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

• Author(s): Navega, Felipe Gomes ; Claro, Ingra ; Giovanetti, Marta ; Jesus, Jaqueline Goes de ; Xavier, Joilson ; Iani, Felipe Campos de Melo ; Nascimento, Valdinete Alves do ; Souza, Victor Costa de ; Silveira, Paola Paz ; Louren?o, Jos? ; Santillana, Mauricio ; Kraemer, Moritz U. G ; Quick, Josh ; Hill, Sarah C ; Th?z?, Julien ; Carvalho, Rodrigo Dias de Oliveira ; Azevedo, Vasco ; Salles, Flavia Cristina da Silva ; Nunes, M?rcio Roberto Teixeira ; Lemos, Poliana da Silva ; Candido, Darlan da Silva ; Pereira, Glauco de Carvalho ; Oliveira, Marluce Aparecida Assun??o ; Meneses, C?tia Alexandra Ribeiro ; Maito, Rodrigo Melo ; Cunha, Claudeth Rocha Santa Br?gida ; Campos, Daniela Palha de Sousa ; Castilho, Marcia da Costa ; Siqueira, Thalita Caroline da Silva ; Terra, Tiza Matos ; Albuquerque, Carlos F. Campelo de ; Cruz, Laura Nogueira da ; Abreu, Andr? Luis de ; Martins, Divino Valerio ; Sim?es, Daniele Silva de Moraes Vanlume ; Aguiar, Renato Santana de ; Luz, S?rgio Luiz Bessa ; Loman, Nicholas ; Pybus, Oliver G ; Sabino, Ester C ; Okumoto, Osnei ; Alc?ntara, Luiz Carlos Junior ; Faria, Nuno Rodrigues
• Date: 2019
• Origin: Oasisbr
• Subject(s): Arbovirus / patogenicidade; V?rus Chikungunya / gen?tica; Varia??o Gen?tica; Genoma Viral; Monitoramento Epidemiol?gico; Filogenia; Filogeografia; Boa Vista (RR)
• Document Type: Journal article
• Language: English

Description

The ZIBRA-2 project is funded by Conselho Nacional de Desenvolvimento Cient?fico e Tecnol?gico (grant 440685/2016-8) and Coordena??o de Aperfei?oamento de Pessoal de N?vel Superior (grant 88887.130716/2016-00). FGN is funded by Conselho Nacional de Desenvolvimento Cient?fico e Tecnol?gico (http:// www.cnpq.br, grant 440856/2016?7) and Coordena??o de Aperfei?oamento de Pessoal de N?vel 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.

Funda??o Oswaldo Cruz. Instituto Le?nidas e Maria Deane. Laborat?rio de Ecologia de Doen?as Transmiss?veis na Amaz?nia. Manaus, AM, Brazil.

Universidade de S?o Paulo. Instituto de Medicina Tropical e Faculdade de Medicina. S?o Paulo, SP, Brazil.

Funda??o Oswaldo Cruz. Instituto Oswaldo Cruz. Laborat?rio de Flaviv?rus. Rio de Janeiro, RJ, Brazil / Universidade Federal de Minas Gerais. Instituto de Ci?ncias Biol?gicas. Laborat?rio de Gen?tica Celular e Molecular. Belo Horizonte, MG, Brazil.

Funda??o Oswaldo Cruz. Instituto Oswaldo Cruz. Laborat?rio de Flaviv?rus. Rio de Janeiro, RJ, Brazil / Funda??o Oswaldo Cruz. Instituto Gon?alo Moniz. Laborat?rio de Patologia Experimental. Salvador, BA, Brazil.

Funda??o Oswaldo Cruz. Instituto Oswaldo Cruz. Laborat?rio de Flaviv?rus. Rio de Janeiro, RJ, Brazil / Funda??o Oswaldo Cruz. Instituto Gon?alo Moniz. Laborat?rio de Patologia Experimental. Salvador, BA, Brazil.

Universidade Federal de Minas Gerais. Instituto de Ci?ncias Biol?gicas. Laborat?rio de Gen?tica Celular e Molecular. Belo Horizonte, MG, Brazil / Funda??o Ezequiel Dias. Instituto Oct?vio Magalh?es. Laborat?rio Central de Sa?de P?blica. Belo Horizonte, MG, Brazil.

Funda??o Oswaldo Cruz. Instituto Le?nidas e Maria Deane. Laborat?rio de Ecologia de Doen?as Transmiss?veis na Amaz?nia. Manaus, AM, Brazil.

Funda??o Oswaldo Cruz. Instituto Le?nidas e Maria Deane. Laborat?rio de Ecologia de Doen?as Transmiss?veis na Amaz?nia. Manaus, AM, Brazil.

Universidade Federal do Rio de Janeiro. Instituto de Biologia. Departamento de Gen?tica. Laborat?rio 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 Ci?ncias Biol?gicas. Laborat?rio de Gen?tica Celular e Molecular. Belo Horizonte, MG, Brazil.

Universidade Federal de Minas Gerais. Instituto de Ci?ncias Biol?gicas. Laborat?rio de Gen?tica Celular e Molecular. Belo Horizonte, MG, Brazil.

Universidade de S?o Paulo. Instituto de Medicina Tropical e Faculdade de Medicina. S?o Paulo, SP, Brazil.

Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de. Instituto Evandro Chagas. Centro de Tecnologia de Inova??o. Ananindeua, PA, Brasil.

Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de. Instituto Evandro Chagas. Centro de Tecnologia de Inova??o. Ananindeua, PA, Brasil.

University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom.

Universidade Federal de Minas Gerais. Instituto de Ci?ncias Biol?gicas. Laborat?rio de Gen?tica Celular e Molecular. Belo Horizonte, MG, Brazil.

Universidade Federal de Minas Gerais. Instituto de Ci?ncias Biol?gicas. Laborat?rio de Gen?tica Celular e Molecular. Belo Horizonte, MG, Brazil.

Laborat?rio Central de Sa?de P?blica. Boa Vista, RR, Brazil.

Laborat?rio Central de Sa?de P?blica. Boa Vista, RR, Brazil.

Laborat?rio Central de Sa?de P?blica. Boa Vista, RR, Brazil.

Superintend?ncia de Vigil?ncia em Sa?de. Secretaria Municipal de Sa?de de Boa Vista. Boa Vista, RR, Brazil.

Funda??o de Medicina Tropical Doutor Heitor Vieira Dourado. Departamento de Virologia. Manaus, AM, Brazil.

Superintend?ncia de Vigil?ncia em Sa?de. Secretaria Municipal de Sa?de de Boa Vista. Boa Vista, RR, Brazil.

Laborat?rio Central de Sa?de P?blica do Amazonas. Manaus, AM, Brazil.

Organiza??o Pan?Americana da Sa?de / Organiza??o Mundial da Sa?de. Bras?lia, DF, Brazil.

Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de, Bras?lia, DF, Brazil.

Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de, Bras?lia, DF, Brazil.

Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de, Bras?lia, DF, Brazil.

Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de, Bras?lia, DF, Brazil.

Universidade Federal do Rio de Janeiro. Instituto de Biologia. Departamento de Gen?tica. Laborat?rio de Virologia Molecular. Rio de Janeiro, RJ, Brazil.

Funda??o Oswaldo Cruz. Instituto Le?nidas e Maria Deane. Laborat?rio de Ecologia de Doen?as Transmiss?veis na Amaz?nia. 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 S?o Paulo. Instituto de Medicina Tropical e Faculdade de Medicina. S?o Paulo, SP, Brazil.

Minist?rio da Sa?de. Secretaria de Vigil?ncia em Sa?de, Bras?lia, DF, Brazil.

Funda??o Oswaldo Cruz. Instituto Oswaldo Cruz. Laborat?rio de Flaviv?rus. Rio de Janeiro, RJ, Brazil / Universidade Federal de Minas Gerais. Instituto de Ci?ncias Biol?gicas. Laborat?rio de Gen?tica Celular e Molecular. Belo Horizonte, MG, Brazil.

University of Oxford. Department of Zoology. South Parks Road, Oxford, United Kingdom.

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.