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SARS-CoV-2 evolution during treatment of chronic infection
Open accessPublished version of a preprint
Abstract
The spike protein of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is critical for virus infection through the engagement of the human ACE2 protein 1 and is a major antibody target. Here we show that chronic infection with SARS-CoV-2 leads to viral evolution and reduced sensitivity to neutralizing antibodies in an immunosuppressed individual treated with convalescent plasma, by generating whole-genome ultra-deep sequences for 23 time points that span 101 days and using in vitro techniques to characterize the mutations revealed by sequencing. There was little change in the overall structure of the viral population after two courses of remdesivir during the first 57 days. However, after convalescent plasma therapy, we observed large, dynamic shifts in the viral population, with the emergence of a dominant viral strain that contained a substitution (D796H) in the S2 subunit and a deletion (ΔH69/ΔV70) in the S1 N-terminal domain of the spike protein. As passively transferred serum antibodies diminished, viruses with the escape genotype were reduced in frequency, before returning during a final, unsuccessful course of convalescent plasma treatment. In vitro, the spike double mutant bearing both ΔH69/ΔV70 and D796H conferred modestly decreased sensitivity to convalescent plasma, while maintaining infectivity levels that were similar to the wild-type virus.The spike substitution mutant D796H appeared to be the main contributor to the decreased susceptibility to neutralizing antibodies, but this mutation resulted in an infectivity defect. The spike deletion mutant ΔH69/ΔV70 had a twofold higher level of infectivity than wild-type SARS-CoV-2, possibly compensating for the reduced infectivity of the D796H mutation. These data reveal strong selection on SARS-CoV-2 during convalescent plasma therapy, which is associated with the emergence of viral variants that show evidence of reduced susceptibility to neutralizing antibodies in immunosuppressed individuals.
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“The possible theories about the origin of novel variants are the evolution of circulating intermediate mutants in the chronically infected immunocompromised patients supporting high viral replication while on treatment with immune plasma or monoclonal antibodies [88, 89].”
From Waves and variants of SARS-CoV-2: understanding the causes and effect of the COVID-19 catastrophe (2022) · cites this paper as [89]
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In the citing paper
“Previous studies showed that the binding affinity of SARS-CoV for human ACE2 correlated with the rate of viral replication in distinct species, transmissibility and disease severity 29–31.”
From Sensitivity of SARS-CoV-2 B.1.1.7 to mRNA vaccine-elicited antibodies (2021) · cites this paper as [31]
Experimental — accuracy not yet measuredIn the citing paper
“The recent emergence of B.1.1.7,B.1.351and P.1 marks the beginning of SARS-CoV-2 antigenic drift.”
From Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7 (2021) · cites this paper as [44]
In the citing paper
“Interestingly, repeated use of plasma therapy in an immunocompromised individual led to the transient emergence of the N501Y mutation as well as the 69–70 deletion in the NTD, which is characteristic of B.1.1.7 (Kemp et al., 2021).”
From Evidence of escape of SARS-CoV-2 variant B.1.351 from natural and vaccine-induced sera (2021) · cites this paper as Kemp et al., 2021
In the citing paper
“The B.1.1.7 variant emerged in the United Kingdom, the B.1.351variant (also termed 501Y.V2) in South Africa and the P.1 and P.2 lineages in Brazil 2,3,5,9-12 .”
From Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies (2021) · cites this paper as [3]
In the citing paper
“Although distinct, the variants share common characteristics, including known escape mutations that were previously identified under antibody pressure selection in vitro 2,3,[13][14][15][16][17] .”
From Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies (2021) · cites this paper as [3]
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“Pre-outbreak Omicron mutations also overlapped with some mutations detected in isolates from chronically infected patients (Kemp et al., 2021; Truong et al., 2021); however, they too showed substantially lower odds ratios and significance levels than those isolated from mice (Fig.”
InfluentialAn infectivity-enhancing site on the SARS-CoV-2 spike protein targeted by antibodies
Liu, Y., Soh, W. T., Kishikawa, J.-I., Hirose, M., Nakayama, E. E., Li, S., Sasai, M., Suzuki, T., Tada, A., Arakawa, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.05.032 · Cited by 277
“Recent studies have suggested that H69-V70 deletion increases infectivity of SARS-CoV-2 (Kemp et al., 2021).”
BackgroundThe total number and mass of SARS-CoV-2 virions
Sender, R., Bar‐On, Y. M., Gleizer, S., Bernshtein, B., Flamholz, A. I., Phillips, R., & Milo, R. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2024815118 · Cited by 292
“As such, our best estimate for the size of the pool of cell types that SARS-CoV-2 likely infects is thus ∼ 10 11 cells, and the number of cells infected during peak infection therefore represents a small fraction of this potential pool (one in 10 5 to 10 7 ).”
A human coronavirus evolves antigenically to escape antibody immunity
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“Although tremendous efforts have been made in vaccine development and COVID-19 therapeutics, including mAbs and COVID-19 pills by Merck, the emergence of VOCs has raised concerns over the efficacy of neutralizing antibodies (21, 22).”
BackgroundBroadly neutralizing antibodies overcome SARS-CoV-2 Omicron antigenic shift
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“and 90% after three doses has been reported, indicating the rise of protection due to booster vaccine shots which may be due to restoring and increasing the levels of neutralizing antibodies [70,96].”
BackgroundMonoclonal antibodies for COVID-19 therapy and SARS-CoV-2 detection
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SARS-CoV-2 prolonged infection during advanced HIV disease evolves extensive immune escape
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Immune responses to two and three doses of the BNT162b2 mRNA vaccine in adults with solid tumors
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Recurrent emergence and transmission of a SARS-CoV-2 spike deletion H69/V70
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Self-citationThe effect of spike mutations on SARS-CoV-2 neutralization
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InfluentialSelf-citationWaves and variants of SARS-CoV-2: understanding the causes and effect of the COVID-19 catastrophe
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Self-citationThe Impact of Evolving SARS-CoV-2 Mutations and Variants on COVID-19 Vaccines
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Self-citationImmune Evasion of SARS-CoV-2 Emerging Variants: What Have We Learnt So Far?
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COVID-19: Unmasking Emerging SARS-CoV-2 Variants, Vaccines and Therapeutic Strategies
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Public health actions to control new SARS-CoV-2 variants
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SARS-CoV-2 gene content and COVID-19 mutation impact by comparing 44 Sarbecovirus genomes
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The Evolution and Biology of SARS-CoV-2 VariantsPreprint
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Epidemic spreading on higher-order networks
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SARS-CoV-2 B.1.617 Mutations L452R and E484Q Are Not Synergistic for Antibody Evasion
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Self-citationResistance Mutations in SARS-CoV-2 Delta Variant after Sotrovimab Use
Rockett, R. J., Basile, K., Maddocks, S., Fong, W., Agius, J. E., Johnson-Mackinnon, J., Arnott, A., Chandra, S., Gall, M., Draper, J. L., et al. (2022) · New England Journal of Medicine · doi:10.1056/nejmc2120219 · Cited by 171
Prolonged evolution of the human B cell response to SARS-CoV-2 infection
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In vitro selection of Remdesivir resistance suggests evolutionary predictability of SARS-CoV-2
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“, [31] SARS-CoV2 virus was never cleared or suppressed by any of the multiple treatments used and they speculated that a V157 mutation may be responsible for the resistance.”
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SARS-CoV-2 one year on: evidence for ongoing viral adaptation
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Self-citationSARS-CoV-2 can recruit a heme metabolite to evade antibody immunity
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Self-citationEfficacy of the BNT162b2 mRNA COVID-19 vaccine in patients with B-cell non-Hodgkin lymphoma
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“NTD deletions, including D H69/V70 (Kemp et al., 2021) and D 141–144 (Avanzato et al., 2020; Choi et al., 2020; McCarthy et al., 2021), have been observed in immunocompromised individuals who remain infected for extended periods.”
InfluentialSelf-citationCompensatory epistasis maintains ACE2 affinity in SARS-CoV-2 Omicron BA.1
Moulana, A., Dupic, T., Phillips, A. M., Chang, J., Nieves, S., Roffler, A. A., Greaney, A. J., Starr, T. N., Bloom, J. D., & Desai, M. M. (2022) · Nature Communications · doi:10.1038/s41467-022-34506-z · Cited by 156
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SARS-CoV-2-neutralising monoclonal antibodies for treatment of COVID-19
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Self-citationEvolutionary trajectory of SARS-CoV-2 and emerging variants
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Metadata
- Authors
- Kemp, S. A., Collier, D. A., Datir, R. P., Ferreira, I. A. T. M., Gayed, S., Jahun, A., Hosmillo, M., Rees-Spear, C., Mlcochova, P., Lumb, I. U., Roberts, D. J., Chandra, A., Temperton, N., The CITIID-NIHR BioResource COVID-19 Collaboration, Principal investigators, Baker, S., Dougan, G., Hess, C., Kingston, N., Lehner, P. J., Lyons, P. A., Matheson, N. J., Owehand, W. H., Saunders, C., Summers, C., Thaventhiran, J. E. D., Toshner, M., Weekes, M. P., nurses, C. &. V. R., Bucke, A., Calder, J., Canna, L., Domingo, J., Elmer, A., Fuller, S., Harris, J., Hewitt, S., Kennet, J., Jose, S., Kourampa, J., Meadows, A., O’Brien, C., Price, J., Publico, C., Rastall, R., Ribeiro, C., Rowlands, J., Ruffolo, V., Tordesillas, H., logistics, S., Bullman, B., Dunmore, B. J., Fawke, S., Gräf, S., Hodgson, J., Huang, C., Hunter, K., Jones, E., Legchenko, E., Matara, C., Martin, J., Mescia, F., O’Donnell, C., Pointon, L., Pond, N., Shih, J., Sutcliffe, R., Tilly, T., Treacy, C., Tong, Z., Wood, J., Wylot, M., acquisition, S. P. &. D., Bergamaschi, L., Betancourt, A., Bower, G., Cossetti, C., De Sa, A., Epping, M., Fawke, S., Gleadall, N., Grenfell, R., Hinch, A., Huhn, O., Jackson, S., Jarvis, I., Lewis, D., Marsden, J., Nice, F., Okecha, G., Omarjee, O., Perera, M., Richoz, N., Romashova, V., Yarkoni, N. S., Sharma, R., Stefanucci, L., Stephens, J., Strezlecki, M., Turner, L., collection, C. D., De Bie, E. M. D. D., Bunclark, K., Josipovic, M., Mackay, M., Rossi, S., Selvan, M., Spencer, S., Yong, C., Royal Papworth Hospital, I. C. U., Ansaripour, A., Michael, A., Mwaura, L., Patterson, C., Polwarth, G., Addenbrooke’s Hospital, I. C. U., Polgarova, P., di Stefano, G., Cambridge & Peterborough Foundation Trust, Fahey, C., Michel, R., ANPC & Centre for Molecular Medicine & Innovative Therapeutics, Bong, S.-H., Coudert, J. D., Holmes, E., BioResource, N., Allison, J., Butcher, H., Caputo, D., Clapham-Riley, D., Dewhurst, E., Furlong, A., Graves, B., Gray, J., Ivers, T., Kasanicki, M., Le Gresley, E., Linger, R., Meloy, S., Muldoon, F., Ovington, N., Papadia, S., Phelan, I., Stark, H., Stirrups, K. E., Townsend, P., Walker, N., Webster, J., The COVID-19 Genomics UK (COG-UK) Consortium, Funding acquisition, L. &. S., Robson, S. C., Funding acquisition, L. &. S., Loman, N. J., Connor, T. R., Leadership & supervision, M. C., Golubchik, T., Funding acquisition, M. C., Martinez Nunez, R. T., Funding acquisition, L. &. S., Ludden, C., Funding acquisition, L. &. S., Corden, S., Funding acquisition, L. &. S., Johnston, I., Bonsall, D., Funding acquisition, L. &. S., Smith, C. P., Awan, A. R., Funding acquisition, S. &. L., Bucca, G., Leadership & supervision, M. C., Estee Torok, M., Leadership & supervision, M. C., Saeed, K., Prieto, J. A., Leadership & supervision, M. C., Jackson, D. K., Metadata curation, P. A., Hamilton, W. L., Metadata curation, P. A., Snell, L. B., Funding acquisition, L. &. S., Moore, C., Funding acquisition, L. &. S., Harrison, E. M., Leadership & supervision, M. C., Goncalves, S., Leadership & supervision, M. C., Fairley, D. J., Loose, M. W., Watkins, J., Leadership & supervision, M. C., Livett, R., Leadership & supervision, M. C., Moses, S., Leadership & supervision, M. C., Amato, R., Nicholls, S., Bull, M., Leadership & supervision, P. A., Smith, D. L., Leadership & supervision, S. &. A., Barrett, J., Aanensen, D. M., Metadata curation, P. A., Curran, M. D., Parmar, S., Aggarwal, D., Shepherd, J. G., Metadata curation, P. A., Parker, M. D., Metadata curation, S. &. L., Glaysher, S., Metadata curation, S. &. A., Bashton, M., Underwood, A. P., Pacchiarini, N., Loveson, K. F., Project administration, S. &. A., Carabelli, A. M., Funding acquisition, L. &. S. A. M. C., Templeton, K. E., Funding acquisition, L. &. S. A. P. A., Langford, C. F., Sillitoe, J., de Silva, T. I., Wang, D., Funding acquisition, L. &. S. A. S. &. A., Kwiatkowski, D., Rambaut, A., O’Grady, J., Cottrell, S., Leadership & supervision, M. C. A. S. &. A., Holden, M. T. G., Thomson, E. C., Leadership & supervision, P. A. A. S. &. L., Osman, H., Andersson, M., Chauhan, A. J., Hassan-Ibrahim, M. O., Leadership & supervision, P. A. A. S. &. A., Lawniczak, M., Leadership & supervision, S. &. L. A. S. &. A., Alderton, A., Chand, M., Constantinidou, C., Unnikrishnan, M., Darby, A. C., Hiscox, J. A., Paterson, S., Leadership & supervision, S. &. A. A. S. &. A. T., Martincorena, I., Robertson, D. L., Volz, E. M., Page, A. J., Pybus, O. G., Leadership & supervision, S. &. A. A. V., Bassett, A. R., Metadata curation, P. A. A. S. &. L., Ariani, C. V., Spencer Chapman, M. H., Li, K. K., Shah, R. N., Jesudason, N. G., Taha, Y., Metadata curation, P. A. A. S. &. A., McHugh, M. P., Dewar, R., Metadata curation, S. &. L. A. S. &. A., Jahun, A. S., McMurray, C., Pandey, S., McKenna, J. P., Nelson, A., Young, G. R., McCann, C. M., Elliott, S., Metadata curation, S. &. L. A. V., Lowe, H., Metadata curation, S. &. A. A. S. &. A. T., Temperton, B., Roy, S., Price, A., Rey, S., Wyles, M., Metadata curation, S. &. A. A. V., Rooke, S., Shaaban, S., Project administration, S. &. L. A. S. &. A., de Cesare, M., Project administration, S. &. L. A. S. &. A. T., Letchford, L., Project administration, S. &. L. A. V., Silveira, S., Pelosi, E., Wilson-Davies, E., Samples & logistics, S. &. A. A. S. &. A. T., Hosmillo, M., Sequencing & analysis, S. &. A. T. A. V., O’Toole, Á., Hesketh, A. R., Stark, R., du Plessis, L., Ruis, C., Adams, H., Bourgeois, Y., supervision, F. A. A. L. &., Michell, S. L., Grammatopoulos, D., Edgeworth, J., Breuer, J., Todd, J. A., Fraser, C., Funding acquisition and project administration, Buck, D., John, M., curation, L. &. S. A. M., Kay, G. L., Leadership & supervision and project administration, Palmer, S., Peacock, S. J., Heyburn, D., logistics, L. &. S. A. S. &., Weldon, D., Robinson, E., McNally, A., Muir, P., Vipond, I. B., Boyes, J., Sivaprakasam, V., Salluja, T., Dervisevic, S., Meader, E. J., analysis, L. &. S. A. S. &., Park, N. R., Oliver, K., Jeffries, A. R., Ott, S., da Silva Filipe, A., Simpson, D. A., Williams, C., visualization, L. &. S. A., Masoli, J. A. H., logistics, M. C. A. S. &., Knight, B. A., Jones, C. R., Koshy, C., Ash, A., Casey, A., Bosworth, A., Ratcliffe, L., Xu-McCrae, L., Pymont, H. M., Hutchings, S., Berry, L., Jones, K., Halstead, F., Davis, T., Holmes, C., Iturriza-Gomara, M., Lucaci, A. O., Randell, P. A., Cox, A., Madona, P., Harris, K. A., Brown, J. R., Mahungu, T. W., Irish-Tavares, D., Haque, T., Hart, J., Witele, E., Fenton, M. 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M., Ellard, S., Auckland, C., Harrison, I., Bishop, C., Chalker, V., Richter, A., Beggs, A., Best, A., Percival, B., Mirza, J., Megram, O., Mayhew, M., Crawford, L., Ashcroft, F., Moles-Garcia, E., Cumley, N., Hopes, R., Asamaphan, P., Niebel, M. O., Gunson, R. N., Bradley, A., Maclean, A., Mollett, G., Blacow, R., Bird, P., Helmer, T., Fallon, K., Tang, J., Hale, A. D., Macfarlane-Smith, L. R., Harper, K. L., Carden, H., Machin, N. W., Jackson, K. A., Ahmad, S. S. Y., George, R. P., Turtle, L., O’Toole, E., Watts, J., Breen, C., Cowell, A., Alcolea-Medina, A., Charalampous, T., Patel, A., Levett, L. J., Heaney, J., Rowan, A., Taylor, G. P., Shah, D., Atkinson, L., Lee, J. C. D., Westhorpe, A. P., Jannoo, R., Lowe, H. L., Karamani, A., Ensell, L., Chatterton, W., Pusok, M., Dadrah, A., Symmonds, A., Sluga, G., Molnar, Z., Baker, P., Bonner, S., Essex, S., Barton, E., Padgett, D., Scott, G., Greenaway, J., Payne, B. A. I., Burton-Fanning, S., Waugh, S., Raviprakash, V., Sheriff, N., Blakey, V., Williams, L.-A., Moore, J., Stonehouse, S., Smith, L., Davidson, R. K., Bedford, L., Coupland, L., Wright, V., Chappell, J. G., Tsoleridis, T., Ball, J., Khakh, M., Fleming, V. M., Lister, M. M., Howson-Wells, H. C., Berry, L., Boswell, T., Joseph, A., Willingham, I., Duckworth, N., Walsh, S., Wise, E., Moore, N., Mori, M., Cortes, N., Kidd, S., Williams, R., Gifford, L., Bicknell, K., Wyllie, S., Lloyd, A., Impey, R., Malone, C. S., Cogger, B. J., Levene, N., Monaghan, L., Keeley, A. J., Partridge, D. G., Raza, M., Evans, C., Johnson, K., Abnizova, I., Aigrain, L., Alderton, A., Ali, M., Allen, L., Amato, R., Anderson, R., Ariani, C., Austin-Guest, S., Bala, S., Barrett, J., Bassett, A., Battleday, K., Beal, J., Beale, M., Beaver, C., Bellany, S., Bellerby, T., Bellis, K., Berger, D., Berriman, M., Betteridge, E., Bevan, P., Binley, S., Bishop, J., Blackburn, K., Bonfield, J., Boughton, N., Bowker, S., Brendler-Spaeth, T., Bronner, I., Brooklyn, T., Buddenborg, S. K., Bush, R., Caetano, C., Cagan, A., Carter, N., Cartwright, J., Monteiro, T. 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J., Johnston, I., Jones, M., Kallepally, K., Kane, L., Kay, K., Kay, S., Keatley, J., Keith, A., King, A., Kitchin, L., Kleanthous, M., Klimekova, M., Korlevic, P., Krasheninnkova, K., Kwiatkowski, D., Lane, G., Langford, C., Laverack, A., Law, K., Lawniczak, M., Lensing, S., Leonard, S., Letchford, L., Lewis, K., Lewis-Wade, A., Liddle, J., Lin, Q., Lindsay, S., Linsdell, S., Livett, R., Lo, S., Long, R., Lovell, J., Lovell, J., Ludden, C., Mack, J., Maddison, M., Makunin, A., Mamun, I., Mansfield, J., Marriott, N., Martin, M., Martincorena, I., Mayho, M., McCarthy, S., McClintock, J., McGuigan, S., McHugh, S., McMinn, L., Meadows, C., Mobley, E., Moll, R., Morra, M., Morrow, L., Murie, K., Nash, S., Nathwani, C., Naydenova, P., Neaverson, A., Nelson, R., Nerou, E., Nicholson, J., Nimz, T., Noell, G. G., O’Meara, S., Ohan, V., Oliver, K., Olney, C., Ormond, D., Oszlanczi, A., Palmer, S., Pang, Y. F., Pardubska, B., Park, N., Parmar, A., Patel, G., Patel, M., Payne, M., Peacock, S., Petersen, A., Plowman, D., Preston, T., Prestwood, L., Puethe, C., Quail, M., Rajan, D., Rajatileka, S., Rance, R., Rawlings, S., Redshaw, N., Reynolds, J., Reynolds, M., Rice, S., Richardson, M., Roberts, C., Robinson, K., Robinson, M., Robinson, D., Rogers, H., Rojo, E. M., Roopra, D., Rose, M., Rudd, L., Sadri, R., Salmon, N., Saul, D., Schwach, F., Scott, C., Seekings, P., Shirley, L., Sillitoe, J., Simms, A., Sinnott, M., Sivadasan, S., Siwek, B., Sizer, D., Skeldon, K., Skelton, J., Slater-Tunstill, J., Sloper, L., Smerdon, N., Smith, C., Smith, C., Smith, J., Smith, K., Smith, M., Smith, S., Smith, T., Sneade, L., Soria, C. D., Sousa, C., Souster, E., Sparkes, A., Spencer-Chapman, M., Squares, J., Stanley, R., Steed, C., Stickland, T., Still, I., Stratton, M., Strickland, M., Swann, A., Swiatkowska, A., Sycamore, N., Swift, E., Symons, E., Szluha, S., Taluy, E., Tao, N., Taylor, K., Taylor, S., Thompson, S., Thompson, M., Thomson, M., Thomson, N., Thurston, S., Tonkin-Hill, G., Toombs, D., Topping, B., Tovar-Corona, J., Ungureanu, D., Uphill, J., Urbanova, J., Jansen Van, P., Vancollie, V., Voak, P., Walker, D., Walker, M., Waller, M., Ward, G., Weatherhogg, C., Webb, N., Weldon, D., Wells, A., Wells, E., Westwood, L., Whipp, T., Whiteley, T., Whitton, G., Whitwham, A., Widaa, S., Williams, M., Wilson, M., Wright, S., analysis, S. &., Betteridge, E., Farr, B. W., Goodwin, S., Quail, M. A., Scott, C., Shirley, L., Thurston, S. A. J., Rajan, D., Bronner, I. F., Aigrain, L., Redshaw, N. M., Lensing, S. V., McCarthy, S., Makunin, A., Balcazar, C. E., Gallagher, M. D., Williamson, K. A., Stanton, T. D., Michelsen, M. L., Warwick-Dugdale, J., Manley, R., Farbos, A., Harrison, J. W., Sambles, C. M., Studholme, D. J., Lackenby, A., Mbisa, T., Platt, S., Miah, S., Bibby, D., Manso, C., Hubb, J., Dabrera, G., Ramsay, M., Bradshaw, D., Schaefer, U., Groves, N., Gallagher, E., Lee, D., Williams, D., Ellaby, N., Hartman, H., Manesis, N., Patel, V., Ledesma, J., Twohig, K. A., Allara, E., Pearson, C., Cheng, J. K. J., Bridgewater, H. E., Frost, L. R., Taylor-Joyce, G., Brown, P. E., Tong, L., Broos, A., Mair, D., Nichols, J., Carmichael, S. N., Smollett, K. L., Nomikou, K., Aranday-Cortes, E., Johnson, N., Nickbakhsh, S., Vamos, E. E., Hughes, M., Rainbow, L., Eccles, R., Nelson, C., Whitehead, M., Gregory, R., Gemmell, M., Wierzbicki, C., Webster, H. J., Fisher, C. L., Signell, A. W., Betancor, G., Wilson, H. D., Nebbia, G., Flaviani, F., Cerda, A. C., Merrill, T. V., Wilson, R. E., Cotic, M., Bayzid, N., Thompson, T., Acheson, E., Rushton, S., O’Brien, S., Baker, D. 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- Affiliations
- University College London (GB)
- University of Cambridge (GB)
- Cambridge University Hospitals NHS Foundation Trust (GB)
- NHS Blood and Transplant (GB)
- Medway School of Pharmacy (GB)
- University of Basel (CH)
- Addenbrooke's Hospital (GB)
- Papworth Hospital NHS Foundation Trust (GB)
- Fulbourn Hospital (GB)
- Murdoch University (AU)
- King's College London (GB)
- Public Health Wales (GB)
- Wellcome Sanger Institute (GB)
- University of Oxford (GB)
- University of Brighton (GB)
- Guy's Hospital (GB)
- University Hospital Southampton NHS Foundation Trust (GB)
- St Thomas' Hospital (GB)
- Belfast Health and Social Care Trust (GB)
- East Kent Hospitals University NHS Foundation Trust (GB)
- University of Birmingham (GB)
- Public Health England (GB)
- University of Sheffield (GB)
- University of Nottingham (GB)
- Northumbria University (GB)
- Queen's University Belfast (GB)
- University of Kent (GB)
- Quadram Institute (GB)
- Public Health Scotland (GB)
- Portsmouth Hospitals NHS Trust (GB)
- University of Liverpool (GB)
- Imperial College London (GB)
- MRC University of Glasgow Centre for Virus Research (GB)
- NHS Lothian (GB)
- University Hospitals Coventry and Warwickshire NHS Trust (GB)
- University of East Anglia (GB)
- University of Exeter (GB)
- Brighton and Sussex University Hospitals NHS Trust (GB)
- Betsi Cadwaladr University Health Board (GB)
- Centre for Human Genetics (GB)
- Cardiff and Vale University Health Board (GB)
- Gloucestershire Hospitals NHS Foundation Trust (GB)
- Sandwell & West Birmingham Hospitals NHS Trust (GB)
- Norfolk and Norwich University Hospital (GB)
- University of Warwick (GB)
- Barking, Havering And Redbridge University Hospitals NHS Trust (GB)
- Queen Elizabeth Hospital Birmingham (GB)
- Wye Valley NHS Trust (GB)
- University Hospitals of Leicester NHS Trust (GB)
- Great Ormond Street Hospital (GB)
- Royal Free London NHS Foundation Trust (GB)
- South Tees Hospitals NHS Foundation Trust (GB)
- North Cumbria Integrated Care NHS Foundation Trust (GB)
- North Tees and Hartlepool NHS Foundation Trust (GB)
- County Durham and Darlington NHS Foundation Trust (GB)
- Basingstoke and North Hampshire Hospital (GB)
- University of Portsmouth (GB)
- Kettering General Hospital (GB)
- North West London Pathology (GB)
- University of Surrey (GB)
- Swansea University (GB)
- Royal Hampshire County Hospital (GB)
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- Royal Devon & Exeter NHS Foundation Trust (GB)
- National Institute for Health and Care Research (GB)
- NHS Greater Glasgow and Clyde (GB)
- Leeds Teaching Hospitals NHS Trust (GB)
- London School of Hygiene & Tropical Medicine (GB)
- Maidstone and Tunbridge Wells NHS Trust (GB)
- University of Edinburgh (GB)
- Norfolk County Council (GB)
- East Suffolk and North Essex NHS Foundation Trust (GB)
- Queen's Medical Centre (GB)
- Manchester University NHS Foundation Trust (GB)
- Princess Alexandra Hospital NHS Trust (GB)
- Guy's and St Thomas' NHS Foundation Trust (GB)
- MRC Laboratory of Molecular Biology (GB)
- Amsterdam UMC Location University of Amsterdam (NL)
- Facultad de Estudios Superiores Cuautitlán (MX)
- Newcastle University (GB)
- Cardiff University (GB)
- University of Colorado Anschutz (US)
- Corresponding author
- Gupta, Ravindra K.
- ORCID
- Kemp, Steven A.
- Collier, Dami A.
- Datir, Rawlings P.
- Ferreira, Isabella A. T. M.
- Jahun, Aminu
- Rees-Spear, Chloe
- Roberts, David J.
- Chandra, Anita
- Temperton, Nigel
- Baker, Stephen
- Hess, Christoph
- Kingston, Nathalie
- Lehner, Paul J.
- Lyons, Paul A.
- Matheson, Nicholas J.
- Summers, Charlotte
- Thaventhiran, James E. D.
- Toshner, Mark
- Weekes, Michael P.
- Domingo, Jason
- Kennet, Jane
- Price, Jane
- Rowlands, Jane
- Dunmore, Benjamin J.
- Gräf, Stefan
- Legchenko, Ekaterina
- Martin, Jennifer
- Mescia, Federica
- Pointon, Linda
- Tilly, Tobias
- Wood, Jennifer
- Cossetti, Chiara
- Epping, Madeline
- Grenfell, Richard
- Jackson, Sarah
- Nice, Francesca
- Omarjee, Ommar
- Perera, Marianne
- Richoz, Nathan
- Yarkoni, Natalia Savinykh
- Sharma, Rahul
- Stefanucci, Luca
- Stephens, Jonathan
- Bunclark, Katherine
- Rossi, Sabrina
- Yong, Cissy
- Ansaripour, Ali
- Mwaura, Lucy
- Polwarth, Gary
- Polgarova, Petra
- Bong, Sze-How
- Holmes, Elaine
- Papadia, Sofia
- Stark, Hannah
- Stirrups, Kathleen E.
- Walker, Neil
- Webster, Jennifer
- Robson, Samuel C.
- Loman, Nicholas J.
- Connor, Thomas R.
- Golubchik, Tanya
- Bonsall, David
- Smith, Colin P.
- Bucca, Giselda
- Saeed, Kordo
- Prieto, Jacqui A.
- Snell, Luke B.
- Moore, Catherine
- Fairley, Derek J.
- Loose, Matthew W.
- Moses, Samuel
- Bull, Matthew
- Aanensen, David M.
- Curran, Martin D.
- Parmar, Surendra
- Aggarwal, Dinesh
- Shepherd, James G.
- Glaysher, Sharon
- Bashton, Matthew
- Pacchiarini, Nicole
- Carabelli, Alessandro M.
- Templeton, Kate E.
- Wang, Dennis
- Rambaut, Andrew
- O’Grady, Justin
- Cottrell, Simon
- Holden, Matthew T. G.
- Thomson, Emma C.
- Andersson, Monique
- Chauhan, Anoop J.
- Chand, Meera
- Constantinidou, Chrystala
- Unnikrishnan, Meera
- Darby, Alistair C.
- Hiscox, Julian A.
- Paterson, Steve
- Robertson, David L.
- Volz, Erik M.
- Page, Andrew J.
- Pybus, Oliver G.
- Li, Kathy K.
- Shah, Rajiv N.
- Jesudason, Natasha G.
- Dewar, Rebecca
- McMurray, Claire
- McKenna, James P.
- Nelson, Andrew
- Young, Gregory R.
- McCann, Clare M.
- Temperton, Ben
- Roy, Sunando
- Price, Anna
- Rey, Sara
- Rooke, Stefan
- Shaaban, Sharif
- Silveira, Siona
- Pelosi, Emanuela
- Wilson-Davies, Eleri
- Stark, Richard
- Bourgeois, Yann
- Grammatopoulos, Dimitris
- Edgeworth, Jonathan
- Breuer, Judith
- Todd, John A.
- Fraser, Christophe
- Buck, David
- Kay, Gemma L.
- McNally, Alan
- Muir, Peter
- Sivaprakasam, Venkat
- Dervisevic, Samir
- Jeffries, Aaron R.
- Ott, Sascha
- Simpson, David A.
- Masoli, Jane A. H.
- Knight, Bridget A.
- Jones, Christopher R.
- Bosworth, Andrew
- Pymont, Hannah M.
- Hutchings, Stephanie
- Jones, Katie
- Halstead, Fenella
- Holmes, Christopher
- Randell, Paul Anthony
- Cox, Alison
- Harris, Kathryn Ann
- Brown, Julianne Rose
- Haque, Tanzina
- Liggett, Steven
- Graham, Clive
- Collins, Jennifer
- Clark, Gemma
- Sloan, Tim J.
- Lynch, Jessica
- Warne, Ben
- Williams, Thomas
- Haldenby, Sam T.
- Storey, Nathaniel
- Alikhan, Nabil-Fareed
- Holmes, Nadine
- Perry, Malorie
- Lyons, Ronan A.
- Beckett, Angela H.
- Fearn, Christopher
- Cook, Kate
- Blane, Beth
- Batra, Rahul
- Williams, Rachel J.
- Green, Angie
- Samaraweera, Buddhini
- Quick, Joshua
- Poplawski, Radoslaw
- Reynolds, Nicola
- Hall, Grant
- Chaudhry, Yasmin
- Pinckert, Malte L.
- Georgana, Iliana
- Myers, Richard
- Stockton, Joanne
- Williams, Charlotte A.
- Yew, Wen C.
- Trotter, Alexander J.
- Trebes, Amy
- Plimmer, Amy
- McKerr, Caoimhe
- Asad, Hibo
- Graham, Lee
- Taylor, Sarah
- Gallis, Marta
- Louka, Stavroula F.
- Starinskij, Igor
- Jackson, Chris
- Baxter, Laura
- Alam, Mohammad T.
- Orton, Richard J.
- Hughes, Joseph
- Jorgensen, David
- Geidelberg, Lily
- Zarebski, Alex E.
- Raghwani, Jayna
- Kraemer, Moritz U. G.
- Southgate, Joel
- Lindsey, Benjamin B.
- Singer, Joshua B.
- Yeats, Corin A.
- Taylor, Ben E. W.
- Danesh, John
- Eldirdiri, Sahar
- Holmes, Alison
- Price, James
- Hartley, John A.
- Mather, Alison E.
- Chapman, Michael R.
- Mookerjee, Siddharth
- Stanley, Rachael
- Eyre, David
- Crook, Derrick
- Vernet, Gabrielle
- Merrick, Ian
- Bradley, Declan T.
- Bolt, Frances
- Coll, Francesc
- Attwood, Stephen W.
- Davies, Alisha
- Scarlett, Garry P.
- Leek, Danielle
- Sridhar, Sushmita
- Cormie, Claire
- Higginson, Ellen E.
- Maes, Mailis
- Young, Jamie
- Wantoch, Michelle
- Hill, Verity
- Bewshea, Claire M.
- Ellard, Sian
- Auckland, Cressida
- Harrison, Ian
- Richter, Alex
- Beggs, Andrew
- Best, Angus
- Percival, Benita
- Mirza, Jeremy
- Megram, Oliver
- Mayhew, Megan
- Crawford, Liam
- Cumley, Nicola
- Asamaphan, Patawee
- Niebel, Marc O.
- Gunson, Rory N.
- Mollett, Guy
- Blacow, Rachel
- Bird, Paul
- Tang, Julian
- Carden, Holli
- Jackson, Kathryn A.
- Ahmad, Shazaad S. Y.
- Turtle, Lance
- Alcolea-Medina, Adela
- Charalampous, Themoula
- Patel, Amita
- Rowan, Aileen
- Taylor, Graham P.
- Shah, Divya
- Atkinson, Laura
- Lee, Jack C. D.
- Westhorpe, Adam P.
- Lowe, Helen L.
- Ensell, Leah
- Baker, Paul
- Bonner, Stephen
- Essex, Sarah
- Payne, Brendan A. I.
- Raviprakash, Veena
- Smith, Louise
- Davidson, Rose K.
- Bedford, Luke
- Coupland, Lindsay
- Wright, Victoria
- Chappell, Joseph G.
- Tsoleridis, Theocharis
- Ball, Jonathan
- Lister, Michelle M.
- Joseph, Amelia
- Willingham, Iona
- Walsh, Sarah
- Wise, Emma
- Moore, Nathan
- Mori, Matilde
- Kidd, Stephen
- Williams, Rebecca
- Bicknell, Kelly
- Wyllie, Sarah
- Keeley, Alexander J.
- Partridge, David G.
- Raza, Mohammad
- Evans, Cariad
- Johnson, Kate
- Abnizova, Irina
- Barrett, Jeffrey
- Bellis, Katie
- Berger, Duncan
- Blackburn, Kirsty
- Buddenborg, Sarah Kay
- Cagan, Alex
- Clark, Richard
- Cook, Elizabeth
- Coppola, Maria
- Corton, Craig
- Crawford, Mark
- Dogga, Sunil
- Gray, Emma
- Harrott, Alexandria
- Harry, Edward
- Heath, Paul
- Holmes, Sarah
- Iqbal, Sameena
- Jones, Matthew
- Keatley, Jon
- Langford, Cordelia
- Liddle, Jennifer
- Lin, Quan
- Lindsay, Sarah
- Mayho, Matthew
- Murie, Kathryn
- Naydenova, Plamena
- Noell, Guillaume G.
- Ohan, Valeriu
- Patel, Gaurang
- Plowman, Deborah
- Robinson, Katrina
- Robinson, David
- Rogers, Hazel
- Schwach, Frank
- Skeldon, Kenneth
- Smith, James
- Smith, Michelle
- Smith, Sean
- Strickland, Michelle
- Thomson, Nicholas
- Thurston, Scott
- Vancollie, Valerie
- Walker, Matthew
- Waller, Matt
- Wells, Eloise
- Whitton, Georgia
- Widaa, Sara
- Williams, Mia
- Makunin, Alex
- Williamson, Kathleen A.
- Warwick-Dugdale, Joanna
- Farbos, Audrey
- Harrison, James W.
- Sambles, Christine M.
- Studholme, David J.
- Lackenby, Angie
- Miah, Shahjahan
- Bibby, David
- Hubb, Jonathan
- Dabrera, Gavin
- Ramsay, Mary
- Bradshaw, Daniel
- Groves, Natalie
- Gallagher, Eileen
- Lee, David
- Ellaby, Nicholas
- Hartman, Hassan
- Ledesma, Juan
- Twohig, Katherine A.
- Allara, Elias
- Cheng, Jeffrey K. J.
- Bridgewater, Hannah E.
- Frost, Lucy R.
- Brown, Paul E.
- Tong, Lily
- Broos, Alice
- Mair, Daniel
- Nichols, Jenna
- Carmichael, Stephen N.
- Smollett, Katherine L.
- Nomikou, Kyriaki
- Eccles, Richard
- Whitehead, Mark
- Gemmell, Matthew
- Wierzbicki, Claudia
- Webster, Hermione J.
- Signell, Adrian W.
- Betancor, Gilberto
- Wilson, Harry D.
- Nebbia, Gaia
- Flaviani, Flavia
- Cotic, Marius
- Bayzid, Nadua
- Thompson, Thomas
- O’Brien, Sarah
- Baker, David J.
- Rudder, Steven
- Aydin, Alp
- Sang, Fei
- Debebe, Johnny
- Vasylyeva, Tetyana I.
- Marchbank, Angela
- Morgan, Mari
- Workman, Trudy
- Fuller, William
- Bresner, Catherine
- Angyal, Adrienn
- Green, Luke R.
- Parsons, Paul J.
- Tucker, Rachel M.
- Brown, Rebecca
- Whiteley, Max
- Siveroni, Igor
- Le-Viet, Thanh
- Sharrocks, Katherine
- Modis, Yorgo
- Leigh, Kendra E.
- Briggs, John A. G.
- Smith, Kenneth G. C.
- Bradley, John R.
- Pollock, David D.
- Goldstein, Richard A.
- Smielewska, Anna
- Skittrall, Jordan P.
- Gouliouris, Theodore
- Goodfellow, Ian G.
- Gkrania-Klotsas, Effrossyni
- Illingworth, Christopher J. R.
- McCoy, Laura E.
- Gupta, Ravindra K.
- Venue
- Nature
- Published
- 2021-02-05
- Volume
- 592
- Issue
- 7853
- Pages
- 277-282
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7610568
- OpenAlex
- W3128154910
- Cited by
- 1,097
- References
- 54
- Citations by year
- 2026: 36 · 2025: 72 · 2024: 121 · 2023: 157 · 2022: 283 · 2021: 411
- FWCI
- 77.05
- Type
- journal article
- Language
- en
- Update notices
- correction (2022-07-21)
- Open access
- bronze
- doi.org
- Locations
- Nature (publishedVersion)
- medRxiv (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, cc-by)
- PubMed Central (acceptedVersion)
- Kent Academic Repository (University of Kent) (acceptedVersion)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- UEA Digital Repository (University of East Anglia) (submittedVersion)
- Europe PMC (PubMed Central) (submittedVersion, cc-by-nc-nd)
- PubMed Central (submittedVersion, cc-by-nc-nd)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion, cc-by-sa)
- ePrints Soton (University of Southampton) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Institutional Research Information System (Università degli Studi di Brescia) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
- Funders
- Bill and Melinda Gates Foundation (OPP 1175094)
- Wellcome Trust (108082/A/15/Z, 108082, 204911/Z/16/Z, Z/17/Z, WT108082AIA, 217191, 206618/Z/17/Z, 207498, 207498/Z/17/Z)
- UK Research and Innovation (MC_UU_00002/11)
- Cancer Research UK (23923)
- National Institute for Health and Care Research (NF-SI-0514-10109, 207498, RP-PG-0514-20018, ACF-2017-15-004, ACF-2018-04-014, COVID-19-RECPLAS)
- Academy of Medical Sciences (AMS-CSF4-Torok)
- National Institutes of Health (COVID-19)
- NIHR BioResource
- Medical Research Council (MC_UU_00002/11, MR/R015600/1, MR/R008698/1, COVID-19, MC_UP_1201/16)
- Biotechnology and Biological Sciences Research Council (BBS/E/F/000PR10348, BB/P007562/1)
- NIHR Cambridge Biomedical Research Centre
- National Institute of General Medical Sciences (R01GM083127)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- SARS-CoV-2, chronic infection, viral evolution, spike protein, convalescent plasma therapy, neutralizing antibodies, antibody escape, remdesivir, immunosuppression, viral selection, viral infectivity, ultra-deep sequencing
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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