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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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Boshier, F. A. T., Venturini, C., Stirrup, O., Guerra‐Assunção, J. A., Alcolea-Medina, A., Becket, A. H., Byott, M., Charalampous, T., Filipe, A. D. S., Frampton, D., et al. (2021) · Journal of Infection · doi:10.1016/j.jinf.2021.09.022 · Cited by 11
Self-citationMagnetically Enhanced Liquid SERS for Ultrasensitive Analysis of Bacterial and SARS-CoV-2 Biomarkers
Zhang, J., Zhang, C., Yang, Y., Ji, J., Dong, H., Forsberg, E., Cheng, X., & He, S. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.735711 · Cited by 11
“Given the scale and severity of the COVID-19 pandemic with a possibility to prevail in the next few years given the many emerging mutants, such as Delta and Lamda variants (Kemp et al., 2021), it is of importance to develop reproducible methods to quantify IgG antibodies with high sensitivity (Deeks et al.”
BackgroundHe, Y., Qu, J. T., Wei, L., Liao, S., Zheng, N., Liu, Y., Wang, X., Jing, Y., Shen, C. K.-F., Ji, C., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.689065 · Cited by 11
“Coronavirus disease 2019 (COVID-19), caused by infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has threatened global public health for more than a year since it began spreading worldwide at the end of 2019 (1, 2).”
BackgroundConserved Pattern and Potential Role of Recurrent Deletions in SARS-CoV-2 Evolution
Weng, S., Zhou, H., Ji, C., Li, L., Han, N., Yang, R., Shang, J., & Wu, A. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.02191-21 · Cited by 11
Lim, C. P., Kok, B. H., Lim, H. T., Chuah, C., Abdul‐Rahman, B., Majeed, A. B. A., Wykes, M., Leow, C. Y., & Leow, C. Y. (2022) · Pathogens and Global Health · doi:10.1080/20477724.2022.2072456 · Cited by 12
“Substitution P681H is adjacent to the furin cleavage site, which is essential for viral infection [52] while deletion ∆69-70 increases viral infectivity and is associated with immune escape in immunocompromised patients [53].”
BackgroundComplexity of Viral Epitope Surfaces as Evasive Targets for Vaccines and Therapeutic Antibodies
Miller, N. L., Raman, R., Clark, T., & Sasisekharan, R. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.904609 · Cited by 12
Biscarini, S., Villa, S., Genovese, C., Tomasello, M., Tonizzo, A., Fava, M., Iannotti, N., Bolis, M., Mariani, B., Valzano, A. G., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10082002 · Cited by 11
“Reducing the amount of time in which the virus can evolve in this population through the use of early treatments could then be useful from a wider, epidemiological perspective [27].”
BackgroundSARS-CoV-2 intra-host single-nucleotide variants associated with disease severity
Zhang, Y., Jiang, N., Qi, W., Li, T., Zhang, Y., Wu, J., Zhang, H., Zhou, M., Cui, P., Yu, T., et al. (2022) · Virus Evolution · doi:10.1093/ve/veac106 · Cited by 11
Lustig, G., Ganga, Y., Rodel, H. E., Tegally, H., Khairallah, A., Jackson, L., Cele, S., Khan, K., Jule, Z., Reedoy, K., et al. (2023) · Virus Evolution · doi:10.1093/ve/vead075 · Cited by 12
“…group of immunosuppressed people (Avanzato et al. 2020; Choi et al. 2020; Baang et al. 2021; Corey et al. 2021; Hoffman et al. 2021; Jensen et al. 2021; Kemp et al. 2021; Peacock et al. 2021; Karim et al. 2021b; Cele et al. 2022; Maponga et al. 2022; Riddell et al. 2022; Wilkinson et al. 2022).”
Implications of mRNA-based SARS-CoV-2 vaccination for cancer patients
Romano, E., Pascolo, S., & Ott, P. A. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-002932 · Cited by 11
Why are there so few (or so many) circulating coronaviruses?
Rice, B. L., Douek, D. C., McDermott, A. B., Grenfell, B. T., & Metcalf, C. J. E. (2021) · Trends in Immunology · doi:10.1016/j.it.2021.07.001 · Cited by 11
“The presence of these groups within populations might modify the context of viral emergence by altering immune system functioning and changing the evolutionary selection pressure for mutations associated with transmission or immune escape, as suggested for SARS-CoV-2 [42].”
Structures and therapeutic potential of anti-RBD human monoclonal antibodies against SARS-CoV-2
Huang, K.-Y. A., Zhou, D., Tan, T. K., Chen, C., Duyvesteyn, H. M. E., Zhao, Y., Ginn, H. M., Qin, L., Rijal, P., Schimanski, L. M., et al. (2021) · Theranostics · doi:10.7150/thno.65563 · Cited by 12
“7 variant from respiratory samples and its reduced sensitivity to antibody in immunocompromised COVID-19 patients, supporting the emergence of antibody escape variants in vivo [31].”
BackgroundBasu, S., Akash, M. M. H., Hochberg, N. S., Senior, B. A., Joseph‐McCarthy, D., & Chakravarty, A. (2022) · Rhinology online · doi:10.4193/rhinol/21.053 · Cited by 11
“Such a scenario is of particular concern for the current wave of vaccines that target the spike protein; work by us((75)) and others((76-79)) suggests that the spike protein has a relatively high mutational tolerance and can readily generate immuneevading mutations now that vaccinal and natural immunity are widespread…”
BackgroundSARS-CoV-2 gained a novel spike protein S1–N-Terminal Domain (S1-NTD)
Desingu, P. A., Nagarajan, K., & Dhama, K. (2022) · Environmental Research · doi:10.1016/j.envres.2022.113047 · Cited by 11
IS IT TIME TO REFLECT, NOT ON THE “WHAT” BUT THE “WHY” IN EMERGING WILDLIFE DISEASE RESEARCH?
Kock, R. A. (2018) · Journal of Wildlife Diseases · doi:10.7589/2019-01-000 · Cited by 11
Recurrent independent emergence and transmission of SARS-CoV-2 Spike amino acid H69/V70 deletionsPreprint
Gupta, R. K., Kemp, S. A., Harvey, W. T., Lytras, S., Carabelli, A. M., & Robertson, D. L. (2021) · Research Square · doi:10.21203/rs.3.rs-136937/v1 · Cited by 12
Self-citationLemmermann, N. A. W., Lieb, B., Laufs, T., Renzaho, A., Runkel, S., Kohnen, W., Linke, M., Gerber, S., Schweiger, S., Michel, A., et al. (2021) · medRxiv · doi:10.1101/2021.02.11.21251324 · Cited by 9
Alter, G., Gorman, M. J., Patel, N., Guebre‐Xabier, M., Zhu, A. L., Atyeo, C. G., Pullen, K. M., Loos, C., Goez-Gazi, Y., Carrion, R., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-200342/v1 · Cited by 9
Characterization of humoral and SARS-CoV-2 specific T cell responses in people living with HIVPreprint
Alrubayyi, A., Gea‐Mallorquí, E., Touizer, E., Hameiri‐Bowen, D., Kopycinski, J. T., Charlton, B. G., Fisher-Pearson, N., Muir, L., Rosa, A., Roustan, C., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-309746/v1 · Cited by 12
Self-citationSARS-CoV-2 Viral Clearance and Evolution Varies by Extent of ImmunodeficiencyPreprint
Li, Y., Choudhary, M. C., Regan, J., Boucau, J., Nathan, A., Speidel, T., Liew, M. Y., Edelstein, G. E., Kawano, Y., Uddin, R., et al. (2023) · medRxiv · doi:10.1101/2023.07.31.23293441 · Cited by 11
“These included a spectrum of immunocompromised hosts from individuals with solid organ transplants, hematological malignancy( 14, 20, 22, 23, 25, 29, 32-36 ), and autoimmune diseases receiving immunosuppressive therapies.”
Snell, L. B., Alcolea-Medina, A., Charalampous, T., Alder, C., Williams, T. G. S., Flaviani, F., Batra, R., Bakrania, P., Thangarajah, R., Neil, S. J. D., et al. (2022) · Clinical Infectious Diseases · doi:10.1093/cid/ciac864 · Cited by 10
“Chronic infection with SARS-CoV-2 can also occur in immunocompromised patients [5], and the limited evidence”
BackgroundSelf-citationPinder, C. L., Jankovic, D., Fox, T. A., Kirkwood, A. A., Enfield, L., Alrubayyi, A., Touizer, E., Ford, R., Pocock, R., Shin, J., et al. (2023) · British Journal of Haematology · doi:10.1111/bjh.18962 · Cited by 9
Self-citationVirus Evolution in Prolonged Infections of Immunocompromised Individuals
Raglow, Z., & Lauring, A. S. (2024) · Clinical Chemistry · doi:10.1093/clinchem/hvae150 · Cited by 12
Parvin, R., Afrin, S. Z., Begum, J. A., Ahmed, S., Nooruzzaman, M., Chowdhury, E. H., Pohlmann, A., & Paul, S. K. (2021) · Microorganisms · doi:10.3390/microorganisms9051035 · Cited by 13
“In addition, some Bangladeshi strains had H69del + V70del, and Y144del or Y145del, which has shown a twofold higher infectivity than wild type [36], and has a decreased sensitivity to convalescent sera [8] respectively.”
BackgroundCabañero-Navalón, M. D., García-Bustos, V., Ruiz-Rodríguez, P., Comas, I., Coscollá, M., Martinez-Priego, L., Todolí, J., & Moral, P. M. (2021) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2021.10.021 · Cited by 10
“However, the selection pressure after plasma therapy in patients with primary immunodeficiencies with reduced inherent clearance capability could potentially give rise to escape mutations with reduced susceptibility to polyclonal neutralizing antibodies [2].”
der Moeren, N. V., Selhorst, P., Ha, M. K., Heireman, L., Gaal, P.-J. V., Breems, D. A., Meysman, P., Laukens, K., Verstrepen, W. A., Gasse, N. V., et al. (2022) · Viruses · doi:10.3390/v14040752 · Cited by 10
“These mutations preserve the reading frame and ere previously reported in chronic, i unoco promised patients, and occur at a global scale in the GISAID database [1,5,13].”
BackgroundFeng, S., Ali, M. S., Evdokimova, M., Reid, G., Clark, N. M., Uprichard, S. L., & Baker, S. C. (2022) · Viruses · doi:10.3390/v14071408 · Cited by 9
“Since the early stage of the pandemic, the evolution of SARS-CoV-2 has been shaped by selection pressures from vaccination, antiviral therapies, and other mitigation strategies [7,8,10,53].”
BackgroundSelf-citationOn the Evolutionary Trajectory of SARS-CoV-2: Host Immunity as a Driver of Adaptation in RNA Viruses
Warger, J., & Gaudieri, S. (2022) · Viruses · doi:10.3390/v15010070 · Cited by 11
The origins of new SARS-COV-2 variants in immunocompromised individuals
Riddell, A. C., & Cutiño‐Moguel, T. (2023) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0000000000000794 · Cited by 12
An RBD bispecific antibody effectively neutralizes a SARS-CoV-2 Omicron variant
Yuan, M., Zhu, Y., Liu, G., Wang, Y., Wang, G., Zhang, G., Ye, L., Qian, Z., & Liu, P. (2023) · One Health Advances · doi:10.1186/s44280-023-00012-0 · Cited by 10
Gilliland, T. H., Dunn, M., Liu, Y., Alcorn, M. D. H., Terada, Y., Vasilatos, S. N., Lundy, J. D., Li, R., Nambulli, S., Larson, D. P., et al. (2023) · iScience · doi:10.1016/j.isci.2023.107764 · Cited by 10
Leach, A., Miller, A., Bentley, E. M., Mattiuzzo, G., Thomas, J. C., McAndrew, C., van Montfort, R., & Rabbitts, T. H. (2021) · Scientific Reports · doi:10.1038/s41598-021-89887-w · Cited by 11
Eslami, S., Glassy, M. C., & Ghafouri‐Fard, S. (2021) · Gene · doi:10.1016/j.gene.2021.146113 · Cited by 12
Quantum Chemical Computation of Omicron Mutations Near Cleavage Sites of the Spike Protein
Adhikari, P., Jawad, B., Podgornik, R., & Ching, W. Y. (2022) · Microorganisms · doi:10.3390/microorganisms10101999 · Cited by 10
“Previously, it has been revealed that the mutation at this site impairs the neutralization susceptibility of antibodies and reduces SARS-CoV-2 infectivity [49].”
BackgroundModelling SARS-CoV-2 spike-protein mutation effects on ACE2 binding
Thakur, S., Verma, R. K., Kepp, K. P., & Mehra, R. (2022) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2022.108379 · Cited by 13
Purifying selection decreases the potential for Bangui orthobunyavirus outbreaks in humans
Orf, G. S., Perez, L. J., Meyer, T. V., Luk, K., Forberg, K., Rodgers, M. A., Hadji, A., James, L., Mampunza, S. M. M., Achari, A., et al. (2023) · Virus Evolution · doi:10.1093/ve/vead018 · Cited by 10
Murugan, N. A., Javali, P. S., Pandian, C. J., Ali, M. A., Srivastava, V., & Jeyaraman, J. (2022) · Physical Chemistry Chemical Physics · doi:10.1039/d2cp00469k · Cited by 10
Self-citationEmergence and fast spread of B.1.1.7 lineage in LebanonPreprint
Younes, M., Hamze, K., Nassar, H., Makki, M., Ghadar, M., Nguewa, P., & Abdel‐Sater, F. (2021) · medRxiv · doi:10.1101/2021.01.25.21249974 · Cited by 10
Braun, K. M., Moreno, G. K., Wagner, C., Accola, M. A., Rehrauer, W. M., Baker, D., Koelle, K., O’Connor, D. H., Bedford, T., Friedrich, T. C., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.30.440988 · Cited by 10
Self-citationInsertions in the SARS-CoV-2 Spike N-Terminal Domain May Aid COVID-19 TransmissionPreprint
Lam, S. D., Waman, V., Orengo, C. A., & Lees, J. G. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.06.471394 · Cited by 10
“Recent experimental studies have suggested that the deletions (at positions 69 and 70) in pocket 3 in the SARS-CoV-2 Alpha variant affect the infectivity of the virus (Kemp et al., 2021; Liu et al., 2021).”
BackgroundCOVID-19 convalescent plasma for the treatment of immunocompromised patients: a systematic reviewPreprint
Senefeld, J. W., Franchini, M., Mengoli, C., Cruciani, M., Zani, M., Gorman, E. K., Focosi, D., Casadevall, A., & Joyner, M. J. (2022) · medRxiv · doi:10.1101/2022.08.03.22278359 · Cited by 10
“Parameters Results Median age, years (range) 55 (1-88)”
BackgroundMethodRaglow, Z., Surie, D., Chappell, J. D., Zhu, Y., Martin, E. T., Kwon, J. H., Frosch, A. E. P., Mohamed, A., Gilbert, J., Bendall, E. E., et al. (2023) · medRxiv · doi:10.1101/2023.08.22.23294416 · Cited by 10
Self-citationSignatures of omicron-like adaptation in early SARS-CoV-2 variants and chronic infection
Cheng, M. T. K., Altaf, M., Jesu Castin, E., Reuschl, A., Sievers, B. L., Kamelian, K., Mesner, D., Morse, R. B., Abdullahi, A., Meng, B., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116135 · Cited by 11
“13,14,16,17 COVID-19 remains a particularly relevant threat for immunocompromised individuals, as COVID-19 vaccines have been shown to induce lower seroconversion rates, 18 reduced neutralization activity, 19 and shorter durations of protection as compared to immune-competent individuals.”
Self-citationJoseph, R., Marais, G. J. K., Iranzadeh, A., Alisoltani, A., Hardie, D. R., Davies, M., Heekes, A., Chetty, N., Timmerman, V., Hsiao, M., et al. (2025) · Journal of Virology · doi:10.1128/jvi.00780-25 · Cited by 8
“A recurring observation during persistent infection is accelerated viral evolution with the emergence of mutations due to host selection pressures in contrast to the limited intra-host diversity observed during acute infections (2, 3, 6, 32, 33, 35).”
Self-citationInada, M., Ishikane, M., Terada, M., Matsunaga, A., Maeda, K., Tsuchiya, K., Miura, K., Sairenji, Y., Kinoshita, N., Ujiie, M., et al. (2021) · Journal of Infection and Chemotherapy · doi:10.1016/j.jiac.2021.04.017 · Cited by 9
“While our patient is not incredibly old, nor does he have the obvious immunodeficiency (only dyslipidemia), there are a few reports suggesting the role of neutralizing antibody in immunocompromised host with persistent COVID-19 [20,21].”
Temporal epistasis inference from more than 3 500 000 SARS-CoV-2 genomic sequences
Zeng, H.-L., Liu, Y., Dichio, V., & Aurell, E. (2022) · Physical review. E · doi:10.1103/physreve.106.044409 · Cited by 9
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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