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; The COVID-19 Genomics UK (COG-UK) Consortium; Deborah Ashby; Wendy Barclay; Graham Taylor; Graham Cooke; Helen Ward; Ara Darzi; Steven Riley; Marc Chadeau-Hyam; Christl A Donnelly; Paul Elliott; Darren L. Smith; Matthew Bashton; Gregory R. Young; Clare M. McCann; Andrew Nelson; Matthew R. Crown; John H. Henderson; Amy Hollis; William Stanley; Wen C. Yew

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, The COVID-19 Genomics UK (COG-UK) Consortium, Deborah Ashby, Wendy Barclay, Graham Taylor, Graham Cooke, Helen Ward, Ara Darzi, Steven Riley, Marc Chadeau-Hyam, Christl A Donnelly^*, Paul Elliott^*, Darren L. SmithMatthew Bashton, Gregory R. Young, Clare M. McCann, Andrew Nelson, Matthew R. Crown, John H. Henderson, Amy Hollis, William Stanley, Wen C. Yew

^*Corresponding author for this work

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
Issue number	1
Early online date	27 Jul 2022
DOIs	https://doi.org/10.1186/s12879-022-07628-4
Publication status	Published - Dec 2022

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Eales, O., Page, A. J., de Oliveira Martins, L., Wang, H., Bodinier, B., Haw, D., Jonnerby, J., Atchison, C., The COVID-19 Genomics UK (COG-UK) Consortium, Ashby, D., Barclay, W., Taylor, G., Cooke, G., Ward, H., Darzi, A., Riley, S., Chadeau-Hyam, M., Donnelly, C. A., Elliott, P., ... Yew, W. C. (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(1), [647]. https://doi.org/10.1186/s12879-022-07628-4

@article{2ca79132902a48a7937913bb819ed6b9,

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 {The COVID-19 Genomics UK (COG-UK) Consortium} and Deborah Ashby and Wendy Barclay and Graham Taylor and Graham Cooke and Helen Ward and Ara Darzi and Steven Riley and Marc Chadeau-Hyam and Donnelly, {Christl A} and Paul Elliott and Smith, {Darren L.} and Matthew Bashton and Young, {Gregory R.} and McCann, {Clare M.} and Andrew Nelson and Crown, {Matthew R.} and Henderson, {John H.} and Amy Hollis and William Stanley and Yew, {Wen C.}",

note = "Funding Information: MC-H acknowledges support from the H2020-EXPANSE project (Horizon 2020 Grant No 874627). MC-H and BB acknowledge support from Cancer Research UK, Population Research Committee Project grant 'Mechanomics{\textquoteright} (Grant No 22184 to MC-H). CAD acknowledges support from the MRC Centre for Global Infectious Disease Analysis and National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU). GC is supported by an NIHR Professorship. HW acknowledges support from an NIHR Senior Investigator Award and the Wellcome Trust (205456/Z/16/Z). PE is Director of the Medical Research Council (MRC) Centre for Environment and Health (MR/L01341X/1, MR/S019669/1). PE acknowledges support from Health Data Research UK (HDR UK); the NIHR Imperial Biomedical Research Centre; NIHR Health Protection Research Units in Chemical and Radiation Threats and Hazards, and Environmental Exposures and Health; the British Heart Foundation Centre for Research Excellence at Imperial College London (RE/18/4/34215); and the UK Dementia Research Institute at Imperial College London (MC_PC_17114). AJP acknowledges the support of the Biotechnology and Biological Sciences Research Council (BB/R012504/1). We thank The Huo Family Foundation for their support of our work on COVID-19.",

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",

number = "1",

}

Eales, O, Page, AJ, de Oliveira Martins, L, Wang, H, Bodinier, B, Haw, D, Jonnerby, J, Atchison, C, The COVID-19 Genomics UK (COG-UK) Consortium, Ashby, D, Barclay, W, Taylor, G, Cooke, G, Ward, H, Darzi, A, Riley, S, Chadeau-Hyam, M, Donnelly, CA, Elliott, P, Smith, DL , Bashton, M, Young, GR, McCann, CM , Nelson, A, Crown, MR, Henderson, JH, Hollis, A, Stanley, W & Yew, WC 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, no. 1, 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

T2 - 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 - The COVID-19 Genomics UK (COG-UK) Consortium

AU - Ashby, Deborah

AU - Barclay, Wendy

AU - Taylor, Graham

AU - Cooke, Graham

AU - Ward, Helen

AU - Darzi, Ara

AU - Riley, Steven

AU - Chadeau-Hyam, Marc

AU - Donnelly, Christl A

AU - Elliott, Paul

AU - Smith, Darren L.

AU - Bashton, Matthew

AU - Young, Gregory R.

AU - McCann, Clare M.

AU - Nelson, Andrew

AU - Crown, Matthew R.

AU - Henderson, John H.

AU - Hollis, Amy

AU - Stanley, William

AU - Yew, Wen C.

N1 - Funding Information: MC-H acknowledges support from the H2020-EXPANSE project (Horizon 2020 Grant No 874627). MC-H and BB acknowledge support from Cancer Research UK, Population Research Committee Project grant 'Mechanomics’ (Grant No 22184 to MC-H). CAD acknowledges support from the MRC Centre for Global Infectious Disease Analysis and National Institute for Health Research (NIHR) Health Protection Research Unit (HPRU). GC is supported by an NIHR Professorship. HW acknowledges support from an NIHR Senior Investigator Award and the Wellcome Trust (205456/Z/16/Z). PE is Director of the Medical Research Council (MRC) Centre for Environment and Health (MR/L01341X/1, MR/S019669/1). PE acknowledges support from Health Data Research UK (HDR UK); the NIHR Imperial Biomedical Research Centre; NIHR Health Protection Research Units in Chemical and Radiation Threats and Hazards, and Environmental Exposures and Health; the British Heart Foundation Centre for Research Excellence at Imperial College London (RE/18/4/34215); and the UK Dementia Research Institute at Imperial College London (MC_PC_17114). AJP acknowledges the support of the Biotechnology and Biological Sciences Research Council (BB/R012504/1). We thank The Huo Family Foundation for their support of our work on COVID-19.

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

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U2 - 10.1186/s12879-022-07628-4

DO - 10.1186/s12879-022-07628-4

M3 - Article

C2 - 35896970

AN - SCOPUS:85135148943

VL - 22

JO - BMC Infectious Diseases

JF - BMC Infectious Diseases

SN - 1471-2334

IS - 1

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

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