The High Capacity of Brazilian Aedes aegypti Populations to Transmit a Locally Circulating Lineage of Chikungunya Virus

Abstract

The incidence of chikungunya has dramatically surged worldwide in recent decades, imposing an expanding burden on public health. In recent years, South America, particularly Brazil, has experienced outbreaks that have ravaged populations following the rapid dissemination of the chikungunya virus (CHIKV), which was first detected in 2014. The primary vector for CHIKV transmission is the urban mosquito species Aedes aegypti, which is highly prevalent throughout Brazil. However, the impact of the locally circulating CHIKV genotypes and specific combinations of local mosquito populations on vector competence remains unexplored. Here, we experimentally analyzed and compared the infectivity and transmissibility of the CHIKV-ECSA lineage recently isolated in Brazil among four Ae. aegypti populations collected from different regions of the country. When exposed to CHIKV-infected AG129 mice for blood feeding, all the mosquito populations displayed high infection rates and dissemination efficiency. Furthermore, we observed that all the populations were highly efficient in transmitting CHIKV to a vertebrate host (naïve AG129 mice) as early as eight days post-infection. These results demonstrate the high capacity of Brazilian Ae. aegypti populations to transmit the locally circulating CHIKV-ECSA lineage. This observation could help to explain the high prevalence of the CHIKV-ECSA lineage over the Asian lineage, which was also detected in Brazil in 2014. However, further studies comparing both lineages are necessary to gain a better understanding of the vector's importance in the epidemiology of CHIKV in the Americas.

Keywords: Aedes aegypti; arbovirus; chikungunya virus; vector competence.

Figure 1

Map of Brazil showing the Aedes aegypti sampling sites.

Figure 2

High infection rates of CHIKV across Brazilian Aedes aegypti populations. (A) Scheme of the experimental design used. Infection rates at 4 (B) and 8 (D) days post-feeding (d.p.f.) are shown. The population origin is indicated below each bar plot (ARA, JAB, PET, POA). The number of mosquitoes tested is indicated below the population abbreviation. The CHIKV RNA levels of each mosquito tested are shown. Significant differences are indicated by the p-value (Kruskal–Wallis test). (C,E) The number of mosquitoes with detected CHIKV RNA out of the total number of mosquitoes tested is presented below the population abbreviation. To quantify the CHIKV load, we utilized the 2^−ΔCt (delta Ct) method. The limit of detection was 10¹⁰. The mosquitoes used to obtain the results in both the midgut and the carcass were the same individuals from the cohort. Empty circles represent samples where viral RNA was not detected.

Figure 3

High dissemination efficiency of CHIKV across Brazilian Aedes aegypti populations. An ECSA strain of CHIKV isolated from a human patient in Niterói, Brazil, in 2018 was used. Dissemination efficiencies at 4 (A) and 8 (C) days post-feeding (d.p.f.) are shown. The population origin is indicated below each bar plot (ARA, JAB, PET, POA). The number of mosquitoes tested is indicated below the population abbreviation. The CHIKV RNA levels of each mosquito tested at 4 (B) and 8 (D) days post-feeding (d.p.f.) are shown. Significant differences are indicated by the p-value (Kruskal–Wallis test). The number of mosquitoes with detected CHIKV RNA out of the total number of mosquitoes tested is presented below the population abbreviation. Empty circles represent samples where viral RNA was not detected.

Figure 4

Brazilian Aedes aegypti populations are highly efficient in transmitting CHIKV. (A) Scheme of the experimental design used to assess the CHIKV transmission efficiency in Aedes aegypti. (B) Transmission efficiency at 8 days post-feeding (d.p.f.). The population origin is indicated below each bar plot (ARA, JAB, PET, POA). The number of mosquitoes tested is indicated below the population abbreviation.