Chikungunya virus outbreak in the Amazon region: replacement of the Asian genotype by an ECSA lineage?

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. In just 48 hours, 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 R 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. Author Summary Until the end of 2017, Brazil notified the highest number of infections caused by chikungunya virus (CHIKV) in the Americas. We investigated a large CHIKV outbreak in Boa vista municipality in the Brazilian Amazon region. Rapid portable genome sequencing of 20 novel isolates and subsequent genetic analysis revealed that ECSA lineage was introduced from northeastern Brazil to Roraima around July 2016. Epidemiological analyses suggest a basic reproductive number of R of 1.66, which suggests that approximately 39% of Roraima’s population was infected with CHIKV-ECSA. Given the dominance of the CHIKV-Asian genotype in the Americas, our data highlights the rapid spread of a less understood and poorly characterized CHIKV-ECSA genotype in Brazil. Investigations on potential associations between public health impact of CHIKV and genetic diversity of circulating strains are warranted to better evaluate its impact in Brazil and beyond.