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

Abstract

48 49 50 51 52 Corresponding authors: luiz.alcantara@ioc.fiocruz.br and nuno.faria@zoo.ox.ac.uk 3 53 Abstract 54 Background 55 Since its first detection in the Caribbean in late 2013, chikungunya virus (CHIKV) has 56 affected 51 countries in the Americas. The CHIKV epidemic in the Americas was 57 caused by the CHIKV-Asian genotype. In August 2014, local transmission of the 58 CHIKV-Asian genotype was detected in the Brazilian Amazon region. However, a 59 distinct lineage, the CHIKV-East-Central-South-America (ECSA)-genotype, was 60 detected nearly simultaneously in Feira de Santana, Bahia state, northeast Brazil. The 61 genomic diversity and the dynamics of CHIKV in the Brazilian Amazon region 62 remains poorly understood despite its importance to better understand the 63 epidemiological spread and public health impact of CHIKV in the country. 64 65 Methodology/Principal Findings 66 We report a large CHIKV outbreak (5,928 notified cases between August 2014 and 67 August 2018) in Boa vista municipality, capital city of Roraima's state, located in the 68 Brazilian Amazon region. In just 48 hours, we generated 20 novel CHIKV-ECSA 69 genomes from the Brazilian Amazon region using MinION portable genome 70 sequencing. Phylogenetic analyses revealed that despite an early introduction of the 71 Asian genotype in 2015 in Roraima, the large CHIKV outbreak in 2017 in Boa Vista 72 was caused by an ECSA-lineage most likely introduced from northeastern Brazil. 73 Epidemiological analyses suggest a basic reproductive number of R 0 of 1.66, which 74 translates in an estimated 39 (95% CI: 36 to 45) % of Roraima's population infected 75 with CHIKV-ECSA. Finally, we find a strong association between Google search 76 activity and the local laboratory-confirmed CHIKV cases in Roraima. 77 78 Conclusions/Significance 79 This study highlights the potential of combining traditional surveillance with portable 80 genome sequencing technologies and digital epidemiology to inform public health 81 surveillance in the Amazon region. Our data reveal a large CHIKV-ECSA outbreak in 82 Boa Vista, limited potential for future CHIKV outbreaks, and indicate a replacement 83 of the Asian genotype by the ECSA genotype in the Amazon region. 84 85 4 86 Author Summary 87 Until the end of 2017, Brazil notified the highest number of infections caused by 88 chikungunya virus (CHIKV) in the Americas. We investigated a large CHIKV 89 outbreak in Boa vista municipality in the Brazilian Amazon region. Rapid portable 90 genome sequencing of 20 novel isolates and subsequent genetic analysis revealed that 91 ECSA lineage was introduced from northeastern Brazil to Roraima around July 2016. 92 Epidemiological analyses suggest a basic reproductive number of R 0 of 1.66, which 93 suggests that approximately 39% of Roraima's population was infected with CHIKV-94 ECSA. Given the dominance of the CHIKV-Asian genotype in the Americas, our data 95 highlights the rapid spread of a less understood and poorly characterized CHIKV-96 ECSA genotype in Brazil. Investigations on p...

Genomic and Epidemiological Surveillance of Zika Virus in the Amazon Region

“…Although evidence of cross-border transmissions among locations that share a tropical climate is frequent and has been observed previously in the region, for example, for DENV serotype 4 (Nunes, 2012) and CHIKV (Naveca et al, 2019), and although our results show that one isolate from Venezuela, a country with a high suitability for Ae. aegypti that has direct river connections to Manaus, clusters within the Manaus clade (Figure 5), we cannot exclude that some of the ZIKV introductions to Manaus were from Venezuela, therefore we cannot make speculations about the direction of the transmissions between the two countries, because of the lack of epidemiological data linked to this sample as well as a larger samples number from Venezuela.…”

Increased interregional virus exchange and nucleotide diversity outline the expansion of the chikungunya virus ECSA lineage in Brazil

“…In this study, we increased the number of CHIKV genomes deposited in the NCBI by generating 422 genomes that cover 12 Brazilian states over the years 2021-2022. By combining genomic and demographic data this effort has provided a comprehensive overview of CHIKV ECSA phylogeny in Brazil which summarizes and updates previous phylogenies from other studies of localized outbreaks 10,12,14,26,27 . The updated and metadataenriched dataset allowed us not only to describe the genetic diversity of circulating CHIKV variants but also to describe branching patterns observed in the updated phylogeny and infer the divergence time and likely location of emerging distinct subclades from the Brazilian lineage.…”

“…Several genomic surveillance initiatives have been carried out in the last few years to build knowledge regarding the genetic diversity and transmission dynamics of arboviruses in Brazil [5][6][7][8][9][10][11] . Genomic sequencing has revealed that the first case of chikungunya fever (CHIKF) reported in Brazil was an infection by the Asian lineage introduced in a northern state in 2014, while another case reported seven days later in a north-eastern state represented the first known introduction of the East-Central-South-African (ECSA) lineage in the country 12 .…”

“…Following the arrival of ECSA lineage in the Northeast region, a number of other studies have predicted and reported the establishment and spread of this lineage to the rest of the country [10][11][12]14,17,[26][27][28][29] . The Bayesian phylogeographic approach employed in this study has revealed the main routes of dispersion of CHIKV in the country.…”

Spatial-temporal dynamics and recurrence of chikungunya virus in Brazil

“…albopictus are widely distributed (15), autochthonous CHIKF cases caused by the Asian and ECSA genotypes were first detected in December 2013 and September 2014, respectively (16). Subsequent genomic investigations indicated the predominance of the ECSA genotype across Brazil's five geographic regions (17)(18)(19)(20)(21). Currently, Brazil has the highest number of CHIKF cases in the Americas (22).…”