SARS-CoV-2 variant replacement constrains vaccine-specific viral diversification

Bethany L. Dearlove; Anthony C. Fries; Nusrat J. Epsi; Stephanie A. Richard; Anuradha Ganesan; Nikhil Huprikar; David A. Lindholm; Katrin Mende; Rhonda E. Colombo; Christopher Colombo; Hongjun Bai; Derek T. Larson; Evan C. Ewers; Tahaniyat Lalani; Alfred G. Smith; Catherine M. Berjohn; Ryan C. Maves; Milissa U. Jones; David Saunders; Carlos J. Maldonado; Rupal M. Mody; Samantha E. Bazan; David R. Tribble; Timothy Burgess; Mark P. Simons; Brian K. Agan; Simon D. Pollett; Morgane Rolland

doi:10.1093/ve/veae071

SARS-CoV-2 variant replacement constrains vaccine-specific viral diversification

Bethany L. Dearlove, Anthony C. Fries, Nusrat J. Epsi, Stephanie A. Richard, Anuradha Ganesan, Nikhil Huprikar, David A. Lindholm, Katrin Mende, Rhonda E. Colombo, Christopher Colombo, Hongjun Bai, Derek T. Larson, Evan C. Ewers, Tahaniyat Lalani, Alfred G. Smith, Catherine M. Berjohn, Ryan C. Maves, Milissa U. Jones, David Saunders, Carlos J. MaldonadoRupal M. Mody, Samantha E. Bazan, David R. Tribble, Timothy Burgess, Mark P. Simons, Brian K. Agan, Simon D. Pollett, Morgane Rolland^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Coronavirus disease 2019 (COVID-19) vaccine breakthrough infections have been important for all circulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variant periods, but the contribution of vaccine-specific SARS-CoV-2 viral diversification to vaccine failure remains unclear. This study analyzed 595 SARS-CoV-2 sequences collected from the Military Health System beneficiaries between December 2020 and April 2022 to investigate the impact of vaccination on viral diversity. By comparing sequences based on the vaccination status of the participant, we found limited evidence indicating that vaccination was associated with increased viral diversity in the SARS-CoV-2 spike, and we show little to no evidence of a substantial sieve effect within major variants; rather, we show that rapid variant replacement constrained intragenotype COVID-19 vaccine strain immune escape. These data suggest that, during past and perhaps future periods of rapid SARS-CoV-2 variant replacement, vaccine-mediated effects were subsumed with other drivers of viral diversity due to the massive scale of infections and vaccinations that occurred in a short time frame. However, our results also highlight some limitations of using sieve analysis methods outside of placebo-controlled clinical trials.

Original language	English
Article number	veae071
Journal	Virus Evolution
Volume	10
Issue number	1
DOIs	https://doi.org/10.1093/ve/veae071
State	Published - 2024
Externally published	Yes

Keywords

SARS-CoV-2
sieve analysis
vaccine breakthrough
variants

Access to Document

10.1093/ve/veae071

Cite this

Dearlove, B. L., Fries, A. C., Epsi, N. J., Richard, S. A., Ganesan, A., Huprikar, N., Lindholm, D. A., Mende, K., Colombo, R. E., Colombo, C., Bai, H., Larson, D. T., Ewers, E. C., Lalani, T., Smith, A. G., Berjohn, C. M., Maves, R. C., Jones, M. U., Saunders, D., ... Rolland, M. (2024). SARS-CoV-2 variant replacement constrains vaccine-specific viral diversification. Virus Evolution, 10(1), Article veae071. https://doi.org/10.1093/ve/veae071

@article{8606ba75e8a3425386d722f79b06726d,

title = "SARS-CoV-2 variant replacement constrains vaccine-specific viral diversification",

abstract = "Coronavirus disease 2019 (COVID-19) vaccine breakthrough infections have been important for all circulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variant periods, but the contribution of vaccine-specific SARS-CoV-2 viral diversification to vaccine failure remains unclear. This study analyzed 595 SARS-CoV-2 sequences collected from the Military Health System beneficiaries between December 2020 and April 2022 to investigate the impact of vaccination on viral diversity. By comparing sequences based on the vaccination status of the participant, we found limited evidence indicating that vaccination was associated with increased viral diversity in the SARS-CoV-2 spike, and we show little to no evidence of a substantial sieve effect within major variants; rather, we show that rapid variant replacement constrained intragenotype COVID-19 vaccine strain immune escape. These data suggest that, during past and perhaps future periods of rapid SARS-CoV-2 variant replacement, vaccine-mediated effects were subsumed with other drivers of viral diversity due to the massive scale of infections and vaccinations that occurred in a short time frame. However, our results also highlight some limitations of using sieve analysis methods outside of placebo-controlled clinical trials.",

keywords = "SARS-CoV-2, sieve analysis, vaccine breakthrough, variants",

author = "Dearlove, {Bethany L.} and Fries, {Anthony C.} and Epsi, {Nusrat J.} and Richard, {Stephanie A.} and Anuradha Ganesan and Nikhil Huprikar and Lindholm, {David A.} and Katrin Mende and Colombo, {Rhonda E.} and Christopher Colombo and Hongjun Bai and Larson, {Derek T.} and Ewers, {Evan C.} and Tahaniyat Lalani and Smith, {Alfred G.} and Berjohn, {Catherine M.} and Maves, {Ryan C.} and Jones, {Milissa U.} and David Saunders and Maldonado, {Carlos J.} and Mody, {Rupal M.} and Bazan, {Samantha E.} and Tribble, {David R.} and Timothy Burgess and Simons, {Mark P.} and Agan, {Brian K.} and Pollett, {Simon D.} and Morgane Rolland",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

doi = "10.1093/ve/veae071",

language = "English",

volume = "10",

journal = "Virus Evolution",

issn = "2057-1577",

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Dearlove, BL, Fries, AC, Epsi, NJ, Richard, SA , Ganesan, A, Huprikar, N, Lindholm, DA , Mende, K , Colombo, RE , Colombo, C, Bai, H, Larson, DT, Ewers, EC, Lalani, T, Smith, AG, Berjohn, CM, Maves, RC, Jones, MU, Saunders, D, Maldonado, CJ, Mody, RM, Bazan, SE, Tribble, DR , Burgess, T , Simons, MP , Agan, BK , Pollett, SD & Rolland, M 2024, 'SARS-CoV-2 variant replacement constrains vaccine-specific viral diversification', Virus Evolution, vol. 10, no. 1, veae071. https://doi.org/10.1093/ve/veae071

TY - JOUR

T1 - SARS-CoV-2 variant replacement constrains vaccine-specific viral diversification

AU - Dearlove, Bethany L.

AU - Fries, Anthony C.

AU - Epsi, Nusrat J.

AU - Richard, Stephanie A.

AU - Ganesan, Anuradha

AU - Huprikar, Nikhil

AU - Lindholm, David A.

AU - Mende, Katrin

AU - Colombo, Rhonda E.

AU - Colombo, Christopher

AU - Bai, Hongjun

AU - Larson, Derek T.

AU - Ewers, Evan C.

AU - Lalani, Tahaniyat

AU - Smith, Alfred G.

AU - Berjohn, Catherine M.

AU - Maves, Ryan C.

AU - Jones, Milissa U.

AU - Saunders, David

AU - Maldonado, Carlos J.

AU - Mody, Rupal M.

AU - Bazan, Samantha E.

AU - Tribble, David R.

AU - Burgess, Timothy

AU - Simons, Mark P.

AU - Agan, Brian K.

AU - Pollett, Simon D.

AU - Rolland, Morgane

PY - 2024

Y1 - 2024

N2 - Coronavirus disease 2019 (COVID-19) vaccine breakthrough infections have been important for all circulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variant periods, but the contribution of vaccine-specific SARS-CoV-2 viral diversification to vaccine failure remains unclear. This study analyzed 595 SARS-CoV-2 sequences collected from the Military Health System beneficiaries between December 2020 and April 2022 to investigate the impact of vaccination on viral diversity. By comparing sequences based on the vaccination status of the participant, we found limited evidence indicating that vaccination was associated with increased viral diversity in the SARS-CoV-2 spike, and we show little to no evidence of a substantial sieve effect within major variants; rather, we show that rapid variant replacement constrained intragenotype COVID-19 vaccine strain immune escape. These data suggest that, during past and perhaps future periods of rapid SARS-CoV-2 variant replacement, vaccine-mediated effects were subsumed with other drivers of viral diversity due to the massive scale of infections and vaccinations that occurred in a short time frame. However, our results also highlight some limitations of using sieve analysis methods outside of placebo-controlled clinical trials.

AB - Coronavirus disease 2019 (COVID-19) vaccine breakthrough infections have been important for all circulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variant periods, but the contribution of vaccine-specific SARS-CoV-2 viral diversification to vaccine failure remains unclear. This study analyzed 595 SARS-CoV-2 sequences collected from the Military Health System beneficiaries between December 2020 and April 2022 to investigate the impact of vaccination on viral diversity. By comparing sequences based on the vaccination status of the participant, we found limited evidence indicating that vaccination was associated with increased viral diversity in the SARS-CoV-2 spike, and we show little to no evidence of a substantial sieve effect within major variants; rather, we show that rapid variant replacement constrained intragenotype COVID-19 vaccine strain immune escape. These data suggest that, during past and perhaps future periods of rapid SARS-CoV-2 variant replacement, vaccine-mediated effects were subsumed with other drivers of viral diversity due to the massive scale of infections and vaccinations that occurred in a short time frame. However, our results also highlight some limitations of using sieve analysis methods outside of placebo-controlled clinical trials.

KW - SARS-CoV-2

KW - sieve analysis

KW - vaccine breakthrough

KW - variants

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U2 - 10.1093/ve/veae071

DO - 10.1093/ve/veae071

M3 - Article

AN - SCOPUS:85206473329

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