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; 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

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

BMC Infect Dis. 2022 Jul 27;22(1):647. doi: 10.1186/s12879-022-07628-4.

Authors

Oliver Eales^{1

2}, Andrew J Page³, Leonardo de Oliveira Martins³, Haowei Wang^{1

2}, Barbara Bodinier^{1

4}, David Haw^{1

2}, Jakob Jonnerby^{1

2}, Christina Atchison¹; COVID-19 Genomics UK (COG-UK) Consortium; Deborah Ashby¹, Wendy Barclay⁵, Graham Taylor⁵, Graham Cooke^{5

6

7}, Helen Ward^{1

6

7}, Ara Darzi^{6

7

8}, Steven Riley^{1

2}, Marc Chadeau-Hyam^{1

4}, Christl A Donnelly^{9

10

11}, Paul Elliott^{12

13

14

15

16

17}

Collaborators

COVID-19 Genomics UK (COG-UK) Consortium:
Samuel C Robson, Thomas R Connor, Nicholas J Loman, Tanya Golubchik, Rocio T Martinez Nunez, David Bonsall, Andrew Rambaut, Luke B Snell, Rich Livett, Catherine Ludden, Sally Corden, Eleni Nastouli, Gaia Nebbia, Ian Johnston, Katrina Lythgoe, M Estee Torok, Ian G Goodfellow, Jacqui A Prieto, Kordo Saeed, David K Jackson, Catherine Houlihan, Dan Frampton, William L Hamilton, Adam A Witney, Giselda Bucca, Cassie F Pope, Catherine Moore, Emma C Thomson, Ewan M Harrison, Colin P Smith, Fiona Rogan, Shaun M Beckwith, Abigail Murray, Dawn Singleton, Kirstine Eastick, Liz A Sheridan, Paul Randell, Leigh M Jackson, Cristina V Ariani, Sónia Gonçalves, Derek J Fairley, Matthew W Loose, Joanne Watkins, Samuel Moses, Sam Nicholls, Matthew Bull, Roberto Amato, Darren L Smith, David M Aanensen, Jeffrey C Barrett, Dinesh Aggarwal, James G Shepherd, Martin D Curran, Surendra Parmar, Matthew D Parker, Catryn Williams, Sharon Glaysher, Anthony P Underwood, Matthew Bashton, Nicole Pacchiarini, Katie F Loveson, Matthew Byott, Alessandro M Carabelli, Kate E Templeton, Thushan I de Silva, Dennis Wang, Cordelia F Langford, John Sillitoe, Rory N Gunson, Simon Cottrell, Justin O'Grady, Dominic Kwiatkowski, Patrick J Lillie, Nicholas Cortes, Nathan Moore, Claire Thomas, Phillipa J Burns, Tabitha W Mahungu, Steven Liggett, Angela H Beckett, Matthew T G Holden, Lisa J Levett, Husam Osman, Mohammed O Hassan-Ibrahim, David A Simpson, Meera Chand, Ravi K Gupta, Alistair C Darby, Steve Paterson, Oliver G Pybus, Erik M Volz, Daniela de Angelis, David L Robertson, Inigo Martincorena, Louise Aigrain, Andrew R Bassett, Nick Wong, Yusri Taha, Michelle J Erkiert, Michael H Spencer Chapman, Rebecca Dewar, Martin P McHugh, Siddharth Mookerjee, Stephen Aplin, Matthew Harvey, Thea Sass, Helen Umpleby, Helen Wheeler, James P McKenna, Ben Warne, Joshua F Taylor, Yasmin Chaudhry, Rhys Izuagbe, Aminu S Jahun, Gregory R Young, Claire McMurray, Clare M McCann, Andrew Nelson, Scott Elliott, Hannah Lowe, Anna Price, Matthew R Crown, Sara Rey, Sunando Roy, Ben Temperton, Sharif Shaaban, Andrew R Hesketh, Kenneth G Laing, Irene M Monahan, Judith Heaney, Emanuela Pelosi, Siona Silviera, Eleri Wilson-Davies, Helen Fryer, Helen Adams, Louis du Plessis, Rob Johnson, William T Harvey, Joseph Hughes, Richard J Orton, Lewis G Spurgin, Yann Bourgeois, Chris Ruis, Áine O'Toole, Marina Gourtovaia, Theo Sanderson, Christophe Fraser, Jonathan Edgeworth, Judith Breuer, Stephen L Michell, John A Todd, Michaela John, David Buck, Kavitha Gajee, Gemma L Kay, Sharon J Peacock, David Heyburn, Katie Kitchman, Alan McNally, David T Pritchard, Samir Dervisevic, Peter Muir, Esther Robinson, Barry B Vipond, Newara A Ramadan, Christopher Jeanes, Danni Weldon, Jana Catalan, Neil Jones, Ana da Silva Filipe, Chris Williams, Marc Fuchs, Julia Miskelly, Aaron R Jeffries, Karen Oliver, Naomi R Park, Amy Ash, Cherian Koshy, Magdalena Barrow, Sarah L Buchan, Anna Mantzouratou, Gemma Clark, Christopher W Holmes, Sharon Campbell, Thomas Davis, Ngee Keong Tan, Julianne R Brown, Kathryn A Harris, Stephen P Kidd, Paul R Grant, Li Xu-McCrae, Alison Cox, Pinglawathee Madona, Marcus Pond, Paul A Randell, Karen T Withell, Cheryl Williams, Clive Graham, Rebecca Denton-Smith, Emma Swindells, Robyn Turnbull, Tim J Sloan, Andrew Bosworth, Stephanie Hutchings, Hannah M Pymont, Anna Casey, Liz Ratcliffe, Christopher R Jones, Bridget A Knight, Tanzina Haque, Jennifer Hart, Dianne Irish-Tavares, Eric Witele, Craig Mower, Louisa K Watson, Jennifer Collins, Gary Eltringham, Dorian Crudgington, Ben Macklin, Miren Iturriza-Gomara, Anita O Lucaci, Patrick C McClure, Matthew Carlile, Nadine Holmes, Christopher Moore, Nathaniel Storey, Stefan Rooke, Gonzalo Yebra, Noel Craine, Malorie Perry, Nabil-Fareed Alikhan, Stephen Bridgett, Kate F Cook, Christopher Fearn, Salman Goudarzi, Ronan A Lyons, Thomas Williams, Sam T Haldenby, Jillian Durham, Steven Leonard, Robert M Davies, Rahul Batra, Beth Blane, Moira J Spyer, Perminder Smith, Mehmet Yavus, Rachel J Williams, Adhyana I K Mahanama, Buddhini Samaraweera, Sophia T Girgis, Samantha E Hansford, Angie Green, Charlotte Beaver, Katherine L Bellis, Matthew J Dorman, Sally Kay, Liam Prestwood, Shavanthi Rajatileka, Joshua Quick, Radoslaw Poplawski, Nicola Reynolds, Andrew Mack, Arthur Morriss, Thomas Whalley, Bindi Patel, Iliana Georgana, Myra Hosmillo, Malte L Pinckert, Joanne Stockton, John H Henderson, Amy Hollis, William Stanley, Wen C Yew, Richard Myers, Alicia Thornton, Alexander Adams, Tara Annett, Hibo Asad, Alec Birchley, Jason Coombes, Johnathan M Evans, Laia Fina, Bree Gatica-Wilcox, Lauren Gilbert, Lee Graham, Jessica Hey, Ember Hilvers, Sophie Jones, Hannah Jones, Sara Kumziene-Summerhayes, Caoimhe McKerr, Jessica Powell, Georgia Pugh, Sarah Taylor, Alexander J Trotter, Charlotte A Williams, Leanne M Kermack, Benjamin H Foulkes, Marta Gallis, Hailey R Hornsby, Stavroula F Louka, Manoj Pohare, Paige Wolverson, Peijun Zhang, George MacIntyre-Cockett, Amy Trebes, Robin J Moll, Lynne Ferguson, Emily J Goldstein, Alasdair Maclean, Rachael Tomb, Igor Starinskij, Laura Thomson, Joel Southgate, Moritz U G Kraemer, Jayna Raghwani, Alex E Zarebski, Olivia Boyd, Lily Geidelberg, Chris J Illingworth, Chris Jackson, David Pascall, Sreenu Vattipally, Timothy M Freeman, Sharon N Hsu, Benjamin B Lindsey, Keith James, Kevin Lewis, Gerry Tonkin-Hill, Jaime M Tovar-Corona, MacGregor Cox, Khalil Abudahab, Mirko Menegazzo, Ben E W Taylor MEng, Corin A Yeats, Afrida Mukaddas, Derek W Wright, Rachel Colquhoun, Verity Hill, Ben Jackson, J T McCrone, Nathan Medd, Emily Scher, Jon-Paul Keatley, Tanya Curran, Sian Morgan, Patrick Maxwell, Ken Smith, Sahar Eldirdiri, Anita Kenyon, Alison H Holmes, James R Price, Tim Wyatt, Alison E Mather, Timofey Skvortsov, John A Hartley, Martyn Guest, Christine Kitchen, Ian Merrick, Robert Munn, Beatrice Bertolusso, Jessica Lynch, Gabrielle Vernet, Stuart Kirk, Elizabeth Wastnedge, Rachael Stanley, Giles Idle, Declan T Bradley, Jennifer Poyner, Matilde Mori, Owen Jones, Victoria Wright, Ellena Brooks, Carol M Churcher, Mireille Fragakis, Katerina Galai, Andrew Jermy, Sarah Judges, Georgina M McManus, Kim S Smith, Elaine Westwick, Stephen W Attwood, Frances Bolt, Alisha Davies, Elen De Lacy, Fatima Downing, Sue Edwards, Lizzie Meadows, Sarah Jeremiah, Nikki Smith, Luke Foulser, Themoula Charalampous, Amita Patel, Louise Berry, Tim Boswell, Vicki M Fleming, Hannah C Howson-Wells, Amelia Joseph, Manjinder Khakh, Michelle M Lister, Paul W Bird, Karlie Fallon, Thomas Helmer, Claire L McMurray, Mina Odedra, Jessica Shaw, Julian W Tang, Nicholas J Willford, Victoria Blakey, Veena Raviprakash, Nicola Sheriff, Lesley-Anne Williams, Theresa Feltwell, Luke Bedford, James S Cargill, Warwick Hughes, Jonathan Moore, Susanne Stonehouse, Laura Atkinson, Jack C D Lee, Divya Shah, Adela Alcolea-Medina, Natasha Ohemeng-Kumi, John Ramble, Jasveen Sehmi, Rebecca Williams, Wendy Chatterton, Monika Pusok, William Everson, Anibolina Castigador, Emily Macnaughton, Kate El Bouzidi, Temi Lampejo, Malur Sudhanva, Cassie Breen, Graciela Sluga, Shazaad S Y Ahmad, Ryan P George, Nicholas W Machin, Debbie Binns, Victoria James, Rachel Blacow, Lindsay Coupland, Louise Smith, Edward Barton, Debra Padgett, Garren Scott, Aidan Cross, Mariyam Mirfenderesky, Jane Greenaway, Kevin Cole, Phillip Clarke, Nichola Duckworth, Sarah Walsh, Kelly Bicknell, Robert Impey, Sarah Wyllie, Richard Hopes, Chloe Bishop, Vicki Chalker, Ian Harrison, Laura Gifford, Zoltan Molnar, Cressida Auckland, Cariad Evans, Kate Johnson, David G Partridge, Mohammad Raza, Paul Baker, Stephen Bonner, Sarah Essex, Leanne J Murray, Andrew I Lawton, Shirelle Burton-Fanning, Brendan A I Payne, Sheila Waugh, Andrea N Gomes, Maimuna Kimuli, Darren R Murray, Paula Ashfield, Donald Dobie, Fiona Ashford, Angus Best, Liam Crawford, Nicola Cumley, Megan Mayhew, Oliver Megram, Jeremy Mirza, Emma Moles-Garcia, Benita Percival, Megan Driscoll, Leah Ensell, Helen L Lowe, Laurentiu Maftei, Matteo Mondani, Nicola J Chaloner, Benjamin J Cogger, Lisa J Easton, Hannah Huckson, Jonathan Lewis, Sarah Lowdon, Cassandra S Malone, Florence Munemo, Manasa Mutingwende, Roberto Nicodemi, Olga Podplomyk, Thomas Somassa, Andrew Beggs, Alex Richter, Claire Cormie, Joana Dias, Sally Forrest, Ellen E Higginson, Mailis Maes, Jamie Young, Rose K Davidson, Kathryn A Jackson, Lance Turtle, Alexander J Keeley, Jonathan Ball, Timothy Byaruhanga, Joseph G Chappell, Jayasree Dey, Jack D Hill, Emily J Park, Arezou Fanaie, Rachel A Hilson, Geraldine Yaze, Stephanie Lo, Safiah Afifi, Robert Beer, Joshua Maksimovic, Kathryn McCluggage, Karla Spellman, Catherine Bresner, William Fuller, Angela Marchbank, Trudy Workman, Ekaterina Shelest, Johnny Debebe, Fei Sang, Marina Escalera Zamudio, Sarah Francois, Bernardo Gutierrez, Tetyana I Vasylyeva, Flavia Flaviani, Manon Ragonnet-Cronin, Katherine L Smollett, Alice Broos, Daniel Mair, Jenna Nichols, Kyriaki Nomikou, Lily Tong, Ioulia Tsatsani, Prof Sarah O'Brien, Steven Rushton, Roy Sanderson, Jon Perkins, Seb Cotton, Abbie Gallagher, Elias Allara, Clare Pearson, David Bibby, Gavin Dabrera, Nicholas Ellaby, Eileen Gallagher, Jonathan Hubb, Angie Lackenby, David Lee, Nikos Manesis, Tamyo Mbisa, Steven Platt, Katherine A Twohig, Mari Morgan, Alp Aydin, David J Baker, Ebenezer Foster-Nyarko, Sophie J Prosolek, Steven Rudder, Chris Baxter, Sílvia F Carvalho, Deborah Lavin, Arun Mariappan, Clara Radulescu, Aditi Singh, Miao Tang, Helen Morcrette, Nadua Bayzid, Marius Cotic, Carlos E Balcazar, Michael D Gallagher, Daniel Maloney, Thomas D Stanton, Kathleen A Williamson, Robin Manley, Michelle L Michelsen, Christine M Sambles, David J Studholme, Joanna Warwick-Dugdale, Richard Eccles, Matthew Gemmell, Richard Gregory, Margaret Hughes, Charlotte Nelson, Lucille Rainbow, Edith E Vamos, Hermione J Webster, Mark Whitehead, Claudia Wierzbicki, Adrienn Angyal, Luke R Green, Max Whiteley, Emma Betteridge, Iraad F Bronner, Ben W Farr, Scott Goodwin, Stefanie V Lensing, Shane A McCarthy, Michael A Quail, Diana Rajan, Nicholas M Redshaw, Carol Scott, Lesley Shirley, Scott A J Thurston, Will Rowe, Amy Gaskin, Thanh Le-Viet, James Bonfield, Jennifier Liddle, Andrew Whitwham

Affiliations

¹ School of Public Health, Imperial College London, Norfolk Place, London, W2 1PG, UK.
² MRC Centre for Global Infectious Disease Analysis and Jameel Institute, Imperial College London, London, UK.
³ Quadram Institute, Norwich, UK.
⁴ MRC Centre for Environment and Health, School of Public Health, Imperial College London, London, UK.
⁵ Department of Infectious Disease, Imperial College London, London, UK.
⁶ Imperial College Healthcare NHS Trust, London, UK.
⁷ National Institute for Health Research Imperial Biomedical Research Centre, London, UK.
⁸ Institute of Global Health Innovation, Imperial College London, London, UK.
⁹ School of Public Health, Imperial College London, Norfolk Place, London, W2 1PG, UK. [email protected].
¹⁰ MRC Centre for Global Infectious Disease Analysis and Jameel Institute, Imperial College London, London, UK. [email protected].
¹¹ Department of Statistics, University of Oxford, Oxford, UK. [email protected].
¹² School of Public Health, Imperial College London, Norfolk Place, London, W2 1PG, UK. [email protected].
¹³ MRC Centre for Global Infectious Disease Analysis and Jameel Institute, Imperial College London, London, UK. [email protected].
¹⁴ Imperial College Healthcare NHS Trust, London, UK. [email protected].
¹⁵ National Institute for Health Research Imperial Biomedical Research Centre, London, UK. [email protected].
¹⁶ Health Data Research (HDR) UK, Imperial College London, London, UK. [email protected].
¹⁷ UK Dementia Research Institute Centre at Imperial, Imperial College London, London, UK. [email protected].

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.

MeSH terms

COVID-19* / epidemiology
England / epidemiology
Humans
Phylogeny
SARS-CoV-2* / genetics

Abstract

MeSH terms

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