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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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In the citing paper
“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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Self-citationRaglow, 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. (2024) · The Lancet Microbe · doi:10.1016/s2666-5247(23)00336-1 · Cited by 90
“16,17 This hypothesis is further supported by the selection of immune escape mutations in patients who are immunocompromised and treated with convalescent plasma.”
Self-citationChoudhary, M. C., Crain, C. R., Qiu, X., Hanage, W. P., & Li, J. Z. (2021) · Clinical Infectious Diseases · doi:10.1093/cid/ciab380 · Cited by 82
“Four patients were treated with convalescent plasma at least once during their illness [9, 10, 11, 27], Figure 2.”
Mackuľak, T., Cverenkárová, K., Staňová, A. V., Fehér, M., Tamáš, M., Škulcová, A., Gál, M., Naumowicz, M., Špalková, V., & Bírošová, L. (2021) · Antibiotics · doi:10.3390/antibiotics10091070 · Cited by 92
“The method will be even more crucial to employ at healthcare facilities as vaccination and the convalescence plasma treatment will increase selective pressure on the virus to mutate [43].”
MethodSARS-CoV-2 and innate immunity: the good, the bad, and the “goldilocks”
Sievers, B. L., Cheng, M. T. K., Csiba, K., Meng, B., & Gupta, R. K. (2023) · Cellular and Molecular Immunology · doi:10.1038/s41423-023-01104-y · Cited by 91
“Although infectivity and antibody evasion are the two primary factors that drive SARS-CoV-2 evolution [217], it has become increasingly clear that IFN resistance may also play a critical role in shaping the trajectory of SARS-CoV-2 [216, 218].”
BackgroundSelf-citationCOVID-19 vaccines for low- and middle-income countries
Choi, E. M. (2021) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1093/trstmh/trab045 · Cited by 77
“38”
Spurbeck, R. R., Minard-Smith, A. T., & Catlin, L. A. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.147829 · Cited by 85
Use of convalescent plasma in COVID ‐19 patients with immunosuppression
Senefeld, J. W., Klassen, S. A., Ford, S. K., Senese, K. A., Wiggins, C. C., Bostrom, B., Thompson, M. A., Baker, S. E., Nicholson, W. T., Johnson, P. W., et al. (2021) · Transfusion · doi:10.1111/trf.16525 · Cited by 80
“However, there is some hesitancy about using convalescent plasma due to concern that it could select for the emergence of SARS-CoV-2 variants, given reports that new SARS-CoV-2 variants were found in a COVID19 patient with immunosuppression treated with plasma.(67) As described elsewhere,(107) it is highly unlikely th…”
BackgroundSelf-citationEvolution of pathogen tolerance and emerging infections: A missing experimental paradigm
Seal, S., Dharmarajan, G., & Khan, I. (2021) · eLife · doi:10.7554/elife.68874 · Cited by 82
Immunocompromised Patients with Protracted COVID-19: a Review of “Long Persisters”
Dioverti, M. V., Salto‐Alejandre, S., & Haidar, G. (2022) · Current Transplantation Reports · doi:10.1007/s40472-022-00385-y · Cited by 79
An engineered bispecific human monoclonal antibody against SARS-CoV-2
Li, Z., Li, S., Zhang, G., Peng, W., Chang, Z., Zhang, X., Fan, Z., Chai, Y., Wang, F., Zhao, X., et al. (2022) · Nature Immunology · doi:10.1038/s41590-022-01138-w · Cited by 79
Tackling COVID-19 with neutralizing monoclonal antibodies
Corti, D., Purcell, L. A., Snell, G., & Veesler, D. (2021) · Cell · doi:10.1016/j.cell.2021.07.027 · Cited by 78
“However, this may not necessarily apply to acute viral infections and be a consideration in the treatment of prolonged infections in immunocompromised individuals, such as has been observed with COVID-19 (Avanzato et al., 2020; Choi et al., 2020; Kemp et al., 2021; McCarthy et al., 2021).”
Rotondo, J. C., Martini, F., Maritati, M., Mazziotta, C., Mauro, G. D., Lanzillotti, C., Barp, N., Gallerani, A., Tognon, M. G., & Contini, C. (2021) · Viruses · doi:10.3390/v13091687 · Cited by 81
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Self-citationOrgan-specific genome diversity of replication-competent SARS-CoV-2
Cleemput, J. V., van Snippenberg, W., Lambrechts, L., Dendooven, A., D’Onofrio, V., Couck, L., Trypsteen, W., Vanrusselt, J., Theuns, S., Vereecke, N., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26884-7 · Cited by 77
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Self-citationEarly cross-coronavirus reactive signatures of humoral immunity against COVID-19
Kapłonek, P., Wang, C., Bartsch, Y. C., Fischinger, S., Gorman, M. J., Bowman, K. A., Kang, J., Dayal, D., Martin, P., Nowak, R. P., et al. (2021) · Science Immunology · doi:10.1126/sciimmunol.abj2901 · Cited by 77
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Could mutations of SARS-CoV-2 suppress diagnostic detection?
Ascoli, C. A. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00845-3 · Cited by 74
Fantini, J., Yahi, N., Azzaz, F., & Chahinian, H. (2021) · Journal of Infection · doi:10.1016/j.jinf.2021.06.001 · Cited by 73
COVID-19 in B Cell-Depleted Patients After Rituximab: A Diagnostic and Therapeutic Challenge
Furlan, A., Forner, G., Cipriani, L., Vian, E., Rigoli, R., Gherlinzoni, F., & Scotton, P. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.763412 · Cited by 74
Origin and evolution of SARS-CoV-2
Pagani, I., Ghezzi, S., Alberti, S., Poli, G., & Vicenzi, E. (2023) · The European Physical Journal Plus · doi:10.1140/epjp/s13360-023-03719-6 · Cited by 85
The immune response to SARS-CoV-2 in people with HIV
Höft, M. A., Burgers, W. A., & Riou, C. (2023) · Cellular and Molecular Immunology · doi:10.1038/s41423-023-01087-w · Cited by 81
“Prolonged infection in immunocompromised patients was documented early in the pandemic, including patients with cancers, organ transplants, and primary immunode fi ciencies as well as those treated with immunosuppressive medications [88 – 91].”
BackgroundA stem-loop RNA RIG-I agonist protects against acute and chronic SARS-CoV-2 infection in mice
Mao, T., Israelow, B., Lucas, C. G. D. O., Vogels, C. B. F., Gomez-Calvo, M. L., Fedorova, O., Breban, M. I., Menasché, B. L., Dong, H., Linehan, M. M., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20211818 · Cited by 70
Lista, M. J., Winstone, H., Wilson, H., Dyer, A. S., Pickering, S., Galão, R. P., Lorenzo, G. D., Cowton, V. M., Furnon, W., Suárez, N. M., et al. (2022) · Journal of Virology · doi:10.1128/jvi.01250-22 · Cited by 86
Self-citationCharacterization and functional interrogation of the SARS-CoV-2 RNA interactome
Labeau, A., Fery-Simonian, L., Lefèvre‐Utile, A., Pourcelot, M., Bonnet‐Madin, L., Soumelis, V., Lotteau, V., Vidalain, P., Amara, A., & Meertens, L. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110744 · Cited by 75
Xue, S., Han, Y., Wu, F., & Wang, Q. (2024) · Protein & Cell · doi:10.1093/procel/pwae007 · Cited by 81
“Besides, mutations within RBD could affect other spike characteristics, such as protein expression and spike stability (Gupta et al., 2021; Kemp et al., 2021; Kumar et al., 2021).”
BackgroundLevy, G., Guglielmelli, P., Langmuir, P. B., & Constantinescu, S. N. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-002838 · Cited by 70
Pathophysiological, immunological, and inflammatory features of long COVID
Böhmwald, K., Diethelm‐Varela, B., Rodríguez‐Guilarte, L., Rivera, T., Riedel, C. A., González, P. A., & Kalergis, A. M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1341600 · Cited by 80
“This is crucial, especially given the limited but strong evidence suggesting that persistent infection in these individuals may contribute to the emergence of new variants, as discussed earlier (69 – 72).”
BackgroundHueso, T., Godron, A.-S., Lanoy, É., Pacanowski, J., Levi, L. I., Gras, E., Surgers, L., Guemriche, A., Meynard, J., Pirenne, F., et al. (2022) · Leukemia · doi:10.1038/s41375-022-01511-6 · Cited by 67
“In light of this, the emergence of variants due to protracted shedding or therapyrelated selection [34, 35] remains the most important challenge to face.”
BackgroundOmicron-B.1.1.529 leads to widespread escape from neutralizing antibody responsesPreprint
Dejnirattisai, W., Huo, J., Zhou, D., Zahradník, J., Supasa, P., Liu, C., Duyvesteyn, H. M. E., Ginn, H. M., Mentzer, A. J., Tuekprakhon, A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.03.471045 · Cited by 69
Self-citationDrug Combinations as a First Line of Defense against Coronaviruses and Other Emerging Viruses
White, J. M., Schiffer, J. T., Bender Ignacio, R. A., Xu, S., Kainov, D., Ianevski, A., Aittokallio, T., Frieman, M., Olinger, G. G., & Polyak, S. J. (2021) · mBio · doi:10.1128/mbio.03347-21 · Cited by 64
SARS-CoV-2 variants and effectiveness of vaccines: a review of current evidence
Tatsi, E., Filippatos, F., & Michos, A. G. (2021) · Epidemiology and Infection · doi:10.1017/s0950268821002430 · Cited by 68
“Compared to previous circulating strains, it seems that generation of NAbs levels is suggestively lower against B.1.351 and B.1.617.2 [85, 86].”
BackgroundInfluentialGenomic Perspectives on the Emerging SARS-CoV-2 Omicron Variant
Ma, W., Yang, J., Fu, H., Su, C., Yu, C., Wang, Q., de Vasconcelos, A. T. R., Bazykin, G. A., Bào, Y., & Li, M. (2022) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2022.01.001 · Cited by 59
“This hypothesis was supported 235 by the accelerated viral evolution observed in immunocompromised patients and has 236 been previously proposed to explain how the Alpha variant was generated [24,25] 237 (https://virological.”
BackgroundRemdesivir-induced emergence of SARS-CoV2 variants in patients with prolonged infection
Heyer, A., Günther, T., Robitaille, A., Lütgehetmann, M., Addo, M. M., Jarczak, D., Kluge, S., Aepfelbacher, M., Wiesch, J. S. Z., Fischer, N., et al. (2022) · Cell Reports Medicine · doi:10.1016/j.xcrm.2022.100735 · Cited by 65
“Unlike remdesivir, for which patient reports and in vitro studies on resistance mutations are available, 2,3,5,8,11,23,26 similar data for Paxlovid or mulnopiravir treatment regimen are still lacking.”
One year into the pandemic: Short-term evolution of SARS-CoV-2 and emergence of new lineages
Gónzález‐Candelas, F., Shaw, M., Phan, T. G., Kulkarni‐Kale, U., Paraskevis, D. N., Luciani, F., Kimura, H., & Sironi, M. (2021) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2021.104869 · Cited by 65
Cantón, R., Ramos, P. D. L., Botella, A. G., García‐Lledó, A., Gómez‐Pavón, J., del Castillo, J. M. G., Hernández‐Sampelayo, T., Delgado, M. C. M., Martín‐Sánchez, F. J., Martínez‐Sellés, M., et al. (2021) · Revista Española de Quimioterapia · doi:10.37201/req/071.2021 · Cited by 66
Landscape of human antibody recognition of the SARS-CoV-2 receptor binding domain
Wheatley, A. K., Pymm, P., Esterbauer, R., Dietrich, M. H., Lee, W. S., Drew, D. R., Kelly, H. G., Chan, L., Mordant, F. L., Black, K. A., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109822 · Cited by 62
Unlocking capacities of genomics for the COVID-19 response and future pandemics
Knyazev, S., Chhugani, K., Sarwal, V., Ayyala, R., Singh, H., Karthikeyan, S., Deshpande, D., Baykal, P. I., Comarova, Z., Lu, A., et al. (2022) · Nature Methods · doi:10.1038/s41592-022-01444-z · Cited by 61
Self-citationSARS-CoV-2 variants – Evolution, spike protein, and vaccines
Chen, K.-W. K., Huang, D. T., & Huang, L. (2022) · Biomedical Journal · doi:10.1016/j.bj.2022.04.006 · Cited by 63
“[8] Kemp SA, Collier DA, Datir RP, Ferreira IATM, Gayed S, Jahun A, et al.”
Contributions of adaptation and purifying selection to SARS-CoV-2 evolution
Neher, R. A. (2022) · Virus Evolution · doi:10.1093/ve/veac113 · Cited by 58
Leung, W., Chorlton, S. D., Tyson, J. R., Al‐Rawahi, G. N., Jassem, A. N., Prystajecky, N., Masud, S., Deans, G. D., Chapman, M. G., Mirzanejad, Y., et al. (2021) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2021.10.045 · Cited by 63
Self-citationSARS-CoV-2 Variants and Their Relevant Mutational Profiles: Update Summer 2021
Alkhatib, M., Svicher, V., Salpini, R., Ambrosio, F. A., Bellocchi, M. C., Carioti, L., Piermatteo, L., Scutari, R., Costa, G., Artese, A., et al. (2021) · Microbiology Spectrum · doi:10.1128/spectrum.01096-21 · Cited by 62
Cheng, M. H., Porritt, R. A., Rivas, M. N., Krieger, J., Ozdemir, A. B., Garcia, G., Arumugaswami, V., Fries, B. C., Arditi, M., & Bahar, İ. (2021) · Structure · doi:10.1016/j.str.2021.04.005 · Cited by 59
Focosi, D., Maggi, F., Franchini, M., McConnell, S. A., & Casadevall, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010029 · Cited by 61
“In one instance of immune escape associated with CCP, a variant with D796H mutation manifested modestly reduced sensitivity to neutralization by CCP that was associated with reduced infectivity, which was only partly compensated by ∆HV69–70 [36].”
BackgroundRecent Chronology of COVID-19 Pandemic
Siddiqui, S., Alhamdi, H. W. S., & Alghamdi, H. A. (2022) · Frontiers in Public Health · doi:10.3389/fpubh.2022.778037 · Cited by 80
SARS-CoV-2 escape from cytotoxic T cells during long-term COVID-19
Stanevich, O. V., Alekseeva, E. I., Sergeeva, M. V., Fadeev, A. V., Komissarova, K., Ivanova, A. A., Simakova, T., Vasilyev, K., Shurygina, A.-P. S., Stukova, M., et al. (2023) · Nature Communications · doi:10.1038/s41467-022-34033-x · Cited by 60
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“It has been hypothesized that such highly mutated variants may have emerged from immune-compromised patients [28].”
BackgroundB cell receptor repertoire kinetics after SARS-CoV-2 infection and vaccination
Kotagiri, P., Mescia, F., Rae, W. M., Bergamaschi, L., Tuong, Z. K., Turner, L., Hunter, K., Gerber, P. P., Hosmillo, M. D. T., Hess, C., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110393 · Cited by 61
“B cell depletion can result in persisting viremia (Buckland et al., 2020; Kemp et al., 2021), SARS-CoV-2 neutralizing monoclonal antibodies and convalescent plasma may have a therapeutic role (Joyner et al., 2021; Libster et al., 2021), and neutralizing antibodies may prevent re-infection and…”
Self-citationAn mRNA-based T-cell-inducing antigen strengthens COVID-19 vaccine against SARS-CoV-2 variants
Tai, W., Feng, S., Chai, B., Lu, S., Zhao, G., Chen, D., Yu, W., Ren, L., Shi, H., Lü, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38751-8 · Cited by 58
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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