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Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil
Open accessPublished version of a preprint
Abstract
Unmitigated spread in Brazil: Despite an extensive network of primary care availability, Brazil has suffered profoundly during the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic. Using daily data from state health offices, Castro et al. analyzed the pattern of spread of COVID-19 cases and deaths in the country from February to October 2020. Clusters of deaths before cases became apparent indicated unmitigated spread. SARS-CoV-2 circulated undetected in Brazil for more than a month as it spread north from Sã o Paulo. In Manaus, transmission reached unprecedented levels after a momentary respite in mid-2020. Faria et al. tracked the evolution of a new, more aggressive lineage called P.1, which has 17 mutations, including three (K417T, E484K, and N501Y) in the spike protein. After a period of accelerated evolution, this variant emerged in Brazil during November 2020. Coupled with the emergence of P.1, disease spread was accelerated by stark local inequalities and political upheaval, which compromised a prompt federal response. Science , abh1558 and abh2644, this issue p. 821 and p. 815
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“The past several months have witnessed the emergence of four SArS-cov-2 variants of concern (Alpha, beta, Gamma and Delta)”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [19]
In the citing paper
“The Gamma variant contains the RBD mutations N501Y, E484K and K417T (ref. 19 ).”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [19]
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“As the Gamma variant was associated with a surge of infections in a region of Brazil estimated to have achieved a high infection rate, it is suspected of being able to infect and cause illness in persons previously infected with other variants 19,29,30 .”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [19]
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“It was estimated to result in virus levels 3-4 times higher than earlier variants and to be responsible for an estimated 1.1-fold to 1.8-fold higher mortality 19 .”
From The biological and clinical significance of emerging SARS-CoV-2 variants (2021) · cites this paper as [19]
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Tracking SARS-COV-2 Variants Using Nanopore Sequencing in Ukraine in Summer 2021Preprint
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Self-citationTransmission dynamics of SARS-CoV-2 variants in the Brazilian state of Pará
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“This VOC was first identified in Brazil in December 2020, in the city of Manaus, capital of the Amazonas state, and since then until the end of 2021 it caused several cases in Brazil, especially in the North region (17).”
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“Four of these variants are classified as variants of concern (VOC) by the World Health Organization (WHO): Alpha variant/Lineage B.1.1.7 (first detected in the UK) [5], Beta variant/Lineage B.1.351 (first detected in South Africa) [6], Gamma variant/Lineage P.1 (first detected in Brazil) [7] and Delta variant/Lineage…”
BackgroundInfluentialOsnes, M. N., Alfsnes, K., Bråte, J., García, I., Riis, R. K., Instefjord, K. H., Elshaug, H., Vollan, H. S., Moen, L. V., Pedersen, B. N., et al. (2021) · Virus Evolution · doi:10.1093/ve/veab086 · Cited by 11
The Analyses of High Infectivity Mechanism of SARS-CoV-2 and Its Variants
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“The variants recently considered to be of greatest concern are those carrying amino acid substitutions N501Y and/or E484K within the spike protein [9, 10], as they have increased affinity for the ACE2 cellular receptor, decreased sensitivity to neutralising antibodies, and may escape the immune responses elicited by t…”
BackgroundSgorlon, G., Silva-Flannery, L. M., Silva, J. F., Siza, C. R., Esteves, R., Marston, B. J., Morgan, J., Pluciński, M. M., Roca, T. P., Silva, A. M. P., et al. (2022) · Journal of Medical Virology · doi:10.1002/jmv.27686 · Cited by 8
“1) variant was first identified in Manaus, the capital of Amazonas, in mild November 2020.(8) From April to June 2021, as part of a household transmission study of the Gamma (P.”
BackgroundSelf-citationHighly Sensitive Lineage Discrimination of SARS-CoV-2 Variants through Allele-Specific Probe PCR
Ratcliff, J., Al-Beidh, F., Bibi, S., Bonsall, D., Clemens, S. C., Estcourt, L., Evans, A., Fish, M., Folegatti, P., Gordon, A., et al. (2022) · Journal of Clinical Microbiology · doi:10.1128/jcm.02283-21 · Cited by 7
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“28, named gamma and zeta, emerged in the Brazilian states of Amazonas and Rio de Janeiro, respectively [41,42].”
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“For example, in Brazil, the gamma variant, first identified in early January 2021, was associated with higher viral loads (~10- fold) in infected patients and to be more transmissible from 1.7 to 2.4 (Faria et al., 2021).”
BackgroundInfluentialInsights into organoid-based modeling of COVID-19 pathology
Boroojerdi, M. H., Jabry, T. A., Mirarefin, S. M. J., & Albalushi, H. M. A. (2023) · Virology Journal · doi:10.1186/s12985-023-01996-2 · Cited by 10
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“The VOC’s establishment has also been responsible for upsurges in cases and deaths in Brazil [18], for example, the collapse of the health system observed in Manaus in early 2021 by Gamma VOC [14,19], the increase in the number of severe cases due to Delta VOC in mid-2021 [20], and finally, the rise in the number of c…”
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Modelling the unexpected dynamics of COVID-19 in Manaus, Brazil
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“In all cases, the method accurately reproduces the two-wave COVID-19 dynamics in Manaus without considering large reinfection rates, as in other studies (Buss et al., 2020; Faria et al., 2021a).”
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Early mutational signatures and transmissibility of SARS-CoV-2 Gamma and Lambda variants in Chile
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“Our estimates reflect better the situation observed in Manaus, Brazil, for P.1, with peak transmissibility at reproduction numbers close to 5 60 .”
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“Additional caveats to the framework developed here includes lack of waning immunity or the possibility of novel SARSCoV-2 variants able to partially evade protective immunity (as in Brazil [2], South Africa [31], and many other countries), nor how emergence of new variants may erode efficacy of previously effective th…”
InfluentialSelf-citationZhao, S., Ran, J., & Han, L. (2021) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.21-0412 · Cited by 7
“possible transmission advantage over their preceding variants.(24) On one hand, recent analyses reported evidence”
BackgroundPostvaccination SARS-COV-2 among Health Care Workers in New Jersey: A Genomic Epidemiological Study
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Viral loads observed under competing strain dynamicsPreprint
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“However, such data are 47 rare, and comparisons of viral loads have therefore typically been done using routinely 48 collected RT-qPCR surveillance data from asymptomatic or symptomatic individuals [5,22].”
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SARS-COV-2 γ variant acquires spike P681H or P681R for improved viral fitnessPreprint
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Integrating Fréchet distance and AI reveals the evolutionary trajectory and origin of SARS‐CoV‐2
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Novel Highly Divergent SARS-CoV-2 Lineage With the Spike Substitutions L249S and E484K
Laiton‐Donato, K., Usme-Ciro, J. A., Franco-Muñoz, C., Álvarez-Díaz, D. A., Ruiz-Moreno, H. A., Reales-González, J., Prada-Cardozo, D., Corchuelo, S., Herrera-Sepúlveda, M. T., Naizaque, J., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.697605 · Cited by 7
“1 variant (8), therefore, its effect in combination to S249L or other changes in critical proteins for viral replication (e.”
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Evolution of SARS-CoV-2 during the first year of the COVID-19 pandemic in Northwestern Argentina
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“Our analysis revealed four waves of the SARS-CoV-2 epidemic in the state, with each wave characterized by the circulation and replacement of different viral strains [11,17].”
BackgroundMethodPlans-Rubió, P. (2023) · Vaccines · doi:10.3390/vaccines11121836 · Cited by 7
Subramanian, S., Schnell, G., di Iulio, J., Gupta, A. K., Shapiro, A. E., Sarkis, E. H., Lopuski, A., Peppercorn, A., Aldinger, M., Hebner, C. M., et al. (2023) · Future Virology · doi:10.2217/fvl-2023-0146 · Cited by 7
“Additionally, the VOC / VOI detected in COMET-ICE participants included the Alpha, Epsilon, Gamma, Iota, Lambda, Zeta and B.1.1.519 variants, which corresponds with the circulating strains during that time [29 , 38–40] .”
BackgroundInfluentialTambe, L. A. M., Mathobo, P., Matume, N. D., Munzhedzi, M., Edokpayi, J. N., Viraragavan, A., Glanzmann, B., Tebit, D. M., Mavhandu-Ramarumo, L. G., Street, R. A., et al. (2023) · Frontiers in Public Health · doi:10.3389/fpubh.2023.1309869 · Cited by 7
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“This beta variant contains 9 different spike mutations (Table 1) including L18F, D614G, L18F, A701V, E484K, K417 N, R2461, D215G, and D80A (Tegally et al., 2020).”
BackgroundResearch progress of spike protein mutation of SARS-CoV-2 mutant strain and antibody development
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Molecular surveillance of the on-going SARS-COV-2 epidemic in Ribeirao Preto City, Brazil
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“1 VOC compared to the initial strains led to unprecedented rise in the SARS-CoV-2 cases between November–December 2020 (Faria et al., 2021; Naveca et al., 2021) despite of the high SARS-CoV-2 seroprevalence.”
BackgroundTransmission of SARS-CoV-2 Indoor and Outdoor Environments
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Scrima, M., Cossu, A. M., D’Andrea, E. L., Bocchetti, M., Abruzzese, Y., Iannarone, C., Miarelli, C., Grisolia, P., Melisi, F., Genua, L., et al. (2022) · Frontiers in Virology · doi:10.3389/fviro.2022.814114 · Cited by 7
“1) (15), and 15 with low frequency in all lineages (L54F, R78K, T95I, Y144F, L189F, A222V, N439K, S477N, V772I, Y789N, P812S, S813N, H1101Y, T1117I, and Q1201K) distributed in all four different spike protein domains (S2, S1-N terminal, RBD, and S1-C terminal) as indicated in Figure 4.”
BackgroundAbduljaleel, Z., Shahzad, N., Aziz, S. A., & Malik, S. M. (2022) · Molecular Diversity · doi:10.1007/s11030-022-10449-x · Cited by 7
Effects of Vaccination and the Spatio‐Temporal Diffusion of Covid‐19 Incidence in Turkey
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“4 times more contagious than wild type (Faria et al., 2021) and Delta variant is the most contagious of all its predecessors (Mahase, 2021).”
BackgroundTakaoka, Y., Sugano, A., Morinaga, Y., Ohta, M., Miura, K., Kataguchi, H., Kumaoka, M., Kimura, S., & Maniwa, Y. (2022) · bioRxiv · doi:10.1016/j.mran.2022.100227 · Cited by 6
Ward, B., Yombi, J. C., Balligand, J., Cani, P. D., Collet, J., Greef, J. D., Dewulf, J. P., Gatto, L., Haufroid, V., Jodogne, S., et al. (2022) · Viruses · doi:10.3390/v14071373 · Cited by 7
Barbosa, P. M., Júnior, F. C. D. S., Lima, G. M. C., Bertini, S., de Lima, R. R., Furuta, K. A., Mapa, C. H., Roschel, L., & de Oliveira, E. S. (2022) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x2022e11959 · Cited by 7
“4% of the samples from January 2021 (2,10,11).”
BackgroundResultInfluentialHu, Y., Wang, K., & Wang, W. (2022) · Bulletin of Mathematical Biology · doi:10.1007/s11538-022-01050-2 · Cited by 7
“A variety of mutant viruses have occurred, such as α-virus in British (Davies et al. 2021), β-virus in South Africa (Tegally et al. 2020), γ -virus in Brazil (Faria et al. 2021), δ-virus in India (Campbell et al. 2021) and the latest Omicron-virus (Karim and Karim2021).”
BackgroundRecursive state and parameter estimation of COVID-19 circulating variants dynamics
Silva, D. M., & Secchi, A. R. (2022) · Scientific Reports · doi:10.1038/s41598-022-18208-6 · Cited by 7
Croda, M. G., Barbosa, M. D. S., Marchioro, S. B., do Nascimento, D. D. G., Melo, E. C. P., Cruz, O. G., Torres, A., de Oliveira, L. A., Ganem, F., & Simionatto, S. (2022) · Revista do Instituto de Medicina Tropical de São Paulo · doi:10.1590/s1678-9946202264069 · Cited by 7
Scale-free dynamics of COVID-19 in a Brazilian city
Policarpo, J. M. P., Ramos, A. A. G. F., Dye, C., Faria, N. R., Leal, F. E., Moraes, O. J. S., Parag, K. V., Peixoto, P. S., Buss, L., Sabino, É. C., et al. (2023) · Applied Mathematical Modelling · doi:10.1016/j.apm.2023.03.039 · Cited by 7
Self-citationCOVID-19: A Pediatric Update in Epidemiology, Management, Prevention, and Long-term Effects
Inagaki, K., & Hobbs, C. V. (2023) · Pediatrics in Review · doi:10.1542/pir.2022-005686 · Cited by 7
Seroprevalence of SARS-CoV-2 in Brazil: A systematic review and meta-analysis
Figueiredo, G. M., Tengan, F. M., Campos, S. R. D. S. L. D. C., & Luna, E. J. D. A. (2023) · Clinics · doi:10.1016/j.clinsp.2023.100233 · Cited by 7
Miotto, M., Rienzo, L. D., Grassmann, G., Desantis, F., Cidonio, G., Gosti, G., Leonetti, M., Ruocco, G., & Milanetti, E. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1205919 · Cited by 7
“Beta and gamma only differ for the substitution at position 417; even if the corresponding single experimental mutations (K417N and K417T) have different numbers of contacts, the two variants show no difference.”
BackgroundInfluentialda Costa, A. C., Mendes-Corrêa, M. C., Tozetto‐Mendoza, T. R., Villas-Boas, L. S., de Paula, A. V., Paião, H. G. O., Leal, F. E., Ferreira, N. E., Honorato, L., Leal, E. D. S., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0291027 · Cited by 7
“SARS-CoV-2 complementary DNA was also sequenced using the MinION platform (Oxford Nanopore Technologies, UK) and Miseq (Illumina, San Diego, CA, USA) to detect the B1 and Gamma strain variants [16].”
MethodSelf-citationRucker, G., Qin, H., & Zhang, L. (2023) · PLoS ONE · doi:10.1371/journal.pone.0289432 · Cited by 12
Spatiotemporal transmission of SARS-CoV-2 lineages during 2020–2021 in Pernambuco—Brazil
Machado, L. C., Dezordi, F. Z., de Lima, G. B., de Lima, R. E., Silva, L. C. A., Pereira, L. D. M., da Silva, A. F., Neto, A. M. D. S., de Oliveira, A. L. S., Armstrong, A. D. C., et al. (2024) · Microbiology Spectrum · doi:10.1128/spectrum.04218-23 · Cited by 6
Phylo2Vec: A Vector Representation for Binary Trees
Penn, M. J., Scheidwasser, N., Khurana, M. P., Duchêne, D. A., Donnelly, C. A., & Bhatt, S. (2024) · Systematic Biology · doi:10.1093/sysbio/syae030 · Cited by 7
“…cal sciences, phylogenetic trees are integral to multiple research domains, including evolution (Morlon et al. 2010), conservation (Rolland et al. 2011), and epidemiol‑ ogy, where they allow us to better understand infectious disease transmission dynamics (Ypma et al. 2013; Faria et al. 2021).”
Self-citationHassan, S. S., Basu, P., Redwan, E. M. M. M., Lundstrom, K. H., Choudhury, P. P., Serrano‐Aroca, Á., Azad, G. K., Aljabali, A. A. A., Palù, G., El‐Aziz, T. M. A., et al. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112092 · Cited by 7
“Of note, the majority of Manaus (Brazil) citizens had been reinfected with the P.1 strain bearing these mutations, which may offer a further capability of immune escape (Faria et al., 2021).”
Zhao, S., Musa, S. S., Chong, K. C., Ran, J., Javanbakht, M., Han, L., Wang, K., Hussaini, N., Habib, A. G., Wang, M. H., et al. (2021) · Journal of Global Health · doi:10.7189/jogh.11.05028 · Cited by 7
dos Santos, V. B., Stein, A. T., Barilli, S. L. S., Garbini, A. F., de Almeida, R. C., Carazai, D. D. R., dos Santos, F. C., Lutkmeier, R., Greve, I. H., Klafke, A., et al. (2022) · Revista do Instituto de Medicina Tropical de São Paulo · doi:10.1590/s1678-9946202264020 · Cited by 7
Silva, A. V. F. G., Menezes, D., Moreira, F. R. R., Torres, O. A., Fonseca, P. L. C., Moreira, R. G., Alves, H. J., Alves, V. R., Amaral, T. M. D. R., Coelho, A. N., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.799713 · Cited by 7
“In December 2020, Manaus, the largest city in the North Region, experienced a resurgence of COVID-19 (Sabino et al., 2021) despite high seroprevalence (Buss et al., 2021), likely due to the gamma variant (Faria et al., 2021).”
BackgroundInfluentialSelf-citationPalyanova, N. V., Sobolev, I. A., Alekseev, А. Y., Glushenko, A., Kazachkova, E., Markhaev, A. G., Коnonova, Y. V., Gulyaeva, M. A., Сергеевна, А. Л., Kurskaya, O., et al. (2022) · Viruses · doi:10.3390/v14092036 · Cited by 7
Tan, J., Wu, Z., Hu, P., Gan, L., Wang, Y., & Zhang, D. (2022) · Pathogens · doi:10.3390/pathogens11091008 · Cited by 7
Oliveira, J. R., Machado, R. R. G., Arcuri, H. A., Magawa, J. Y., Daher, I. P., Urbanski, A. H., Schmitz, G. J. H., Silva, R. C. V., Durigon, E. L., Boscardin, S. B., et al. (2021) · medRxiv · doi:10.1101/2021.03.11.21253399 · Cited by 6
The new SARS-CoV-2 variant and reinfection in the resurgence of COVID-19 outbreaks in Manaus, BrazilPreprint
He, D., Fan, G., Wang, X., Li, Y., & Peng, Z. (2021) · medRxiv · doi:10.1101/2021.03.25.21254281 · Cited by 7
“A two-strain model It was reported that P1 strain could have caused the second wave in Manaus with a large amount of reinfections (13-15).”
BackgroundResultViral sequencing to inform the global elimination of dog-mediated rabies - a systematic review
Jaswant, G., Bautista, C. T., Ogoti, B. M., Changalucha, J. J., Oyugi, J. O., Campbell, K., Mutunga, M., Thumbi, S. M., Hampson, K., & Brunker, K. (2024) · One Health & Implementation Research · doi:10.20517/ohir.2023.61 · Cited by 6
Moussaoui, M. E., Bontems, S., Meex, C., Hayette, M., Lejeune, M., Hong, S. L., Dellicour, S., Moutschen, M. P., Cambisano, N., Renotte, N., et al. (2024) · Virus Evolution · doi:10.1093/ve/veae073 · Cited by 7
“Unlike the aforementioned amino acid changes, NSP3:K977Q has previously been observed in a VOC (Gamma, P.1) and has been detected in the context of chronic infections as well as within cryptic lineages sampled from wastewater (Faria et al. 2021, Gregory et al. 2022, Nabieva et al. 2023).”
BackgroundIntranasal liposomal remdesivir induces SARS-CoV-2 clearance in K18-hACE2 mice and ensures survival.
Mendes, S., Guimaraes, L. C., de Oliveira, L. C., Costa, P., da Silva, N. J. A., Pereira, G., Fernandez, C. C., Figueiredo, M. M., Santos, R. A. D. D., Teixeira, M. M., et al. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.01.044 · Cited by 6
National investment case development for pathogen genomics
Khoo, Y. K., Wulandari, S., Getchell, M., Moe, L., Kumar, S., Liu, E. J., Sun, Y., Pang, J., Mishra, S., Clapham, H., et al. (2025) · Cell Genomics · doi:10.1016/j.xgen.2025.100781 · Cited by 6
Self-citationMolecular mechanisms of SARS-CoV-2 entry: implications for biomedical strategies
Santamaria-Castro, I., Leiva-Rebollo, R., Marín‐Wong, S., Jiménez-Guardeño, J. M., & Ortega‐Prieto, A. M. (2025) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00260-24 · Cited by 7
SARS‐CoV‐2 Variants and Immune Evasion: Mapping the Future of Vaccine Design
Üzer, F., Erendor, F., & Şanlıoğlu, S. (2026) · Reviews in Medical Virology · doi:10.1002/rmv.70157 · Cited by 6
“JN. Phase II (late 2020–early 2021) was defined by the emergence of early VOCs such as Alpha (B.1.1.7), Beta (B.1.351), and Gamma (P.1) which reflected convergent evolutionary responses to rising population immunity [7–10].”
InfluentialDetection of SARS-CoV-2 variant 501Y.V2 in Comoros Islands in January 2021
Agoti, C. N., Githinji, G., Mohammed, K. S., Lambisia, A. W., de Laurent, Z. R., Mburu, M. W., Ong’era, E. M., Morobe, J. M., Otieno, E. G., Azali, H. A., et al. (2021) · Wellcome Open Research · doi:10.12688/wellcomeopenres.16889.1 · Cited by 5
Mwangi, P. N., Okendo, J., Mogotsi, M. T., Ogunbayo, A. E., Adelabu, O. A., Sondlane, H., Maotoana, M. G., Mahomed, L., Morobadi, M. D., Vawda, S., et al. (2022) · Frontiers in Virology · doi:10.3389/fviro.2022.935131 · Cited by 6
Genomic landscape of the SARS-CoV-2 pandemic in Brazil suggests an external P.1 variant origin
Perico, C. P., Pierri, C. R. D., Neto, G. P., Fernandes, D. R., Pedrosa, F. O., de Souza, E. M., & Raittz, R. T. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1037455 · Cited by 6
Houdroge, F., Palmer, A. Y., Delport, D., Walsh, T., Kelly, S. L., Hainsworth, S. W., Abeysuriya, R., Stuart, R. M., Kerr, C. C., COPLAN, P. M., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-27711-3 · Cited by 6
Yu, B., Xu, C., Huang, S., Ni, J., Zhou, J., Zhang, Y., Wu, M., Zhang, J., & Fang, L. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1181097 · Cited by 6
Li, J., Zhang, Q., Xu, C., Zhang, Y., Lu, Y., Ai, M., & Tan, X. (2023) · BMC Gastroenterology · doi:10.1186/s12876-023-02907-z · Cited by 6
Focused Review: Insight and Updates on COVID-19 from Progress in Microbes and Molecular Biology
Thye, A. Y.-K., & Law, J. W. (2023) · Progress In Microbes & Molecular Biology · doi:10.36877/pmmb.a0000333 · Cited by 6
“Its emergence marks the start of Manaus’s second COVID-19 wave, and in January 2021, it was associated with 87% of all infections [10,110] .”
Barreto-Vieira, D. F., Bandeira, D. M., da Silva, M. A. N., de Almeida, A. L. T., Araújo, M., Machado, A. B., Tort, L. F. L., Nacife, V. P., Siqueira, M. M., Motta, F. C., et al. (2023) · The Brazilian Journal of Infectious Diseases · doi:10.1016/j.bjid.2023.103706 · Cited by 6
Studying SARS-CoV-2 interactions using phage-displayed receptor binding domain as a model protein
Pérez-Massón, B., Quintana-Perez, Y., Tundidor, Y., Pérez‐Martínez, D., Castro-Martínez, C., Pupo-Meriño, M., Orosa-Vázquez, I., Relova-Hernández, E., Villegas, R., Guirola, O., et al. (2024) · Scientific Reports · doi:10.1038/s41598-023-50450-4 · Cited by 6
“It also appeared in Beta 17 , Gamma 18 and in the expanding Omicron family 20 of VOC, playing a dominant role in viral evolution.”
Combe, M., Chérif, E., Deremarque, T., Rivera‐Ingraham, G. A., Seck-Thiam, F., Justy, F., Doudou, J.-C., Carod, J.-F., Carage, T., Procureur, A., et al. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.171645 · Cited by 6
Norwood, K., Deng, Z.-L., Reimering, S., Robertson, G., Foroughmand-Araabi, M.-H., Goliaei, S., Hölzer, M., Klawonn, F., & McHardy, A. C. (2025) · Nature Communications · doi:10.1038/s41467-025-60231-4 · Cited by 10
“…saltatory evolution of SARS-CoV-2 and the emergence of highly divergent variants like the Omicron BA.2 and BA.5 lineages will usually lead to noticeable changes in the virus phenotype (see https://www.nature.com/articles/s41579-023-00878-2 and https://www.nature.com/articles/s41579-022-00841-7).”
Metaviromic identification of discriminative genomic features in SARS-CoV-2 using machine learning
Park, J. J.-Y., & Chen, S. (2021) · Patterns · doi:10.1016/j.patter.2021.100407 · Cited by 6
Genomic monitoring of the SARS-CoV-2 B1.1.7 (WHO VOC Alpha) in the Sao Paulo state, Brazil
Slavov, S. N., Bezerra, R. D. S., Rodrigues, E. S., Santos, E. V., Borges, J. S., de La‐Roque, D. G. L., Patané, J. S. L., Lima, A. R. J., Ribeiro, G. D. C., Viala, V. L., et al. (2021) · Virus Research · doi:10.1016/j.virusres.2021.198643 · Cited by 6
Fumagalli, M. J., de Castro-Jorge, L. A., de Souza, W. M., de Azevedo, P. O., Hansen, A. W., Gazzinelli, R. T., da Fonseca, B. A. L., Spilki, F. R., & Figueiredo, L. T. M. (2022) · Viruses · doi:10.3390/v14020305 · Cited by 6
Self-citationChiang, C.-Y., Chen, M., Hsu, C.-W., Liu, C., Tsai, Y.-W., Liao, H., Yan, J., Chuang, Z.-S., Wang, H.-I., Pan, C.-H., et al. (2022) · Journal of Biomedical Science · doi:10.1186/s12929-022-00823-0 · Cited by 6
Ciubotariu, I. I., Dorman, J., Perry, N. M., Gorenstein, L., Kattoor, J. J., Fola, A. A., Zine, A., Hendrix, G. K., Wilkes, R. P., Kitchen, A., et al. (2022) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofac268 · Cited by 6
The past, present and future of genomics and bioinformatics: A survey of Brazilian scientists
Rocha, M., Massarani, L., SOUZA, S. J. D., & de Vasconcelos, A. T. R. (2022) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2021-0354 · Cited by 6
“…of the SARS-CoV-2 virus, which caused the COVID-19 pandemic (Araujo et al. , 2020; Jesus et al. , 2020), and to study the spread of the virus in the country since March 2020 (Candido et al. , 2020; Silva Francisco Jr et al. , 2020; Buss et al. , 2021; Faria et al. , 2021; Voloch et al. , 2021).”
Novel Lateral Flow-Based Assay for Simple and Visual Detection of SARS-CoV-2 Mutations
Gomez-Martinez, J., Henry, S., Tuaillon, É., de Perre, P. V., Fournier‐Wirth, C., Foulongne, V., & Brès, J.-C. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.902914 · Cited by 6
Ferreira, M. U., Giacomini, I., Sato, P. D. M., Lourenço, B. H., Nicolete, V. C., Buss, L., Matijasevich, A., Castro, M. C., Cardoso, M. A., & for the MINA-Brazil Working Group (2022) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0010580 · Cited by 6
Grikscheit, K., Rabenau, H. F., Ghodratian, Z., Widera, M., Wilhelm, A., Toptan, T., Hoehl, S., Layer, E., Helfritz, F., & Ciesek, S. (2022) · Vaccines · doi:10.3390/vaccines10071163 · Cited by 7
“1) [13] revealed dominant immune escape capacities.”
Metadata
- Authors
- Faria, N. R., Mellan, T. A., Whittaker, C., Claro, I. M., Candido, D. D. S., Mishra, S., Crispim, M. A. E., Sales, F. C. S., Hawryluk, I., McCrone, J. T., Hulswit, R. J. G., Franco, L. A. M., Ramundo, M. S., de Jesus, J. G., Andrade, P. S., Coletti, T. M., Ferreira, G. M., Silva, C. A. M., Manuli, E. R., Pereira, R. H. M., Peixoto, P. S., Kraemer, M. U. G., Gaburo, N., Camilo, C. D. C., Hoeltgebaum, H., Souza, W. M., Rocha, E. C., de Souza, L. M., de Pinho, M. C., Araujo, L. J. T., Malta, F. S. V., de Lima, A. B., Silva, J. D. P., Zauli, D. A. G., Ferreira, A. C. D. S., Schnekenberg, R. P., Laydon, D. J., Walker, P. G. T., Schlüter, H. M., dos Santos, A. L. P., Vidal, M. S., Del Caro, V. S., Filho, R. M. F., dos Santos, H. M., Aguiar, R. S., Proença-Modena, J. L., Nelson, B., Hay, J. A., Monod, M., Miscouridou, X., Coupland, H., Sonabend, R., Vollmer, M., Gandy, A., Prete, C. A., Nascimento, V. H., Suchard, M. A., Bowden, T. A., Pond, S. L. K., Wu, C.-H., Ratmann, O., Ferguson, N. M., Dye, C., Loman, N. J., Lemey, P., Rambaut, A., Fraiji, N. A., Carvalho, M. D. P. S. S., Pybus, O. G., Flaxman, S., Bhatt, S., & Sabino, E. C.
- Affiliations
- Universidade de São Paulo (BR)
- Imperial College London (GB)
- Instituto de Medicina Tropical, Faculdade de Medicina da Universidade de São Paulo, São Paulo, Brazil.
- Fundação Hospitalar de Hematologia e Hemoterapia do Amazonas (BR)
- University of Edinburgh (GB)
- Centre for Human Genetics (GB)
- Departamento de Epidemiologia, Faculdade de Saúde Pública da Universidade de São Paulo, Sao Paulo, Brazil.
- Universidade Federal de Uberlândia (BR)
- Institute of Applied Economic Research (BR)
- University of Oxford (GB)
- DB Diagnósticos do Brasil, São Paulo, Brazil.
- Laboratory of Quantitative Pathology, Center of Pathology, Adolfo Lutz Institute, São Paulo, Brazil.
- Instituto Hermes Pardini, Belo Horizonte, Brazil.
- CDL Laboratório Santos e Vidal, Manaus, Brazil.
- Universidade Federal de Minas Gerais (BR)
- Laboratory of Emerging Viruses, Department of Genetics, Evolution, Microbiology, and Immunology, Institute of Biology, University of Campinas (UNICAMP), São Paulo, Brazil.
- Instituto Nacional de Pesquisas da Amazônia (BR)
- Harvard University (US)
- Departamento de Engenharia de Sistemas Eletrônicos, Escola Politécnica da Universidade de São Paulo, São Paulo, Brazil.
- University of California, Los Angeles (US)
- Temple University (US)
- University of Southampton (GB)
- Institute for Microbiology and Infection, University of Birmingham, Birmingham, UK.
- Rega Institute for Medical Research (BE)
- Royal Veterinary College (GB)
- University of Copenhagen (DK)
- Corresponding author
- Faria, Nuno R.
- Mellan, Thomas A.
- Whittaker, Charles
- Claro, Ingra M.
- Mishra, Swapnil
- Pybus, Oliver G.
- Flaxman, Seth
- Bhatt, Samir
- ORCID
- Faria, Nuno R.
- Mellan, Thomas A.
- Whittaker, Charles
- Claro, Ingra M.
- Candido, Darlan da S.
- Mishra, Swapnil
- Crispim, Myuki A. E.
- Sales, Flavia C. S.
- Hawryluk, Iwona
- McCrone, John T.
- Hulswit, Ruben J. G.
- Franco, Lucas A. M.
- Ramundo, Mariana S.
- de Jesus, Jaqueline G.
- Andrade, Pamela S.
- Coletti, Thais M.
- Ferreira, Giulia M.
- Silva, Camila A. M.
- Manuli, Erika R.
- Pereira, Rafael H. M.
- Peixoto, Pedro S.
- Kraemer, Moritz U. G.
- Gaburo, Nelson
- Camilo, Cecilia da C.
- Hoeltgebaum, Henrique
- Souza, William M.
- Rocha, Esmenia C.
- de Souza, Leandro M.
- de Pinho, Mariana C.
- Araujo, Leonardo J. T.
- Malta, Frederico S. V.
- de Lima, Aline B.
- Silva, Joice do P.
- Zauli, Danielle A. G.
- Ferreira, Alessandro C. de S.
- Schnekenberg, Ricardo P.
- Laydon, Daniel J.
- Walker, Patrick G. T.
- Schlüter, Hannah M.
- dos Santos, Ana L. P.
- Vidal, Maria S.
- Del Caro, Valentina S.
- Aguiar, Renato S.
- Proença-Modena, José L.
- Nelson, Bruce
- Hay, James A.
- Monod, Mélodie
- Coupland, Helen
- Sonabend, Raphael
- Vollmer, Michaela
- Gandy, Axel
- Prete, Carlos A.
- Nascimento, Vitor H.
- Suchard, Marc A.
- Bowden, Thomas A.
- Pond, Sergei L. K.
- Wu, Chieh-Hsi
- Ratmann, Oliver
- Ferguson, Neil M.
- Dye, Christopher
- Loman, Nick J.
- Lemey, Philippe
- Rambaut, Andrew
- Fraiji, Nelson A.
- Carvalho, Maria do P. S. S.
- Pybus, Oliver G.
- Flaxman, Seth
- Bhatt, Samir
- Sabino, Ester C.
- Venue
- Science
- Published
- 2021-05-21
- Volume
- 372
- Issue
- 6544
- Pages
- 815-821
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC8139423
- OpenAlex
- W3156343712
- Cited by
- 1,461
- References
- 93
- Citations by year
- 2026: 48 · 2025: 73 · 2024: 104 · 2023: 227 · 2022: 492 · 2021: 502
- FWCI
- 105.79
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Science (publishedVersion, cc-by)
- medRxiv (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (publishedVersion, cc-by)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- Spiral (Imperial College London) (submittedVersion, cc-by)
- PubMed Central (submittedVersion, cc-by-nc-nd)
- ePrints Soton (University of Southampton) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Lirias (KU Leuven) (submittedVersion, other-oa)
- TUScholarShare (Temple University) (submittedVersion, cc-by)
- Funders
- Medical Research Council (MR/S0195/1)
- National Institute for Health Research (203141/Z/16/Z, MR/S007555/1, ALTF 869-2019, OPP1175094, 2018/12579-7 CNP)
- Wellcome Trust and Royal Society (204311/Z/16/Z)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Physical Sciences › Mathematics › Modeling and Simulation › COVID-19 epidemiological studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- P.1 lineage, SARS-CoV-2, COVID-19 pandemic, variants of concern, spike protein mutations, E484K, N501Y, ACE2 binding, transmissibility, immune evasion, molecular clock, epidemic resurgence, Manaus, genomic surveillance
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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