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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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Molecular Beacons Allow Specific RT-LAMP Detection of B.1.1.7 Variant SARS-CoV-2
Sherrill-Mix, S. A., Duyne, G. D. V., & Bushman, F. D. (2021) · Journal of Biomolecular Techniques JBT · doi:10.7171/jbt.21-3203-004 · Cited by 26
Antigenic evolution of SARS-CoV-2 in immunocompromised hosts
Smith, C. A., & Ashby, B. (2022) · Evolution Medicine and Public Health · doi:10.1093/emph/eoac037 · Cited by 26
“In SARS-CoV-2, the mutation D796H protects against neutralizing antibodies but reduces infectivity, unless the mutation ΔH69/ΔV70 is also present [23].”
BackgroundResultSelf-citationNiemeyer, D., Stenzel, S., Veith, T., Schroeder, S., Friedmann, K., Weege, F., Trimpert, J., Heinze, J., Richter, A. M., Jansen, J., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001871 · Cited by 25
“In accordance with previous reports [34,35], deletion of H(69)/V(70) increased spike abundance in pseudotyped particles.”
ResultSelf-citationMeijer, S. E., Paran, Y., Belkin, A., Ben‐Ami, R., Maor, ., Nesher, L., Hussein, K., Rahav, G., & Brosh‐Nissimov, T. (2024) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2024.04.009 · Cited by 27
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Self-citationUp State of the SARS-COV-2 Spike Homotrimer Favors an Increased Virulence for New Variants
Giron, C. C., Laaksonen, A., & da Silva, F. L. B. (2021) · Frontiers in Medical Technology · doi:10.3389/fmedt.2021.694347 · Cited by 25
Franceschi, V. B., Ferrareze, P. A. G., Zimerman, R. A., Cybis, G. B., & Thompson, C. E. (2021) · Virus Research · doi:10.1016/j.virusres.2021.198532 · Cited by 25
Functional Effects of Receptor-Binding Domain Mutations of SARS-CoV-2 B.1.351 and P.1 Variants
Bayarri‐Olmos, R., Jarlhelt, I., Johnsen, L. B., Hansen, C. B., Helgstrand, C., Bjelke, J. R., Matthiesen, F., Nielsen, S. D., Iversen, K. K., Ostrowski, S. R., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.757197 · Cited by 25
Cunha, M. D. P., Vilela, A. P. P., Molina, C. V., Acuña, S. M., Muxel, S. M., Barroso, V. D. M., Baroni, S., de Oliveira, L. G., Angelo, Y. D. S., Peron, J. P. S., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.760170 · Cited by 24
“Other studies that characterized the intra-host viral diversity in patients with persistent infection showed a strong selection bias, with the introduction of neutralizing antibody cocktails or several interventions to treat secondary symptoms to the virus action (11, 12).”
BackgroundBarona‐Gómez, F., Delaye, L., Díaz-Valenzuela, E., Plisson, F., Cruz‐Pérez, A., Díaz-Sánchez, M., García-Sepúlveda, C. A., Sánchez‐Flores, A., Abreu, R. P., Valencia-Valdespino, F. J., et al. (2021) · Microbial Genomics · doi:10.1099/mgen.0.000684 · Cited by 24
“Cases where natural or unintended immunological pressures, such as the use of convalescent plasma [17] or high prevalence of the disease leading to a high immunological burden [11], can help us understand what to expect during the vaccination stage of the pandemic, but further population genomics and epidemiological s…”
BackgroundThe impact of hypoxia on B cells in COVID-19
Kotagiri, P., Mescia, F., Hanson, A., Turner, L., Bergamaschi, L., Peñalver, A., Richoz, N., Moore, S. D., Ortmann, B. M., Dunmore, B. J., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.103878 · Cited by 27
Self-citationHuman coronaviruses: The emergence of SARS-CoV-2 and management of COVID-19
Solomon, M., & Liang, C. (2022) · Virus Research · doi:10.1016/j.virusres.2022.198882 · Cited by 25
Alfonso, R., Lin, J., Kirschner, V., Lei, J., Feuer, G., Malin, M. L., Liu, J., Roche, M., & Sadiq, S. A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.926318 · Cited by 28
Fang, L., Xu, J., Zhao, Y., Fan, J., Shen, J., Liu, W., & Cao, G. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1228128 · Cited by 26
Within-host evolutionary dynamics and tissue compartmentalization during acute SARS-CoV-2 infection
Farjo, M., Koelle, K., Martin, M. A., Gibson, L. L., Walden, K. K. O., Rendon, G., Fields, C. J., Alnaji, F. G., Gallagher, N., Luo, C. H., et al. (2024) · Journal of Virology · doi:10.1128/jvi.01618-23 · Cited by 27
Self-citationAddetia, A., Piccoli, L., Case, J. B., Park, Y., Beltramello, M., Guarino, B., Dang, H. V., Pinto, D., Scheaffer, S. M., Sprouse, K. R., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.17.523798 · Cited by 25
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Ex vivo and in vivo suppression of SARS-CoV-2 with combinatorial AAV/RNAi expression vectors
Becker, J., Stanifer, M. L., Leist, S. R., Stolp, B., Maiakovska, O., West, A., Wiedtke, E., Börner, K., Ghanem, A., Ambiel, I., et al. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.01.024 · Cited by 25
Perspectives: SARS-CoV-2 Spike Convergent Evolution as a Guide to Explore Adaptive Advantage
Zahradník, J., Nunvář, J., & Schreiber, G. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.748948 · Cited by 25
Khatamzas, E., Antwerpen, M. H., Rehn, A., Graf, A., Hellmuth, J. C., Hollaus, A., Mohr, A., Gaitzsch, E., Weiglein, T., Georgi, E., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32772-5 · Cited by 22
Naturally occurring spike mutations influence the infectivity and immunogenicity of SARS-CoV-2
Peng, Q., Zhou, R., Liu, N., Wang, H., Xu, H., Zhao, M., Yang, D., Au, K., Huang, H., Liu, L., et al. (2022) · Cellular and Molecular Immunology · doi:10.1038/s41423-022-00924-8 · Cited by 26
“In addition, deletions at residues 69–70 of the NTD are related to increased virus replication in the upper respiratory tract [15].”
BackgroundA comprehensive update on CIDO: the community-based coronavirus infectious disease ontology
He, Y. O., Yu, H. J., Huffman, A., Lin, Y., Natale, D. A., Beverley, J. R., Zheng, L., Perl, Y., Wang, Z., Liu, Y., et al. (2022) · Journal of Biomedical Semantics · doi:10.1186/s13326-022-00279-z · Cited by 24
“These include: S:E484K, S:N501Y, S:H69-, and S:144Y [76, 80-82] and are predominantly located on the N-Terminal Domain (NTD) of the S protein.”
BackgroundPersistent SARS-CoV-2 PCR Positivity Despite Anti-viral Treatment in Immunodeficient Patients
Chan, M. M. H., Linn, M. M. N., O’Hagan, T., Guerra‐Assunção, J. A., Lackenby, A., Workman, S., Dacre, A., Burns, S. O., Breuer, J., Hart, J., et al. (2023) · Journal of Clinical Immunology · doi:10.1007/s10875-023-01504-9 · Cited by 26
“Indeed, early COVID-19 CP trials showed favourable outcomes [11], especially in patients with common variable immunodeficiency (CVID) [12, 13], but CP has since been withdrawn due to its inefficacy in large trials treating largely immunocompetent patients and a potential association with driving emergence of immune es…”
BackgroundSelf-citationKarim, F., Riou, C., Bernstein, M. P., Jule, Z., Lustig, G., van Graan, S., Keeton, R., Upton, J., Ganga, Y., Khan, K., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-46673-2 · Cited by 26
Bridging animal and clinical research during SARS-CoV-2 pandemic: A new-old challenge
Winkler, M. S., Skirecki, T., Brunkhorst, F. M., Cajander, S., Cavaillon, J., Ferrer, R., Flohé, S. B., García‐Salido, A., Giamarellos‐Bourboulis, E. J., Girardis, M., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103291 · Cited by 26
Colson, P., Devaux, C. A., Lagier, J., Gautret, P., & Raoult, D. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10153276 · Cited by 22
“Some immunocompromised patients with persistent SARS-CoV-2 infection [13,20] were administered remdesivir, which possibly increases the frequency of mutations, and received convalescent plasma or anti-spike antibodies that were reported to drive the occurrence of spike escape mutations.”
BackgroundLu, M., Zhang, Y., Dravid, P., Li, A., Zeng, C., Mahesh, K. C., Trivedi, S., Sharma, H., Chaiwatpongsakorn, S., Zani, A., et al. (2021) · Journal of Virology · doi:10.1128/jvi.00592-21 · Cited by 44
SARS-CoV-2 infection and disease outcomes in non-human primate models: advances and implications
Yuan, L., Tang, Q., Zhu, H., Guan, Y., Cheng, T., & Xia, N. (2021) · Emerging Microbes & Infections · doi:10.1080/22221751.2021.1976598 · Cited by 20
Bean, D. J., Monroe, J., Turcinovic, J., Moreau, Y., Connor, J. H., & Sagar, M. (2021) · Clinical Infectious Diseases · doi:10.1093/cid/ciab940 · Cited by 24
Targeted escape of SARS-CoV-2 in vitro from monoclonal antibody S309, the precursor of sotrovimab
Magnus, C. L., Hiergeist, A., Schuster, P., Rohrhofer, A., Medenbach, J., Gessner, A., Peterhoff, D., & Schmidt, B. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.966236 · Cited by 23
“In a multicenter, double-blind phase 3 study, sotrovimab reduced disease progression and hospitalization by 85% in high-risk outpatients with mild-to-moderate COVID-19 (12).”
BackgroundInfluentialKumar, S., Delipan, R., Chakraborty, D., Kanjo, K., Singh, R., Singh, N., Siddiqui, S., Tyagi, A., Jha, V., Thakur, K. G., et al. (2023) · Journal of Virology · doi:10.1128/jvi.00922-23 · Cited by 23
“Kemp et al. showed that D796H/D796Y frequently surfaced in viremia in an immunocompromised COVID-19 patient during plasma therapy (29).”
BackgroundEvolution of evolvability in rapidly adapting populations
Ferrare, J. T., & Good, B. H. (2024) · Nature Ecology & Evolution · doi:10.1038/s41559-024-02527-0 · Cited by 28
“previously unappreciated role in driving the success of genetic variants in large microbial populations, from laboratory evolution experiments (7, 9, 12, 25, 43) to natural systems like cancer (13, 14), influenza (26), or SARS-CoV-2 (29, 44).”
Prolonged viral replication in patients with hematologic malignancies hospitalized with COVID-19
García‐Vidal, C., Puerta‐Alcalde, P., Mateu, A., Cuesta, G., Meira, F. S., Lopera, C., Monzó, P., Bravo, M. S., Dueñas, G., Chumbita, M., et al. (2022) · Haematologica · doi:10.3324/haematol.2021.280407 · Cited by 23
Koeckerling, D., & Barker, J. (2021) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiab328 · Cited by 22
“8 generates strong selective pressures that can promote the emergence and dominance of escape variants when applied to diverse viral populations.[22] Combining mAbs directed towards separate vulnerable epitopes of the SARS-CoV-2 spike protein may diminish the dangers of immune escape by reducing the likelihood that mu…”
BackgroundPhenotypic evolution of SARS-CoV-2 spike during the COVID-19 pandemic
Furnon, W., Cowton, V. M., Lorenzo, G. D., Orton, R. J., Herder, V., Cantoni, D. M., Ilia, G., Mendonça, D. C., Kerr, K., Allan, J., et al. (2025) · Nature Microbiology · doi:10.1038/s41564-024-01878-5 · Cited by 23
Self-citationHoffmann, S., Schrezenmeier, E. V., Desmarets, M., Halleck, F., Dürrbach, A., Peters, L., Tremmel, A.-T., Seidel, A., Führer, M., Bachmann, F., et al. (2025) · EBioMedicine · doi:10.1016/j.ebiom.2025.105613 · Cited by 22
“33 – 36 This possibility has not been studied so far in the context of a controlled trial.”
Self-citationMore Than Just Gene Therapy Vectors: Lentiviral Vector Pseudotypes for Serological Investigation
Toon, K., Bentley, E. M., & Mattiuzzo, G. (2021) · Viruses · doi:10.3390/v13020217 · Cited by 23
Egeren, D. V., Novokhodko, A., Stoddard, M., Tran, U., Zetter, B. R., Rogers, M. S., Joseph‐McCarthy, D., & Chakravarty, A. (2021) · Scientific Reports · doi:10.1038/s41598-021-02148-8 · Cited by 20
Why are some coronavirus variants more infectious?
Mukherjee, R., & Satardekar, R. (2021) · Journal of Biosciences · doi:10.1007/s12038-021-00221-y · Cited by 23
“In an immunosuppressed individual receiving plasma therapy upon infection by the B.1 strain, a dominant viral genotype with the deletion at H69/V70 was found to emerge together with mutation (D796H) in S2 subunit (Kemp et al. 2021).”
Backgroundde Souza, G. A. P., Bideau, M. L., Boschi, C., Ferreira, L., Wurtz, N., Devaux, C. A., Colson, P., & Scola, B. L. (2021) · Viruses · doi:10.3390/v14010023 · Cited by 21
“The emergence of new SARS-CoV-2 variants throughout the COVID-19 pandemic brought with them public health concerns, due to the increase in transmissibility [10–12] and especially regarding the effectiveness of vaccines [13,14], as mutations in the spike protein, which is a target for many of the approved vaccines, wer…”
BackgroundWastewater Sequencing—An Innovative Method for Variant Monitoring of SARS-CoV-2 in Populations
Tamáš, M., Potočárová, A., Konečná, B., Kľúčár, Ľ., & Mackuľak, T. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19159749 · Cited by 22
Convalescent plasma (hyperimmune immunoglobulin) for COVID-19 management: An update
Chavda, V. P., Bezbaruah, R., Dolia, S., Shah, N., Verma, S., Savale, S. S., & Ray, S. (2023) · Process Biochemistry · doi:10.1016/j.procbio.2023.01.018 · Cited by 25
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. L., Liggett, S., Graham, C., Swindells, E., Collins, J., Eltringham, G., Campbell, S., McClure, P. C., Clark, G., Sloan, T. J., Jones, C., Lynch, J., analysis, M. C. A. S. &., Warne, B., Leonard, S., Durham, J., Williams, T., Haldenby, S. T., Storey, N., Alikhan, N.-F., Holmes, N., Moore, C., Carlile, M., Perry, M., Craine, N., Lyons, R. A., Beckett, A. H., Goudarzi, S., Fearn, C., Cook, K., Dent, H., Paul, H., tools, M. C. A. S. &. A., Davies, R., Project administration and samples & logistics, Blane, B., Girgis, S. T., Beale, M. A., Bellis, K. L., Dorman, M. J., Drury, E., Kane, L., Kay, S., McGuigan, S., Nelson, R., Prestwood, L., Rajatileka, S., Batra, R., Williams, R. J., Kristiansen, M., Green, A., Justice, A., Mahanama, A. I. K., Samaraweera, B., Project administration and sequencing & analysis, Hadjirin, N. F., Quick, J., Project administration and software & analysis tools, Poplawski, R., analysis, S. &. L. A. S. &., Kermack, L. M., Reynolds, N., Hall, G., Chaudhry, Y., Pinckert, M. L., Georgana, I., Moll, R. J., Thornton, A., Myers, R., Stockton, J., Williams, C. A., Yew, W. C., Trotter, A. J., Trebes, A., MacIntyre-Cockett, G., Birchley, A., Adams, A., Plimmer, A., Gatica-Wilcox, B., McKerr, C., Hilvers, E., Jones, H., Asad, H., Coombes, J., Evans, J. M., Fina, L., Gilbert, L., Graham, L., Cronin, M., Kumziene-Summerhayes, S., Taylor, S., Jones, S., Groves, D. C., Zhang, P., Gallis, M., Louka, S. F., tools, S. &. L. A. S. &. A., Starinskij, I., tools, S. &. A. A. S. &. A., Jackson, C., Gourtovaia, M., Tonkin-Hill, G., Lewis, K., Tovar-Corona, J. M., James, K., Baxter, L., Alam, M. T., Orton, R. J., Hughes, J., Vattipally, S., Ragonnet-Cronin, M., Nascimento, F. F., Jorgensen, D., Boyd, O., Geidelberg, L., Zarebski, A. E., Raghwani, J., Kraemer, M. U. G., Southgate, J., Lindsey, B. B., Freeman, T. M., visualization, S. &. A. T. A., Keatley, J.-P., Singer, J. B., de Oliveira Martins, L., Yeats, C. A., Abudahab, K., Taylor, B. E. W., Menegazzo, M., supervision, L. &., Danesh, J., Hogsden, W., Eldirdiri, S., Kenyon, A., Mason, J., Robinson, T. I., Holmes, A., Price, J., Hartley, J. A., Curran, T., Mather, A. E., Shankar, G., Jones, R., Howe, R., Morgan, S., curation, M., Wastenge, E., Chapman, M. R., Mookerjee, S., Stanley, R., Smith, W., Peto, T., Eyre, D., Crook, D., Vernet, G., Kitchen, C., Gulliver, H., Merrick, I., Guest, M., Munn, R., Bradley, D. T., Wyatt, T., Project administration, Beaver, C., Foulser, L., Palmer, S., Churcher, C. M., Brooks, E., Smith, K. S., Galai, K., McManus, G. M., Bolt, F., Coll, F., Meadows, L., Attwood, S. W., Davies, A., De Lacy, E., Downing, F., Edwards, S., Scarlett, G. P., Jeremiah, S., Smith, N., logistics, S. &., Leek, D., Sridhar, S., Forrest, S., Cormie, C., Gill, H. K., Dias, J., Higginson, E. E., Maes, M., Young, J., Wantoch, M., Jamrozy, D., Lo, S., Patel, M., Hill, V., Bewshea, C. 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. C., Chapman, L., Chillingworth, T.-J., Clapham, P., Clark, R., Clarke, A., Clarke, C., Cole, D., Cook, E., Coppola, M., Cornell, L., Cornwell, C., Corton, C., Crackett, A., Cranage, A., Craven, H., Craw, S., Crawford, M., Cutts, T., Dabrowska, M., Davies, M., Davies, R., Dawson, J., Day, C., Densem, A., Dibling, T., Dockree, C., Dodd, D., Dogga, S., Dorman, M., Dougan, G., Dougherty, M., Dove, A., Drummond, L., Drury, E., Dudek, M., Durham, J., Durrant, L., Easthope, E., Eckert, S., Ellis, P., Farr, B., Fenton, M., Ferrero, M., Flack, N., Fordham, H., Forsythe, G., Foulser, L., Francis, M., Fraser, A., Freeman, A., Galvin, A., Garcia-Casado, M., Gedny, A., Girgis, S., Glover, J., Goncalves, S., Goodwin, S., Gould, O., Gourtovaia, M., Gray, A., Gray, E., Griffiths, C., Gu, Y., Guerin, F., Hamilton, W., Hanks, H., Harrison, E., Harrott, A., Harry, E., Harvison, J., Heath, P., Hernandez-Koutoucheva, A., Hobbs, R., Holland, D., Holmes, S., Hornett, G., Hough, N., Huckle, L., Hughes-Hallet, L., Hunter, A., Inglis, S., Iqbal, S., Jackson, A., Jackson, D., James, K., Jamrozy, D., Verdejo, C. 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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