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

Felipe Gomes Naveca, Ingra Claro, Marta Giovanetti, Jaqueline Goes de Jesus, Joilson Xavier, Felipe Campos de Melo Iani, Valdinete Alves do Nascimento, Victor Costa de Souza, Paola Paz Silveira, José Lourenço, Mauricio Santillana, Moritz U.G. Kraemer, Josh Quick, Sarah C. Hill, Julien Thézé, Rodrigo Dias de Oliveira Carvalho, Vasco Azevedo, Flavia Cristina da Silva Salles, Márcio Roberto Teixeira Nunes, Poliana da Silva LemosDarlan da Silva Candido, Glauco de Carvalho Pereira, Marluce Aparecida Assunção Oliveira, Cátia Alexandra Ribeiro Meneses, Rodrigo Melo Maito, Claudeth Rocha Santa Brígida Cunha, Daniela Palha de Sousa Campos, Marcia da Costa Castilho, Thalita Caroline da Silva Siqueira, Tiza Matos Terra, Carlos F.Campelo de Albuquerque, Laura Nogueira da Cruz, André Luis de Abreu, Divino Valerio Martins, Daniele Silva de Moraes Vanlume Simoes, Renato Santana de Aguiar, Sérgio Luiz Bessa Luz, Nicholas Loman, Oliver G. Pybus, Ester C. Sabino, Osnei Okumoto, Luiz Carlos Junior Alcantara*, Nuno Rodrigues Faria

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

31 Citations (Scopus)

Abstract

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.

Original languageEnglish
Article numbere0007065
JournalPLoS Neglected Tropical Diseases
Volume13
Issue number3
DOIs
Publication statusPublished - Mar 2018
Externally publishedYes

Bibliographical note

Funding Information:
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. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We are thankful to all personnel from Secretaria de Vigilância em Saúde SVS/MS, PAHO/Brazil, Roraima and Boa Vista Health Surveillance System that coordinated surveillance and helped with data collection and assembly. We thank Oxford Nanopore Technologies for the support to the ZIBRA-2 (Zika in Brazil Real time Analyses-second round) project with additional flowcells and corresponding reagents, and also thank QIAGEN for donation of consumables.

Publisher Copyright:
© 2019 Naveca et al.

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