boosters are installed to cope with drifted viruses, yet data on adaptive evolution under increasing immune pressure in a real-world situation are lacking. METHODS: Cross-secti...

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Autores principales: Duerr, Ralf, Dimartino, Dacia, Marier, Christian, Zappile, Paul, Wang, Guiqing, François, Fritz, Ortigoza, Mila B., Iturrate, Eduardo, Samanovic, Marie I., Mulligan, Mark J., Heguy, Adriana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10623172/
https://www.ncbi.nlm.nih.gov/pubmed/37866115
http://dx.doi.org/10.1016/j.ebiom.2023.104843
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author Duerr, Ralf
Dimartino, Dacia
Marier, Christian
Zappile, Paul
Wang, Guiqing
François, Fritz
Ortigoza, Mila B.
Iturrate, Eduardo
Samanovic, Marie I.
Mulligan, Mark J.
Heguy, Adriana
author_facet Duerr, Ralf
Dimartino, Dacia
Marier, Christian
Zappile, Paul
Wang, Guiqing
François, Fritz
Ortigoza, Mila B.
Iturrate, Eduardo
Samanovic, Marie I.
Mulligan, Mark J.
Heguy, Adriana
author_sort Duerr, Ralf
collection PubMed
description BACKGROUND: High rates of vaccination and natural infection drive immunity and redirect selective viral adaptation. Updated boosters are installed to cope with drifted viruses, yet data on adaptive evolution under increasing immune pressure in a real-world situation are lacking. METHODS: Cross-sectional study to characterise SARS-CoV-2 mutational dynamics and selective adaptation over >1 year in relation to vaccine status, viral phylogenetics, and associated clinical and demographic variables. FINDINGS. The study of >5400 SARS-CoV-2 infections between July 2021 and August 2022 in metropolitan New York portrayed the evolutionary transition from Delta to Omicron BA.1-BA.5 variants. Booster vaccinations were implemented during the Delta wave, yet booster breakthrough infections and SARS-CoV-2 re-infections were almost exclusive to Omicron. In adjusted logistic regression analyses, BA.1, BA.2, and BA.5 had a significant growth advantage over co-occurring lineages in the boosted population, unlike BA.2.12.1 or BA.4. Selection pressure by booster shots translated into diffuse adaptive evolution in Delta spike, contrasting with strong, receptor-binding motif-focused adaptive evolution in BA.2-BA.5 spike (Fisher Exact tests; non-synonymous/synonymous mutation rates per site). Convergent evolution has become common in Omicron, engaging spike positions crucial for immune escape, receptor binding, or cleavage. INTERPRETATION. Booster shots are required to cope with gaps in immunity. Their discriminative immune pressure contributes to their effectiveness but also requires monitoring of selective viral adaptation processes. Omicron BA.2 and BA.5 had a selective advantage under booster vaccination pressure, contributing to the evolution of BA.2 and BA.5 sublineages and recombinant forms that predominate in 2023. FUNDING: The study was supported by NYU institutional funds and partly by the Cancer Center Support Grant P30CA016087 at the Laura and Isaac Perlmutter Cancer Center.
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spelling pubmed-106231722023-11-04 Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study Duerr, Ralf Dimartino, Dacia Marier, Christian Zappile, Paul Wang, Guiqing François, Fritz Ortigoza, Mila B. Iturrate, Eduardo Samanovic, Marie I. Mulligan, Mark J. Heguy, Adriana eBioMedicine Articles BACKGROUND: High rates of vaccination and natural infection drive immunity and redirect selective viral adaptation. Updated boosters are installed to cope with drifted viruses, yet data on adaptive evolution under increasing immune pressure in a real-world situation are lacking. METHODS: Cross-sectional study to characterise SARS-CoV-2 mutational dynamics and selective adaptation over >1 year in relation to vaccine status, viral phylogenetics, and associated clinical and demographic variables. FINDINGS. The study of >5400 SARS-CoV-2 infections between July 2021 and August 2022 in metropolitan New York portrayed the evolutionary transition from Delta to Omicron BA.1-BA.5 variants. Booster vaccinations were implemented during the Delta wave, yet booster breakthrough infections and SARS-CoV-2 re-infections were almost exclusive to Omicron. In adjusted logistic regression analyses, BA.1, BA.2, and BA.5 had a significant growth advantage over co-occurring lineages in the boosted population, unlike BA.2.12.1 or BA.4. Selection pressure by booster shots translated into diffuse adaptive evolution in Delta spike, contrasting with strong, receptor-binding motif-focused adaptive evolution in BA.2-BA.5 spike (Fisher Exact tests; non-synonymous/synonymous mutation rates per site). Convergent evolution has become common in Omicron, engaging spike positions crucial for immune escape, receptor binding, or cleavage. INTERPRETATION. Booster shots are required to cope with gaps in immunity. Their discriminative immune pressure contributes to their effectiveness but also requires monitoring of selective viral adaptation processes. Omicron BA.2 and BA.5 had a selective advantage under booster vaccination pressure, contributing to the evolution of BA.2 and BA.5 sublineages and recombinant forms that predominate in 2023. FUNDING: The study was supported by NYU institutional funds and partly by the Cancer Center Support Grant P30CA016087 at the Laura and Isaac Perlmutter Cancer Center. Elsevier 2023-10-20 /pmc/articles/PMC10623172/ /pubmed/37866115 http://dx.doi.org/10.1016/j.ebiom.2023.104843 Text en © 2023 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Articles
Duerr, Ralf
Dimartino, Dacia
Marier, Christian
Zappile, Paul
Wang, Guiqing
François, Fritz
Ortigoza, Mila B.
Iturrate, Eduardo
Samanovic, Marie I.
Mulligan, Mark J.
Heguy, Adriana
Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study
title Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study
title_full Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study
title_fullStr Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study
title_full_unstemmed Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study
title_short Selective adaptation of SARS-CoV-2 Omicron under booster vaccine pressure: a multicentre observational study
title_sort selective adaptation of sars-cov-2 omicron under booster vaccine pressure: a multicentre observational study
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10623172/
https://www.ncbi.nlm.nih.gov/pubmed/37866115
http://dx.doi.org/10.1016/j.ebiom.2023.104843
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