Genomic epidemiology of the SARS-CoV-2 epidemic in Brazil.


Journal

Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869

Informations de publication

Date de publication:
09 2022
Historique:
received: 07 10 2021
accepted: 28 06 2022
pubmed: 19 8 2022
medline: 31 8 2022
entrez: 18 8 2022
Statut: ppublish

Résumé

The high numbers of COVID-19 cases and deaths in Brazil have made Latin America an epicentre of the pandemic. SARS-CoV-2 established sustained transmission in Brazil early in the pandemic, but important gaps remain in our understanding of virus transmission dynamics at a national scale. We use 17,135 near-complete genomes sampled from 27 Brazilian states and bordering country Paraguay. From March to November 2020, we detected co-circulation of multiple viral lineages that were linked to multiple importations (predominantly from Europe). After November 2020, we detected large, local transmission clusters within the country. In the absence of effective restriction measures, the epidemic progressed, and in January 2021 there was emergence and onward spread, both within and abroad, of variants of concern and variants under monitoring, including Gamma (P.1) and Zeta (P.2). We also characterized a genomic overview of the epidemic in Paraguay and detected evidence of importation of SARS-CoV-2 ancestor lineages and variants of concern from Brazil. Our findings show that genomic surveillance in Brazil enabled assessment of the real-time spread of emerging SARS-CoV-2 variants.

Identifiants

pubmed: 35982313
doi: 10.1038/s41564-022-01191-z
pii: 10.1038/s41564-022-01191-z
pmc: PMC9417986
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1490-1500

Subventions

Organisme : World Health Organization
ID : 001
Pays : International
Organisme : NIAID NIH HHS
ID : U01 AI151698
Pays : United States

Commentaires et corrections

Type : UpdateOf

Informations de copyright

© 2022. The Author(s).

Références

Coronavirus Disease (COVID-19) Situation Reports (WHO, 20 June 2022); https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports
COVID-19 Map (Johns Hopkins Coronavirus Resource Center, 20 June 2022); https://coronavirus.jhu.edu/map.html
COVID-19 Situation Reports (Pan American Health Organization (PAHO)/WHO, 20 June 2022); https://www.paho.org/en/covid-19-situation-reports
Candido, D. S. et al. Evolution and epidemic spread of SARS-CoV-2 in Brazil. Science 369, 1255–1260 (2020).
pubmed: 32703910 doi: 10.1126/science.abd2161
Xavier, J. et al. The ongoing COVID-19 epidemic in Minas Gerais, Brazil: insights from epidemiological data and SARS-CoV-2 whole genome sequencing. Emerg. Microbes Infect. 9, 1824–1834 (2020).
pubmed: 32726185 pmcid: 7473129 doi: 10.1080/22221751.2020.1803146
Coronavírus Brasil (WHO, 20 June 2022); https://covid.saude.gov.br/
Cota, W. Monitoring the Number of Covid-19 Cases in Brazil (Universidade Federal de Vicosa, 20 June 2022); https://covid19br.wcota.me/en/
Faria de Moura Villela, E. et al. COVID-19 outbreak in Brazil: adherence to national preventive measures and impact on people’s lives, an online survey. BMC Public Health 21, 152 (2021).
pubmed: 33461508 pmcid: 7812554 doi: 10.1186/s12889-021-10222-z
Pinto Neto, O. et al. Mathematical model of COVID-19 intervention scenarios for Sao Paulo—Brazil. Nat. Commun. 12, 418 (2021).
pubmed: 33462211 pmcid: 7814036 doi: 10.1038/s41467-020-20687-y
Monteiro de Oliveira, M., Fuller, T. L., Brasil, P., Gabaglia, C. R. & Nielsen-Saines, K. Controlling the COVID-19 pandemic in Brazil: a challenge of continental proportions. Nat. Med. 26, 1505–1506 (2020).
pubmed: 32887951 doi: 10.1038/s41591-020-1071-5
Candido, D. D. S. et al. Routes for COVID-19 importation in Brazil. J. Travel Med. 27, taaa042 (2020).
pubmed: 32211799 pmcid: 7184379 doi: 10.1093/jtm/taaa042
Naveca, F. G. et al. COVID-19 in Amazonas, Brazil, was driven by the persistence of endemic lineages and P.1 emergence. Nat. Med. 27, 1230–1238 (2021).
pubmed: 34035535 doi: 10.1038/s41591-021-01378-7
Sant’Anna, F. H. et al. Emergence of the novel SARS-CoV-2 lineage VUI-NP13L and massive spread of P.2 in South Brazil. Emerg. Microbes Infect. 10, 1431–1440 (2021).
pubmed: 34184973 pmcid: 8284128 doi: 10.1080/22221751.2021.1949948
Voloch, C. M. et al. Genomic characterization of a novel SARS-CoV-2 lineage from Rio de Janeiro, Brazil. J. Virol. 95, e00119-21 (2021).
pmcid: 8139668 doi: 10.1128/JVI.00119-21
de Oliveira Andrade, R. Covid-19 is causing the collapse of Brazil’s national health service. Brit. Med. J. 370, m3032 (2020).
pubmed: 32732376 doi: 10.1136/bmj.m3032
Vacinação Contra a Covid-19 no Brasil - #PÁTRIAVACINADA (Brazilian Ministry of Health); https://www.gov.br/saude/pt-br/vacinacao
Vacinas Contra a COVID-19 (Organização Pan-Americana da Saúde (OPAS)/OMS,); https://www.paho.org/pt/vacinas-contra-covid-19
Brazil (COVID19 Vaccine Tracker, 20 June 2022); https://covid19.trackvaccines.org/country/brazil/
Faria, N. R. et al. Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil. Science 372, 815–821 (2021).
pubmed: 33853970 pmcid: 8139423 doi: 10.1126/science.abh2644
Weisblum, Y. et al. Escape from neutralizing antibodies by SARS-CoV-2 spike protein variants. eLife 9, e61312 (2020).
pubmed: 33112236 pmcid: 7723407 doi: 10.7554/eLife.61312
Nonaka, C. K. V. et al. Genomic evidence of SARS-CoV-2 reinfection involving E484K spike mutation, Brazil. Emerg. Infect. Dis. 27, 1522–1524 (2021).
pubmed: 33605869 pmcid: 8084516 doi: 10.3201/eid2705.210191
Coronavirus Disease 2019 (COVID-19) (Centers for Disease Control and Prevention, 2020); https://www.cdc.gov/coronavirus/2019-ncov/science/science-briefs/scientific-brief-emerging-variants.html
Kraemer, M. U. G. et al. The effect of human mobility and control measures on the COVID-19 epidemic in China. Science 368, 493–497 (2020).
pubmed: 32213647 doi: 10.1126/science.abb4218
Lemey, P. et al. Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2. PLoS Pathog. 10, e1003932 (2014).
pubmed: 24586153 pmcid: 3930559 doi: 10.1371/journal.ppat.1003932
Lu, L. et al. Quantifying predictors for the spatial diffusion of avian influenza virus in China. BMC Evol. Biol. 17, 16 (2017).
pubmed: 28086751 pmcid: 5237338 doi: 10.1186/s12862-016-0845-3
Ganasegeran, K. et al. Influence of population density for COVID-19 spread in Malaysia: an ecological study. Int. J. Environ. Res. Public Health 18, 9866 (2021).
pubmed: 34574790 pmcid: 8468130 doi: 10.3390/ijerph18189866
Magee, D. et al. Combining phylogeography and spatial epidemiology to uncover predictors of H5N1 influenza A virus diffusion. Arch. Virol. 160, 215–224 (2015).
pubmed: 25355432 doi: 10.1007/s00705-014-2262-5
du Plessis, L. et al. Establishment and lineage dynamics of the SARS-CoV-2 epidemic in the UK. Science 371, 708–712 (2021).
pubmed: 33419936 doi: 10.1126/science.abf2946
PAHO Paraguay COVID-19 Response; https://paho-covid19-response-who.hub.arcgis.com/pages/paho-paraguay-covid-19-response
Paraguay: WHO Coronavirus Disease (COVID-19) Dashboard With Vaccination Data (WHO, 20 June 2022); https://covid19.who.int
Shu, Y. & McCauley, J. GISAID: global initiative on sharing all influenza data – from vision to reality. Eur. Surveill. 22, 30494 (2017).
doi: 10.2807/1560-7917.ES.2017.22.13.30494
Jorge, D. C. P. et al. Assessing the nationwide impact of COVID-19 mitigation policies on the transmission rate of SARS-CoV-2 in Brazil. Epidemics 35, 100465 (2021).
pubmed: 33984687 pmcid: 8106524 doi: 10.1016/j.epidem.2021.100465
Victora, P. C. et al. Estimating the early impact of vaccination against COVID-19 on deaths among elderly people in Brazil: analyses of routinely-collected data on vaccine coverage and mortality. EClinicalMedicine 38, 101 (2021).
doi: 10.1016/j.eclinm.2021.101036
Quick, J. nCoV-2019 sequencing protocol (2020); https://doi.org/10.17504/protocols.io.bbmuik6w
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404 pmcid: 4103590 doi: 10.1093/bioinformatics/btu170
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191
Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).
pubmed: 33590861 pmcid: 7931819 doi: 10.1093/gigascience/giab008
Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).
pubmed: 25409509 pmcid: 4237348 doi: 10.1371/journal.pone.0112963
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234 doi: 10.1093/bioinformatics/btp324
Shen, W. et al. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE 11, e0163962 (2016).
pubmed: 27706213 pmcid: 5051824 doi: 10.1371/journal.pone.0163962
Vilsker, M. et al. Genome Detective: an automated system for virus identification from high-throughput sequencing data. Bioinformatics 35, 871–873 (2019).
pubmed: 30124794 doi: 10.1093/bioinformatics/bty695
Katoh, K. et al. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690 pmcid: 3603318 doi: 10.1093/molbev/mst010
Rambaut, A., Lam, T. T., Max Carvalho, L. & Pybus, O. G. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2, vew007 (2016).
pubmed: 27774300 pmcid: 4989882 doi: 10.1093/ve/vew007
Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).
pubmed: 32011700 pmcid: 7182206 doi: 10.1093/molbev/msaa015
Sagulenko, P., Puller, V. & Neher, R. A. TreeTime: maximum-likelihood phylodynamic analysis. Virus Evol. 4, vex042 (2018).
pubmed: 29340210 pmcid: 5758920 doi: 10.1093/ve/vex042
Rambaut, A. et al. A dynamic nomenclature proposal for SARS-CoV-2 lineages to assist genomic epidemiology. Nat. Microbiol. 5, 1403–1407 (2020).
pubmed: 32669681 pmcid: 7610519 doi: 10.1038/s41564-020-0770-5
Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016 (2018).
pubmed: 29942656 pmcid: 6007674 doi: 10.1093/ve/vey016
Tegally, H. et al. Sixteen novel lineages of SARS-CoV-2 in South Africa. Nat. Med. 27, 440–446 (2021).
pubmed: 33531709 doi: 10.1038/s41591-021-01255-3
Lemey, P., Rambaut, A., Welch, J. J. & Suchard, M. A. Phylogeography takes a relaxed random walk in continuous space and time. Mol. Biol. Evol. 27, 1877–1885 (2010).
pubmed: 20203288 pmcid: 2915639 doi: 10.1093/molbev/msq067
Dellicour, S. et al. Relax, keep walking - a practical guide to continuous phylogeographic inference with BEAST. Mol. Biol. Evol. 38, 3486–3493 (2021).
pubmed: 33528560 pmcid: 8321535 doi: 10.1093/molbev/msab031
Dellicour, S., Rose, R., Faria, N. R., Lemey, P. & Pybus, O. G. SERAPHIM: studying environmental rasters and phylogenetically informed movements. Bioinformatics 32, 3204–3206 (2016).
pubmed: 27334476 doi: 10.1093/bioinformatics/btw384
Tegally, H. et al. Detection of a SARS-CoV-2 variant of concern in South Africa. Nature 592, 438–443 (2021).
pubmed: 33690265 doi: 10.1038/s41586-021-03402-9
Viana, R. et al. Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa. Nature 603, 679–686 (2022).
pubmed: 35042229 pmcid: 8942855 doi: 10.1038/s41586-022-04411-y
Dellicour, S. et al. Dispersal dynamics of SARS-CoV-2 lineages during the first epidemic wave in New York City. PLoS Pathog. 17, e1009571 (2021).
pubmed: 34015049 pmcid: 8136714 doi: 10.1371/journal.ppat.1009571

Auteurs

Marta Giovanetti (M)

Laboratório de Flavivirus, Fundacao Oswaldo Cruz, Rio de Janeiro, Brazil.
Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
Department of Science and Technology for Humans and the Environment, University of Campus Bio-Medico di Roma, Rome, Italy.

Svetoslav Nanev Slavov (SN)

Blood Center of Ribeirão Preto, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil.
Butantan Institute, São Paulo, Brazil.

Vagner Fonseca (V)

Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
Pan American Health Organization (PAHO)/World Health Organization (WHO), Brasilia, Distrito Federal, Brazil.
Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa.
KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.

Eduan Wilkinson (E)

Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa.
KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.

Houriiyah Tegally (H)

Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa.
KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.

José Salvatore Leister Patané (JSL)

Butantan Institute, São Paulo, Brazil.

Vincent Louis Viala (VL)

Butantan Institute, São Paulo, Brazil.

Emmanuel James San (EJ)

Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking, Stellenbosch University, Stellenbosch, South Africa.
KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.

Evandra Strazza Rodrigues (ES)

Blood Center of Ribeirão Preto, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil.

Elaine Vieira Santos (EV)

Blood Center of Ribeirão Preto, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil.

Flavia Aburjaile (F)

Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.

Joilson Xavier (J)

Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.

Hegger Fritsch (H)

Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.

Talita Emile Ribeiro Adelino (TER)

Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.

Felicidade Pereira (F)

Laboratório Central de Saúde Pública do Estado da Bahia (LACEN-BA), Salvador, Bahia, Brazil.

Arabela Leal (A)

Laboratório Central de Saúde Pública do Estado da Bahia (LACEN-BA), Salvador, Bahia, Brazil.

Felipe Campos de Melo Iani (FCM)

Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.

Glauco de Carvalho Pereira (G)

Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.

Cynthia Vazquez (C)

Laboratório Central de Salud Pública, Asunción, Paraguay.

Gladys Mercedes Estigarribia Sanabria (GME)

Laboratório Central de Salud Pública, Asunción, Paraguay.
Instituto Regional de Investigación em Salud, Universidad Nacional del Caaguazú, Caaguazú, Paraguay.
Laboratório de Biología Molecular, Hospital Regional de Coronel Oviedo, Ministerio de Salud Pública y Bienestar Social, Asunción, Paraguay.

Elaine Cristina de Oliveira (EC)

Laboratório Central de Saúde Pública do Estado de Mato Grosso (LACEN-MT), Cuiabá, Mato Grosso, Brazil.

Luiz Demarchi (L)

Laboratório Central de Saúde Pública do Estado de Mato Grosso do Sul (LACEN-MS), Campo Grande, Mato Grosso do Sul, Brazil.

Julio Croda (J)

Universidade Federal do Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil.

Rafael Dos Santos Bezerra (R)

Blood Center of Ribeirão Preto, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil.

Loyze Paola Oliveira de Lima (L)

Butantan Institute, São Paulo, Brazil.

Antonio Jorge Martins (AJ)

Butantan Institute, São Paulo, Brazil.

Claudia Renata Dos Santos Barros (C)

Butantan Institute, São Paulo, Brazil.

Elaine Cristina Marqueze (EC)

Butantan Institute, São Paulo, Brazil.

Jardelina de Souza Todao Bernardino (J)

Butantan Institute, São Paulo, Brazil.

Debora Botequio Moretti (DB)

Butantan Institute, São Paulo, Brazil.

Ricardo Augusto Brassaloti (RA)

Centro de Genômica Funcional da ESALQ, University of São Paulo, Piracicaba, São Paulo, Brazil.

Raquel de Lello Rocha Campos Cassano (R)

Centro de Genômica Funcional da ESALQ, University of São Paulo, Piracicaba, São Paulo, Brazil.

Pilar Drummond Sampaio Corrêa Mariani (PDSC)

NGS Soluções Genômicas, Piracicaba, São Paulo, Brazil.

João Paulo Kitajima (JP)

Mendelics Análise Genômica, São Paulo, Brazil.

Bibiana Santos (B)

Mendelics Análise Genômica, São Paulo, Brazil.

Rodrigo Proto-Siqueira (R)

Instituto de Biologia Molecular, Laboratório Antonello, Rio Grande do Sul, Brazil.

Vlademir Vicente Cantarelli (VV)

Universidade Federal de Ciencias da Saúde de Porto Alegre (UFCSPA), Universidade Feevale, Grupo Exame Laboratórios, Rio Grande do Sul, Brazil.

Stephane Tosta (S)

Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
Laboratório Central de Saúde Pública do Estado da Bahia (LACEN-BA), Salvador, Bahia, Brazil.

Vanessa Brandão Nardy (VB)

Laboratório Central de Saúde Pública do Estado da Bahia (LACEN-BA), Salvador, Bahia, Brazil.

Luciana Reboredo de Oliveira da Silva (L)

Laboratório Central de Saúde Pública do Estado da Bahia (LACEN-BA), Salvador, Bahia, Brazil.

Marcela Kelly Astete Gómez (MKA)

Laboratório Central de Saúde Pública do Estado da Bahia (LACEN-BA), Salvador, Bahia, Brazil.

Jaqueline Gomes Lima (JG)

Laboratório Central de Saúde Pública do Estado da Bahia (LACEN-BA), Salvador, Bahia, Brazil.

Adriana Aparecida Ribeiro (AA)

Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.

Natália Rocha Guimarães (NR)

Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.

Luiz Takao Watanabe (LT)

Laboratório Central de Saúde Pública do Estado de Mato Grosso (LACEN-MT), Cuiabá, Mato Grosso, Brazil.

Luana Barbosa Da Silva (L)

Laboratório Central de Saúde Pública do Estado de Mato Grosso (LACEN-MT), Cuiabá, Mato Grosso, Brazil.

Raquel da Silva Ferreira (R)

Laboratório Central de Saúde Pública do Estado de Mato Grosso (LACEN-MT), Cuiabá, Mato Grosso, Brazil.

Mara Patricia F da Penha (MPF)

Vigilancia em Saúde do Estado de Mato Grosso, Cuiabá, Mato Grosso, Brazil.

María José Ortega (MJ)

Laboratório Central de Salud Pública, Asunción, Paraguay.

Andrea Gómez de la Fuente (AG)

Laboratório Central de Salud Pública, Asunción, Paraguay.

Shirley Villalba (S)

Laboratório Central de Salud Pública, Asunción, Paraguay.

Juan Torales (J)

Laboratório Central de Salud Pública, Asunción, Paraguay.

María Liz Gamarra (ML)

Laboratório Central de Salud Pública, Asunción, Paraguay.

Carolina Aquino (C)

Laboratório Central de Salud Pública, Asunción, Paraguay.

Gloria Patricia Martínez Figueredo (GPM)

Laboratório Central de Salud Pública, Asunción, Paraguay.
Instituto Regional de Investigación em Salud, Universidad Nacional del Caaguazú, Caaguazú, Paraguay.
Laboratório de Biología Molecular, Hospital Regional de Coronel Oviedo, Ministerio de Salud Pública y Bienestar Social, Asunción, Paraguay.

Wellington Santos Fava (WS)

Universidade Federal do Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil.

Ana Rita C Motta-Castro (ARC)

Universidade Federal do Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil.

James Venturini (J)

Universidade Federal do Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil.

Sandra Maria do Vale Leone de Oliveira (SM)

Universidade Federal do Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil.

Crhistinne Cavalheiro Maymone Gonçalves (CCM)

Secretaria de Saude do Estado do Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil.

Maria do Carmo Debur Rossa (M)

Laboratório Central de Saúde Pública do Estado do Paraná (Lacen-PR), Curitiba, Paraná, Brazil.

Guilherme Nardi Becker (GN)

Laboratório Central de Saúde Pública do Estado do Paraná (Lacen-PR), Curitiba, Paraná, Brazil.

Mayra Presibella Giacomini (MP)

Laboratório Central de Saúde Pública do Estado do Paraná (Lacen-PR), Curitiba, Paraná, Brazil.

Nelson Quallio Marques (NQ)

Laboratório Central de Saúde Pública do Estado do Paraná (Lacen-PR), Curitiba, Paraná, Brazil.

Irina Nastassja Riediger (IN)

Laboratório Central de Saúde Pública do Estado do Paraná (Lacen-PR), Curitiba, Paraná, Brazil.

Sonia Raboni (S)

Hospital de Clínicas da Universidade Federal do Paraná, Curitiba, Paraná, Brazil.

Gabriela Mattoso (G)

Laboratório de Virologia Molecular, Instituto Carlos Chagas/Fiocruz-PR, Curitiba, Paraná, Brazil.

Allan D Cataneo (AD)

Laboratório de Virologia Molecular, Instituto Carlos Chagas/Fiocruz-PR, Curitiba, Paraná, Brazil.

Camila Zanluca (C)

Laboratório de Virologia Molecular, Instituto Carlos Chagas/Fiocruz-PR, Curitiba, Paraná, Brazil.

Claudia N Duarte Dos Santos (CN)

Laboratório de Virologia Molecular, Instituto Carlos Chagas/Fiocruz-PR, Curitiba, Paraná, Brazil.

Patricia Akemi Assato (PA)

Department of Bioprocesses and Biotechnology, School of Agricultural Sciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil.

Felipe Allan da Silva da Costa (F)

Department of Bioprocesses and Biotechnology, School of Agricultural Sciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil.

Mirele Daiana Poleti (MD)

Department of Veterinary Medicine, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, São Paulo, Brazil.

Jessika Cristina Chagas Lesbon (JCC)

Department of Veterinary Medicine, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, São Paulo, Brazil.

Elisangela Chicaroni Mattos (EC)

Department of Veterinary Medicine, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, São Paulo, Brazil.

Cecilia Artico Banho (CA)

Medicine School of São José do Rio Preto (FAMERP), São José do Rio Preto, São Paulo, Brazil.

Lívia Sacchetto (L)

Medicine School of São José do Rio Preto (FAMERP), São José do Rio Preto, São Paulo, Brazil.

Marília Mazzi Moraes (MM)

Medicine School of São José do Rio Preto (FAMERP), São José do Rio Preto, São Paulo, Brazil.

Rejane Maria Tommasini Grotto (RMT)

Department of Bioprocesses and Biotechnology, School of Agricultural Sciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil.
Molecular Biology Laboratory, Applied Biotechnology Laboratory, Clinical Hospital of the Botucatu Medical School, São Paulo, Brazil.

Jayme A Souza-Neto (JA)

Department of Bioprocesses and Biotechnology, School of Agricultural Sciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil.

Maurício Lacerda Nogueira (ML)

Medicine School of São José do Rio Preto (FAMERP), São José do Rio Preto, São Paulo, Brazil.

Heidge Fukumasu (H)

Department of Veterinary Medicine, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, São Paulo, Brazil.

Luiz Lehmann Coutinho (LL)

Centro de Genômica Funcional da ESALQ, University of São Paulo, Piracicaba, São Paulo, Brazil.

Rodrigo Tocantins Calado (RT)

Blood Center of Ribeirão Preto, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil.

Raul Machado Neto (RM)

Butantan Institute, São Paulo, Brazil.

Ana Maria Bispo de Filippis (AM)

Laboratório de Flavivirus, Fundacao Oswaldo Cruz, Rio de Janeiro, Brazil.

Rivaldo Venancio da Cunha (R)

Fundação Oswaldo Cruz, Bio-Manguinhos, Rio de Janeiro, Rio de Janeiro, Brazil.

Carla Freitas (C)

Coordenação Geral dos Laboratórios de Saúde Pública/Secretaria de Vigilância em Saúde, Ministério da Saúde, (CGLAB/SVS-MS), Brasília, Distrito Federal, Brazil.

Cassio Roberto Leonel Peterka (CRL)

Coordenação Geral das Arboviroses, Secretaria de Vigilância em Saúde/Ministério da Saúde (CGARB/SVS-MS), Brasília, Distrito Federal, Brazil.

Cássia de Fátima Rangel Fernandes (C)

Departamento de Imunização e Doenças Transmissíveisa/Secretaria de Vigilancia em Saude, Ministerio da Saude, Brasılia, Distrito Federal, Brazil.

Wildo Navegantes (W)

Pan American Health Organization (PAHO)/World Health Organization (WHO), Brasilia, Distrito Federal, Brazil.

Rodrigo Fabiano do Carmo Said (RF)

Pan American Health Organization (PAHO)/World Health Organization (WHO), Brasilia, Distrito Federal, Brazil.

Carlos F Campelo de A E Melo (CF)

Pan American Health Organization (PAHO)/World Health Organization (WHO), Brasilia, Distrito Federal, Brazil.

Maria Almiron (M)

Pan American Health Organization (PAHO)/World Health Organization (WHO), Brasilia, Distrito Federal, Brazil.

José Lourenço (J)

Department of Zoology, University of Oxford, Oxford, UK.
Biosystems and Integrative Sciences Institute, Universidade de Lisboa, Lisboa, Portugal.

Tulio de Oliveira (T)

KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.
Laboratório Central de Saúde Pública do Estado de Minas Gerais (LACEN-MG), Fundação Ezequiel Dias, Belo Horizonte, Minas Gerais, Brazil.
Centre for the AIDS Programme of Research in South Africa (CAPRISA), Durban, South Africa.
Department of Global Health, University of Washington, Seattle, WA, USA.

Edward C Holmes (EC)

Marie Bashir Institute for Infectious Diseases and Biosecurity, School of Life and Environmental Sciences and School of Medical Sciences, University of Sydney, Sydney, New South Wales, Australia.

Ricardo Haddad (R)

Butantan Institute, São Paulo, Brazil.

Sandra Coccuzzo Sampaio (SC)

Butantan Institute, São Paulo, Brazil. aroli.coccuzzo@butantan.gov.br.

Maria Carolina Elias (MC)

Butantan Institute, São Paulo, Brazil. arolina.eliassabbaga@butantan.gov.br.

Simone Kashima (S)

Blood Center of Ribeirão Preto, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil. skashima@hemocentro.fmrp.usp.br.

Luiz Carlos Junior de Alcantara (LC)

Laboratório de Flavivirus, Fundacao Oswaldo Cruz, Rio de Janeiro, Brazil. luiz.alcantara@ioc.fiocruz.br.
Laboratório de Genética Celular e Molecular, Instituto de Ciências Biologicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil. luiz.alcantara@ioc.fiocruz.br.

Dimas Tadeu Covas (DT)

Blood Center of Ribeirão Preto, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, São Paulo, Brazil. dimas.covas@butantan.gov.br.
Butantan Institute, São Paulo, Brazil. dimas.covas@butantan.gov.br.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH