Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon

Detalhes bibliográficos
Autor(a) principal: Navega, Felipe Gomes
Data de Publicação: 2019
Outros Autores: Claro, Ingra Morales, Giovanetti, Marta, Jesus, Jaqueline Goes de, Xavier, Joilson, Iani, Felipe Campos de Melo, Nascimento, Valdinete Alves do, Souza, Victor Costa de, Silveira, Paola Paz, Lourenço, José, Santillana, Mauricio, Kraemer, Moritz U. G, Quick, Josh, Hill, Sarah C, Thézé, Julien, Carvalho, Rodrigo Dias de Oliveira, Azevedo, Vasco, Salles, Flavia Cristina da Silva, Nunes, Márcio Roberto Teixeira, Lemos, Poliana da Silva, Candido, Darlan da Silva, Pereira, Glauco de Carvalho, Oliveira, Marluce Aparecida Assunção, Meneses, Cátia Alexandra Ribeiro, Maito, Rodrigo Melo, Cunha, Claudeth Rocha Santa Brígida, Campos, Daniela Palha de Sousa, Castilho, Marcia da Costa, Siqueira, Thalita Caroline da Silva, Terra, Tiza Matos, Albuquerque, Carlos Frederico Campelo de, Cruz, Laura Nogueira da, Abreu, André Luiz de, Martins, Divino Valerio, Simões, Daniele Silva de Moraes Vanlume, Aguiar, Renato Santana de, Luz, Sérgio Luiz Bessa, Loman, Nicholas, Pybus, Oliver G, Sabino, Ester Cerdeira, Okumoto, Osnei, Alcantara, Luiz Carlos Júnior, Faria, Nuno Rodrigues
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Digital do Instituto Evandro Chagas (Patuá)
DOI: 10.1371/journal.pntd.0007065.
Texto Completo: https://patua.iec.gov.br/handle/iec/3831
Resumo: Background: Since its first detection in the Caribbean in late 2013, chikungunya virus (CHIKV) has affected 51 countries in the Americas. The CHIKV epidemic in the Americas was caused by the CHIKV-Asian genotype. In August 2014, local transmission of the CHIKV-Asian genotype was detected in the Brazilian Amazon region. However, a distinct lineage, the CHIKV-East-Central-South-America (ECSA)-genotype, was detected nearly simultaneously in Feira de Santana, Bahia state, northeast Brazil. The genomic diversity and the dynamics of CHIKV in the Brazilian Amazon region remains poorly understood despite its importance to better understand the epidemiological spread and public health impact of CHIKV in the country. Methodology/Principal findings: We report a large CHIKV outbreak (5,928 notified cases between August 2014 and August 2018) in Boa vista municipality, capital city of Roraima’s state, located in the Brazilian Amazon region. We generated 20 novel CHIKV-ECSA genomes from the Brazilian Amazon region using MinION portable genome sequencing. Phylogenetic analyses revealed that despite an early introduction of the Asian genotype in 2015 in Roraima, the large CHIKV outbreak in 2017 in Boa Vista was caused by an ECSA-lineage most likely introduced from northeastern Brazil. Epidemiological analyses suggest a basic reproductive number of R0 of 1.66, which translates in an estimated 39 (95% CI: 36 to 45) % of Roraima’s population infected with CHIKV-ECSA. Finally, we find a strong association between Google search activity and the local laboratory-confirmed CHIKV cases in Roraima. Conclusions/Significance: This study highlights the potential of combining traditional surveillance with portable genome sequencing technologies and digital epidemiology to inform public health surveillance in the Amazon region. Our data reveal a large CHIKV-ECSA outbreak in Boa Vista, limited potential for future CHIKV outbreaks, and indicate a replacement of the Asian genotype by the ECSA genotype in the Amazon region.
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spelling Navega, Felipe GomesClaro, Ingra MoralesGiovanetti, MartaJesus, Jaqueline Goes deXavier, JoilsonIani, Felipe Campos de MeloNascimento, Valdinete Alves doSouza, Victor Costa deSilveira, Paola PazLourenço, JoséSantillana, MauricioKraemer, Moritz U. GQuick, JoshHill, Sarah CThézé, JulienCarvalho, Rodrigo Dias de OliveiraAzevedo, VascoSalles, Flavia Cristina da SilvaNunes, Márcio Roberto TeixeiraLemos, Poliana da SilvaCandido, Darlan da SilvaPereira, Glauco de CarvalhoOliveira, Marluce Aparecida AssunçãoMeneses, Cátia Alexandra RibeiroMaito, Rodrigo MeloCunha, Claudeth Rocha Santa BrígidaCampos, Daniela Palha de SousaCastilho, Marcia da CostaSiqueira, Thalita Caroline da SilvaTerra, Tiza MatosAlbuquerque, Carlos Frederico Campelo deCruz, Laura Nogueira daAbreu, André Luiz deMartins, Divino ValerioSimões, Daniele Silva de Moraes VanlumeAguiar, Renato Santana deLuz, Sérgio Luiz BessaLoman, NicholasPybus, Oliver GSabino, Ester CerdeiraOkumoto, OsneiAlcantara, Luiz Carlos JúniorFaria, Nuno Rodrigues2019-08-14T12:54:38Z2019-08-14T12:54:38Z2019NAVECA, Felipe Gomes et al. Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon. PLoS Neglected Tropical Diseases, v. 13, n. 3, e0007065, p. 1-21, Mar. 2019. DOI: https://doi.org/10.1371/journal.pntd.0007065. Disponível em: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6424459/pdf/pntd.0007065.pdf.1935-2727https://patua.iec.gov.br/handle/iec/383110.1371/journal.pntd.0007065Background: Since its first detection in the Caribbean in late 2013, chikungunya virus (CHIKV) has affected 51 countries in the Americas. The CHIKV epidemic in the Americas was caused by the CHIKV-Asian genotype. In August 2014, local transmission of the CHIKV-Asian genotype was detected in the Brazilian Amazon region. However, a distinct lineage, the CHIKV-East-Central-South-America (ECSA)-genotype, was detected nearly simultaneously in Feira de Santana, Bahia state, northeast Brazil. The genomic diversity and the dynamics of CHIKV in the Brazilian Amazon region remains poorly understood despite its importance to better understand the epidemiological spread and public health impact of CHIKV in the country. Methodology/Principal findings: We report a large CHIKV outbreak (5,928 notified cases between August 2014 and August 2018) in Boa vista municipality, capital city of Roraima’s state, located in the Brazilian Amazon region. We generated 20 novel CHIKV-ECSA genomes from the Brazilian Amazon region using MinION portable genome sequencing. Phylogenetic analyses revealed that despite an early introduction of the Asian genotype in 2015 in Roraima, the large CHIKV outbreak in 2017 in Boa Vista was caused by an ECSA-lineage most likely introduced from northeastern Brazil. Epidemiological analyses suggest a basic reproductive number of R0 of 1.66, which translates in an estimated 39 (95% CI: 36 to 45) % of Roraima’s population infected with CHIKV-ECSA. Finally, we find a strong association between Google search activity and the local laboratory-confirmed CHIKV cases in Roraima. Conclusions/Significance: This study highlights the potential of combining traditional surveillance with portable genome sequencing technologies and digital epidemiology to inform public health surveillance in the Amazon region. Our data reveal a large CHIKV-ECSA outbreak in Boa Vista, limited potential for future CHIKV outbreaks, and indicate a replacement of the Asian genotype by the ECSA genotype in the Amazon region.The ZIBRA-2 project is funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant 440685/2016-8) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (grant 88887.130716/2016-00). FGN is funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (http:// www.cnpq.br, grant 440856/2016–7) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (http://www.capes.gov.br, grants 88881.130825/2016–00 and 88887.130823/2016– 00). L.C.J.A. is supported by the EU’s Horizon 2020 Programme through ZIKAlliance (grant PRES-005- FEX-17-4-2-33). N.R.F. is funded by a Royal Society and Wellcome Trust Sir Henry Dale Fellowship (204311/Z/16/Z), internal GCRF grant 005073, and John Fell Research Fund grant 005166. This research received funding from the ERC (grant agreement 614725-PATHPHYLODYN). MS was partially supported by the National Institute of General Medical Sciences of the NIH (USA) under award number R01GM130668.Fundação Oswaldo Cruz. Instituto Leônidas e Maria Deane. Laboratório de Ecologia de Doenças Transmissíveis na Amazônia. Manaus, AM, Brazil.Universidade de São Paulo. Instituto de Medicina Tropical e Faculdade de Medicina. São Paulo, SP, Brazil.Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Flavivírus. Rio de Janeiro, RJ, Brazil / Universidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Laboratório de Genética Celular e Molecular. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Flavivírus. Rio de Janeiro, RJ, Brazil / Fundação Oswaldo Cruz. Instituto Gonçalo Moniz. Laboratório de Patologia Experimental. Salvador, BA, Brazil.Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Flavivírus. Rio de Janeiro, RJ, Brazil / Fundação Oswaldo Cruz. Instituto Gonçalo Moniz. Laboratório de Patologia Experimental. Salvador, BA, Brazil.Universidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Laboratório de Genética Celular e Molecular. Belo Horizonte, MG, Brazil / Fundação Ezequiel Dias. Instituto Octávio Magalhães. Laboratório Central de Saúde Pública. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Leônidas e Maria Deane. Laboratório de Ecologia de Doenças Transmissíveis na Amazônia. Manaus, AM, Brazil.Fundação Oswaldo Cruz. Instituto Leônidas e Maria Deane. Laboratório de Ecologia de Doenças Transmissíveis na Amazônia. Manaus, AM, Brazil.Universidade Federal do Rio de Janeiro. Instituto de Biologia. Departamento de Genética. Laboratório de Virologia Molecular. Rio de Janeiro, RJ, Brazil.University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom.Harvard Medical School. Department of Pediatrics. Boston, MA, United States of America / Boston Children’s Hospital. Computational Health Informatics Program. Boston, MA, United States of America.University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom / Boston Children’s Hospital. Computational Epidemiology Lab. Boston, MA, United States of America.University of Birmingham. Institute of Microbiology and Infection. Birmingham, United Kingdom.University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom.University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom.Universidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Laboratório de Genética Celular e Molecular. Belo Horizonte, MG, Brazil.Universidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Laboratório de Genética Celular e Molecular. Belo Horizonte, MG, Brazil.Universidade de São Paulo. Instituto de Medicina Tropical e Faculdade de Medicina. São Paulo, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Centro de Tecnologia de Inovação. Ananindeua, PA, Brasil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Centro de Tecnologia de Inovação. Ananindeua, PA, Brasil.University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom.Universidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Laboratório de Genética Celular e Molecular. Belo Horizonte, MG, Brazil.Universidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Laboratório de Genética Celular e Molecular. Belo Horizonte, MG, Brazil.Laboratório Central de Saúde Pública. Boa Vista, RR, Brazil.Laboratório Central de Saúde Pública. Boa Vista, RR, Brazil.Laboratório Central de Saúde Pública. Boa Vista, RR, Brazil.Superintendência de Vigilância em Saúde. Secretaria Municipal de Saúde de Boa Vista. Boa Vista, RR, Brazil.Fundação de Medicina Tropical Doutor Heitor Vieira Dourado. Departamento de Virologia. Manaus, AM, Brazil.Superintendência de Vigilância em Saúde. Secretaria Municipal de Saúde de Boa Vista. Boa Vista, RR, Brazil.Laboratório Central de Saúde Pública do Amazonas. Manaus, AM, Brazil.Organização Pan-Americana da Saúde / Organização Mundial da Saúde. Brasília, DF, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde, Brasília, DF, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde, Brasília, DF, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde, Brasília, DF, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde, Brasília, DF, Brazil.Universidade Federal do Rio de Janeiro. Instituto de Biologia. Departamento de Genética. Laboratório de Virologia Molecular. Rio de Janeiro, RJ, Brazil.Fundação Oswaldo Cruz. Instituto Leônidas e Maria Deane. Laboratório de Ecologia de Doenças Transmissíveis na Amazônia. Manaus, AM, Brazil.University of Birmingham. Institute of Microbiology and Infection. Birmingham, United Kingdom.University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom.Universidade de São Paulo. Instituto de Medicina Tropical e Faculdade de Medicina. São Paulo, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde, Brasília, DF, Brazil.Fundação Oswaldo Cruz. Instituto Oswaldo Cruz. Laboratório de Flavivírus. Rio de Janeiro, RJ, Brazil / Universidade Federal de Minas Gerais. Instituto de Ciências Biológicas. Laboratório de Genética Celular e Molecular. Belo Horizonte, MG, Brazil.University of Oxford. Department of Zoology. 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dc.title.pt_BR.fl_str_mv Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
title Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
spellingShingle Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
Navega, Felipe Gomes
Arbovirus / patogenicidade
Vírus Chikungunya / genética
Variação Genética
Genoma Viral
Monitoramento Epidemiológico
Filogenia
Filogeografia
Boa Vista (RR)
Navega, Felipe Gomes
Arbovirus / patogenicidade
Vírus Chikungunya / genética
Variação Genética
Genoma Viral
Monitoramento Epidemiológico
Filogenia
Filogeografia
Boa Vista (RR)
title_short Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
title_full Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
title_fullStr Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
title_full_unstemmed Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
title_sort Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon
author Navega, Felipe Gomes
author_facet Navega, Felipe Gomes
Navega, Felipe Gomes
Claro, Ingra Morales
Giovanetti, Marta
Jesus, Jaqueline Goes de
Xavier, Joilson
Iani, Felipe Campos de Melo
Nascimento, Valdinete Alves do
Souza, Victor Costa de
Silveira, Paola Paz
Lourenço, José
Santillana, Mauricio
Kraemer, Moritz U. G
Quick, Josh
Hill, Sarah C
Thézé, Julien
Carvalho, Rodrigo Dias de Oliveira
Azevedo, Vasco
Salles, Flavia Cristina da Silva
Nunes, Márcio Roberto Teixeira
Lemos, Poliana da Silva
Candido, Darlan da Silva
Pereira, Glauco de Carvalho
Oliveira, Marluce Aparecida Assunção
Meneses, Cátia Alexandra Ribeiro
Maito, Rodrigo Melo
Cunha, Claudeth Rocha Santa Brígida
Campos, Daniela Palha de Sousa
Castilho, Marcia da Costa
Siqueira, Thalita Caroline da Silva
Terra, Tiza Matos
Albuquerque, Carlos Frederico Campelo de
Cruz, Laura Nogueira da
Abreu, André Luiz de
Martins, Divino Valerio
Simões, Daniele Silva de Moraes Vanlume
Aguiar, Renato Santana de
Luz, Sérgio Luiz Bessa
Loman, Nicholas
Pybus, Oliver G
Sabino, Ester Cerdeira
Okumoto, Osnei
Alcantara, Luiz Carlos Júnior
Faria, Nuno Rodrigues
Claro, Ingra Morales
Giovanetti, Marta
Jesus, Jaqueline Goes de
Xavier, Joilson
Iani, Felipe Campos de Melo
Nascimento, Valdinete Alves do
Souza, Victor Costa de
Silveira, Paola Paz
Lourenço, José
Santillana, Mauricio
Kraemer, Moritz U. G
Quick, Josh
Hill, Sarah C
Thézé, Julien
Carvalho, Rodrigo Dias de Oliveira
Azevedo, Vasco
Salles, Flavia Cristina da Silva
Nunes, Márcio Roberto Teixeira
Lemos, Poliana da Silva
Candido, Darlan da Silva
Pereira, Glauco de Carvalho
Oliveira, Marluce Aparecida Assunção
Meneses, Cátia Alexandra Ribeiro
Maito, Rodrigo Melo
Cunha, Claudeth Rocha Santa Brígida
Campos, Daniela Palha de Sousa
Castilho, Marcia da Costa
Siqueira, Thalita Caroline da Silva
Terra, Tiza Matos
Albuquerque, Carlos Frederico Campelo de
Cruz, Laura Nogueira da
Abreu, André Luiz de
Martins, Divino Valerio
Simões, Daniele Silva de Moraes Vanlume
Aguiar, Renato Santana de
Luz, Sérgio Luiz Bessa
Loman, Nicholas
Pybus, Oliver G
Sabino, Ester Cerdeira
Okumoto, Osnei
Alcantara, Luiz Carlos Júnior
Faria, Nuno Rodrigues
author_role author
author2 Claro, Ingra Morales
Giovanetti, Marta
Jesus, Jaqueline Goes de
Xavier, Joilson
Iani, Felipe Campos de Melo
Nascimento, Valdinete Alves do
Souza, Victor Costa de
Silveira, Paola Paz
Lourenço, José
Santillana, Mauricio
Kraemer, Moritz U. G
Quick, Josh
Hill, Sarah C
Thézé, Julien
Carvalho, Rodrigo Dias de Oliveira
Azevedo, Vasco
Salles, Flavia Cristina da Silva
Nunes, Márcio Roberto Teixeira
Lemos, Poliana da Silva
Candido, Darlan da Silva
Pereira, Glauco de Carvalho
Oliveira, Marluce Aparecida Assunção
Meneses, Cátia Alexandra Ribeiro
Maito, Rodrigo Melo
Cunha, Claudeth Rocha Santa Brígida
Campos, Daniela Palha de Sousa
Castilho, Marcia da Costa
Siqueira, Thalita Caroline da Silva
Terra, Tiza Matos
Albuquerque, Carlos Frederico Campelo de
Cruz, Laura Nogueira da
Abreu, André Luiz de
Martins, Divino Valerio
Simões, Daniele Silva de Moraes Vanlume
Aguiar, Renato Santana de
Luz, Sérgio Luiz Bessa
Loman, Nicholas
Pybus, Oliver G
Sabino, Ester Cerdeira
Okumoto, Osnei
Alcantara, Luiz Carlos Júnior
Faria, Nuno Rodrigues
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dc.contributor.author.fl_str_mv Navega, Felipe Gomes
Claro, Ingra Morales
Giovanetti, Marta
Jesus, Jaqueline Goes de
Xavier, Joilson
Iani, Felipe Campos de Melo
Nascimento, Valdinete Alves do
Souza, Victor Costa de
Silveira, Paola Paz
Lourenço, José
Santillana, Mauricio
Kraemer, Moritz U. G
Quick, Josh
Hill, Sarah C
Thézé, Julien
Carvalho, Rodrigo Dias de Oliveira
Azevedo, Vasco
Salles, Flavia Cristina da Silva
Nunes, Márcio Roberto Teixeira
Lemos, Poliana da Silva
Candido, Darlan da Silva
Pereira, Glauco de Carvalho
Oliveira, Marluce Aparecida Assunção
Meneses, Cátia Alexandra Ribeiro
Maito, Rodrigo Melo
Cunha, Claudeth Rocha Santa Brígida
Campos, Daniela Palha de Sousa
Castilho, Marcia da Costa
Siqueira, Thalita Caroline da Silva
Terra, Tiza Matos
Albuquerque, Carlos Frederico Campelo de
Cruz, Laura Nogueira da
Abreu, André Luiz de
Martins, Divino Valerio
Simões, Daniele Silva de Moraes Vanlume
Aguiar, Renato Santana de
Luz, Sérgio Luiz Bessa
Loman, Nicholas
Pybus, Oliver G
Sabino, Ester Cerdeira
Okumoto, Osnei
Alcantara, Luiz Carlos Júnior
Faria, Nuno Rodrigues
dc.subject.decsPrimary.pt_BR.fl_str_mv Arbovirus / patogenicidade
Vírus Chikungunya / genética
Variação Genética
Genoma Viral
Monitoramento Epidemiológico
Filogenia
Filogeografia
Boa Vista (RR)
topic Arbovirus / patogenicidade
Vírus Chikungunya / genética
Variação Genética
Genoma Viral
Monitoramento Epidemiológico
Filogenia
Filogeografia
Boa Vista (RR)
description Background: Since its first detection in the Caribbean in late 2013, chikungunya virus (CHIKV) has affected 51 countries in the Americas. The CHIKV epidemic in the Americas was caused by the CHIKV-Asian genotype. In August 2014, local transmission of the CHIKV-Asian genotype was detected in the Brazilian Amazon region. However, a distinct lineage, the CHIKV-East-Central-South-America (ECSA)-genotype, was detected nearly simultaneously in Feira de Santana, Bahia state, northeast Brazil. The genomic diversity and the dynamics of CHIKV in the Brazilian Amazon region remains poorly understood despite its importance to better understand the epidemiological spread and public health impact of CHIKV in the country. Methodology/Principal findings: We report a large CHIKV outbreak (5,928 notified cases between August 2014 and August 2018) in Boa vista municipality, capital city of Roraima’s state, located in the Brazilian Amazon region. We generated 20 novel CHIKV-ECSA genomes from the Brazilian Amazon region using MinION portable genome sequencing. Phylogenetic analyses revealed that despite an early introduction of the Asian genotype in 2015 in Roraima, the large CHIKV outbreak in 2017 in Boa Vista was caused by an ECSA-lineage most likely introduced from northeastern Brazil. Epidemiological analyses suggest a basic reproductive number of R0 of 1.66, which translates in an estimated 39 (95% CI: 36 to 45) % of Roraima’s population infected with CHIKV-ECSA. Finally, we find a strong association between Google search activity and the local laboratory-confirmed CHIKV cases in Roraima. Conclusions/Significance: This study highlights the potential of combining traditional surveillance with portable genome sequencing technologies and digital epidemiology to inform public health surveillance in the Amazon region. Our data reveal a large CHIKV-ECSA outbreak in Boa Vista, limited potential for future CHIKV outbreaks, and indicate a replacement of the Asian genotype by the ECSA genotype in the Amazon region.
publishDate 2019
dc.date.accessioned.fl_str_mv 2019-08-14T12:54:38Z
dc.date.available.fl_str_mv 2019-08-14T12:54:38Z
dc.date.issued.fl_str_mv 2019
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.citation.fl_str_mv NAVECA, Felipe Gomes et al. Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon. PLoS Neglected Tropical Diseases, v. 13, n. 3, e0007065, p. 1-21, Mar. 2019. DOI: https://doi.org/10.1371/journal.pntd.0007065. Disponível em: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6424459/pdf/pntd.0007065.pdf.
dc.identifier.uri.fl_str_mv https://patua.iec.gov.br/handle/iec/3831
dc.identifier.issn.-.fl_str_mv 1935-2727
dc.identifier.doi.pt_BR.fl_str_mv 10.1371/journal.pntd.0007065
identifier_str_mv NAVECA, Felipe Gomes et al. Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon. PLoS Neglected Tropical Diseases, v. 13, n. 3, e0007065, p. 1-21, Mar. 2019. DOI: https://doi.org/10.1371/journal.pntd.0007065. Disponível em: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6424459/pdf/pntd.0007065.pdf.
1935-2727
10.1371/journal.pntd.0007065
url https://patua.iec.gov.br/handle/iec/3831
dc.language.iso.fl_str_mv eng
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dc.publisher.none.fl_str_mv Public Library of Science
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