SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2

Oliver Eales; Andrew J. Page; Leonardo de Oliveira Martins; Haowei Wang; Barbara Bodinier; David Haw; Jakob Jonnerby; Christina Atchison; Samuel C. Robson; Thomas R. Connor; Nicholas J. Loman; Tanya Golubchik; David K. Jackson; William L. Hamilton; Catherine Moore; Fiona Rogan; Derek J. Fairley; Husam Osman; David A. Simpson; James P. McKenna; Ben Temperton; Helen Adams; Marc Fuchs; Julia Miskelly; Thomas Davis; Anna Casey; Christopher R. Jones; Stephen Bridgett; Salman Goudarzi; Sophie Jones; Sarah Taylor; Tanya Curran; Ken Smith; Tim Wyatt; Timofey Skvortsov; Declan T. Bradley; Jonathan Moore; Jack C.D. Lee; Zoltan Molnar; Kate Johnson; Leanne J. Murray; Darren R. Murray; Chris Baxter; Deborah Lavin; Arun Mariappan; Clara Radulescu; Aditi Singh; Miao Tang; Kathleen A. Williamson; Carol Scott; The COVID-19 Genomics UK (COG-UK) Consortium

doi:10.1186/s12879-022-07628-4

SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2

Oliver Eales, Andrew J. Page, Leonardo de Oliveira Martins, Haowei Wang, Barbara Bodinier, David Haw, Jakob Jonnerby, Christina Atchison, Samuel C. Robson, Thomas R. Connor, Nicholas J. Loman, Tanya Golubchik, David K. Jackson, William L. Hamilton, Catherine Moore, Fiona Rogan, Derek J. Fairley, Husam Osman, David A. Simpson, James P. McKennaBen Temperton, Helen Adams, Marc Fuchs, Julia Miskelly, Thomas Davis, Anna Casey, Christopher R. Jones, Stephen Bridgett, Salman Goudarzi, Sophie Jones, Sarah Taylor, Tanya Curran, Ken Smith, Tim Wyatt, Timofey Skvortsov, Declan T. Bradley, Jonathan Moore, Jack C.D. Lee, Zoltan Molnar, Kate Johnson, Leanne J. Murray, Darren R. Murray, Chris Baxter, Deborah Lavin, Arun Mariappan, Clara Radulescu, Aditi Singh, Miao Tang, Kathleen A. Williamson, Carol Scott, The COVID-19 Genomics UK (COG-UK) Consortium

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

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Abstract

Background: Since the emergence of SARS-CoV-2, evolutionary pressure has driven large increases in the transmissibility of the virus. However, with increasing levels of immunity through vaccination and natural infection the evolutionary pressure will switch towards immune escape. Genomic surveillance in regions of high immunity is crucial in detecting emerging variants that can more successfully navigate the immune landscape.

Methods: We present phylogenetic relationships and lineage dynamics within England (a country with high levels of immunity), as inferred from a random community sample of individuals who provided a self-administered throat and nose swab for rt-PCR testing as part of the REal-time Assessment of Community Transmission-1 (REACT-1) study. During round 14 (9 September–27 September 2021) and 15 (19 October–5 November 2021) lineages were determined for 1322 positive individuals, with 27.1% of those which reported their symptom status reporting no symptoms in the previous month.

Results: We identified 44 unique lineages, all of which were Delta or Delta sub-lineages, and found a reduction in their mutation rate over the study period. The proportion of the Delta sub-lineage AY.4.2 was increasing, with a reproduction number 15% (95% CI 8–23%) greater than the most prevalent lineage, AY.4. Further, AY.4.2 was less associated with the most predictive COVID-19 symptoms (p = 0.029) and had a reduced mutation rate (p = 0.050). Both AY.4.2 and AY.4 were found to be geographically clustered in September but this was no longer the case by late October/early November, with only the lineage AY.6 exhibiting clustering towards the South of England.

Conclusions: As SARS-CoV-2 moves towards endemicity and new variants emerge, genomic data obtained from random community samples can augment routine surveillance data without the potential biases introduced due to higher sampling rates of symptomatic individuals.

Original language	English
Article number	647
Number of pages	17
Journal	BMC Infectious Diseases
Volume	22
Early online date	27 Jul 2022
DOIs	https://doi.org/10.1186/s12879-022-07628-4
Publication status	Published - Dec 2022

Bibliographical note

Funding Information:
The study was funded by the Department of Health and Social Care in England. Sequencing was provided through the COVID-19 Genomics UK Consortium (COG-UK) which is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR) [grant code: MC_PC_19027], and Genome Research Limited, operating as the Wellcome Sanger Institute.

Publisher Copyright:
© 2022, The Author(s).

Keywords

COVID-19
Delta variant
Genetic diversity
Mutation
SARS-CoV-2
Transmission advantage

ASJC Scopus subject areas

Infectious Diseases

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2
Copyright 2022 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
Final published version, 7.19 MBLicence: CC BY

Cite this

Eales, O., Page, A. J., de Oliveira Martins, L., Wang, H., Bodinier, B., Haw, D., Jonnerby, J., Atchison, C., Robson, S. C., Connor, T. R., Loman, N. J., Golubchik, T., Jackson, D. K., Hamilton, W. L., Moore, C., Rogan, F., Fairley, D. J., Osman, H., Simpson, D. A., ... The COVID-19 Genomics UK (COG-UK) Consortium (2022). SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2. BMC Infectious Diseases, 22, Article 647. https://doi.org/10.1186/s12879-022-07628-4

@article{42b9710b38df41129336be3021bca0aa,

title = "SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2",

abstract = "Background: Since the emergence of SARS-CoV-2, evolutionary pressure has driven large increases in the transmissibility of the virus. However, with increasing levels of immunity through vaccination and natural infection the evolutionary pressure will switch towards immune escape. Genomic surveillance in regions of high immunity is crucial in detecting emerging variants that can more successfully navigate the immune landscape. Methods: We present phylogenetic relationships and lineage dynamics within England (a country with high levels of immunity), as inferred from a random community sample of individuals who provided a self-administered throat and nose swab for rt-PCR testing as part of the REal-time Assessment of Community Transmission-1 (REACT-1) study. During round 14 (9 September–27 September 2021) and 15 (19 October–5 November 2021) lineages were determined for 1322 positive individuals, with 27.1% of those which reported their symptom status reporting no symptoms in the previous month. Results: We identified 44 unique lineages, all of which were Delta or Delta sub-lineages, and found a reduction in their mutation rate over the study period. The proportion of the Delta sub-lineage AY.4.2 was increasing, with a reproduction number 15% (95% CI 8–23%) greater than the most prevalent lineage, AY.4. Further, AY.4.2 was less associated with the most predictive COVID-19 symptoms (p = 0.029) and had a reduced mutation rate (p = 0.050). Both AY.4.2 and AY.4 were found to be geographically clustered in September but this was no longer the case by late October/early November, with only the lineage AY.6 exhibiting clustering towards the South of England. Conclusions: As SARS-CoV-2 moves towards endemicity and new variants emerge, genomic data obtained from random community samples can augment routine surveillance data without the potential biases introduced due to higher sampling rates of symptomatic individuals.",

keywords = "COVID-19, Delta variant, Genetic diversity, Mutation, SARS-CoV-2, Transmission advantage",

author = "Oliver Eales and Page, {Andrew J.} and {de Oliveira Martins}, Leonardo and Haowei Wang and Barbara Bodinier and David Haw and Jakob Jonnerby and Christina Atchison and Robson, {Samuel C.} and Connor, {Thomas R.} and Loman, {Nicholas J.} and Tanya Golubchik and Jackson, {David K.} and Hamilton, {William L.} and Catherine Moore and Fiona Rogan and Fairley, {Derek J.} and Husam Osman and Simpson, {David A.} and McKenna, {James P.} and Ben Temperton and Helen Adams and Marc Fuchs and Julia Miskelly and Thomas Davis and Anna Casey and Jones, {Christopher R.} and Stephen Bridgett and Salman Goudarzi and Sophie Jones and Sarah Taylor and Tanya Curran and Ken Smith and Tim Wyatt and Timofey Skvortsov and Bradley, {Declan T.} and Jonathan Moore and Lee, {Jack C.D.} and Zoltan Molnar and Kate Johnson and Murray, {Leanne J.} and Murray, {Darren R.} and Chris Baxter and Deborah Lavin and Arun Mariappan and Clara Radulescu and Aditi Singh and Miao Tang and Williamson, {Kathleen A.} and Carol Scott and {The COVID-19 Genomics UK (COG-UK) Consortium}",

note = "Funding Information: The study was funded by the Department of Health and Social Care in England. Sequencing was provided through the COVID-19 Genomics UK Consortium (COG-UK) which is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR) [grant code: MC_PC_19027], and Genome Research Limited, operating as the Wellcome Sanger Institute. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1186/s12879-022-07628-4",

language = "English",

volume = "22",

journal = "BMC Infectious Diseases",

issn = "1471-2334",

publisher = "BioMed Central",

}

Eales, O, Page, AJ, de Oliveira Martins, L, Wang, H, Bodinier, B, Haw, D, Jonnerby, J, Atchison, C, Robson, SC, Connor, TR, Loman, NJ, Golubchik, T, Jackson, DK, Hamilton, WL, Moore, C, Rogan, F, Fairley, DJ, Osman, H, Simpson, DA, McKenna, JP, Temperton, B, Adams, H, Fuchs, M, Miskelly, J, Davis, T, Casey, A, Jones, CR, Bridgett, S, Goudarzi, S, Jones, S, Taylor, S, Curran, T, Smith, K, Wyatt, T, Skvortsov, T, Bradley, DT, Moore, J, Lee, JCD, Molnar, Z, Johnson, K, Murray, LJ, Murray, DR, Baxter, C, Lavin, D, Mariappan, A, Radulescu, C, Singh, A, Tang, M, Williamson, KA, Scott, C & The COVID-19 Genomics UK (COG-UK) Consortium 2022, 'SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2', BMC Infectious Diseases, vol. 22, 647. https://doi.org/10.1186/s12879-022-07628-4

TY - JOUR

T1 - SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2

AU - Eales, Oliver

AU - Page, Andrew J.

AU - de Oliveira Martins, Leonardo

AU - Wang, Haowei

AU - Bodinier, Barbara

AU - Haw, David

AU - Jonnerby, Jakob

AU - Atchison, Christina

AU - Robson, Samuel C.

AU - Connor, Thomas R.

AU - Loman, Nicholas J.

AU - Golubchik, Tanya

AU - Jackson, David K.

AU - Hamilton, William L.

AU - Moore, Catherine

AU - Rogan, Fiona

AU - Fairley, Derek J.

AU - Osman, Husam

AU - Simpson, David A.

AU - McKenna, James P.

AU - Temperton, Ben

AU - Adams, Helen

AU - Fuchs, Marc

AU - Miskelly, Julia

AU - Davis, Thomas

AU - Casey, Anna

AU - Jones, Christopher R.

AU - Bridgett, Stephen

AU - Goudarzi, Salman

AU - Jones, Sophie

AU - Taylor, Sarah

AU - Curran, Tanya

AU - Smith, Ken

AU - Wyatt, Tim

AU - Skvortsov, Timofey

AU - Bradley, Declan T.

AU - Moore, Jonathan

AU - Lee, Jack C.D.

AU - Molnar, Zoltan

AU - Johnson, Kate

AU - Murray, Leanne J.

AU - Murray, Darren R.

AU - Baxter, Chris

AU - Lavin, Deborah

AU - Mariappan, Arun

AU - Radulescu, Clara

AU - Singh, Aditi

AU - Tang, Miao

AU - Williamson, Kathleen A.

AU - Scott, Carol

AU - The COVID-19 Genomics UK (COG-UK) Consortium

N1 - Funding Information: The study was funded by the Department of Health and Social Care in England. Sequencing was provided through the COVID-19 Genomics UK Consortium (COG-UK) which is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR) [grant code: MC_PC_19027], and Genome Research Limited, operating as the Wellcome Sanger Institute. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - Background: Since the emergence of SARS-CoV-2, evolutionary pressure has driven large increases in the transmissibility of the virus. However, with increasing levels of immunity through vaccination and natural infection the evolutionary pressure will switch towards immune escape. Genomic surveillance in regions of high immunity is crucial in detecting emerging variants that can more successfully navigate the immune landscape. Methods: We present phylogenetic relationships and lineage dynamics within England (a country with high levels of immunity), as inferred from a random community sample of individuals who provided a self-administered throat and nose swab for rt-PCR testing as part of the REal-time Assessment of Community Transmission-1 (REACT-1) study. During round 14 (9 September–27 September 2021) and 15 (19 October–5 November 2021) lineages were determined for 1322 positive individuals, with 27.1% of those which reported their symptom status reporting no symptoms in the previous month. Results: We identified 44 unique lineages, all of which were Delta or Delta sub-lineages, and found a reduction in their mutation rate over the study period. The proportion of the Delta sub-lineage AY.4.2 was increasing, with a reproduction number 15% (95% CI 8–23%) greater than the most prevalent lineage, AY.4. Further, AY.4.2 was less associated with the most predictive COVID-19 symptoms (p = 0.029) and had a reduced mutation rate (p = 0.050). Both AY.4.2 and AY.4 were found to be geographically clustered in September but this was no longer the case by late October/early November, with only the lineage AY.6 exhibiting clustering towards the South of England. Conclusions: As SARS-CoV-2 moves towards endemicity and new variants emerge, genomic data obtained from random community samples can augment routine surveillance data without the potential biases introduced due to higher sampling rates of symptomatic individuals.

AB - Background: Since the emergence of SARS-CoV-2, evolutionary pressure has driven large increases in the transmissibility of the virus. However, with increasing levels of immunity through vaccination and natural infection the evolutionary pressure will switch towards immune escape. Genomic surveillance in regions of high immunity is crucial in detecting emerging variants that can more successfully navigate the immune landscape. Methods: We present phylogenetic relationships and lineage dynamics within England (a country with high levels of immunity), as inferred from a random community sample of individuals who provided a self-administered throat and nose swab for rt-PCR testing as part of the REal-time Assessment of Community Transmission-1 (REACT-1) study. During round 14 (9 September–27 September 2021) and 15 (19 October–5 November 2021) lineages were determined for 1322 positive individuals, with 27.1% of those which reported their symptom status reporting no symptoms in the previous month. Results: We identified 44 unique lineages, all of which were Delta or Delta sub-lineages, and found a reduction in their mutation rate over the study period. The proportion of the Delta sub-lineage AY.4.2 was increasing, with a reproduction number 15% (95% CI 8–23%) greater than the most prevalent lineage, AY.4. Further, AY.4.2 was less associated with the most predictive COVID-19 symptoms (p = 0.029) and had a reduced mutation rate (p = 0.050). Both AY.4.2 and AY.4 were found to be geographically clustered in September but this was no longer the case by late October/early November, with only the lineage AY.6 exhibiting clustering towards the South of England. Conclusions: As SARS-CoV-2 moves towards endemicity and new variants emerge, genomic data obtained from random community samples can augment routine surveillance data without the potential biases introduced due to higher sampling rates of symptomatic individuals.

KW - COVID-19

KW - Delta variant

KW - Genetic diversity

KW - Mutation

KW - SARS-CoV-2

KW - Transmission advantage

U2 - 10.1186/s12879-022-07628-4

DO - 10.1186/s12879-022-07628-4

M3 - Article

C2 - 35896970

AN - SCOPUS:85135148943

SN - 1471-2334

VL - 22

JO - BMC Infectious Diseases

JF - BMC Infectious Diseases

M1 - 647

ER -

SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

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