Estimating the effect of the wMel release programme on the incidence of dengue and chikungunya in Rio de Janeiro, Brazil: a spatiotemporal modelling study

Abstract

Background: Introgression of genetic material from species of the insect bacteria Wolbachia into populations of Aedes aegypti mosquitoes has been shown in randomised and non-randomised trials to reduce the incidence of dengue; however, evidence for the real-world effectiveness of large-scale deployments of Wolbachia-infected mosquitoes for arboviral disease control in endemic settings is still scarce. A large Wolbachia (wMel strain) release programme was implemented in 2017 in Rio de Janeiro, Brazil. We aimed to assess the effect of this programme on the incidence of dengue and chikungunya in the city.

Methods: 67 million wMel-infected mosquitoes were released across 28 489 locations over an area of 86·8 km² in Rio de Janeiro between Aug 29, 2017 and Dec 27, 2019. Following releases, mosquitoes were trapped and the presence of wMel was recorded. In this spatiotemporal modelling study, we assessed the effect of the release programme on the incidence of dengue and chikungunya. We used spatiotemporally explicit mathematical models applied to geocoded dengue cases (N=283 270) from 2010 to 2019 and chikungunya cases (N=57 705) from 2016 to 2019.

Findings: On average, 32% of mosquitoes collected from the release zones between 1 month and 29 months after the initial release tested positive for wMel. Reduced wMel introgression occurred in locations and seasonal periods in which cases of dengue and chikungunya were historically high, with a decrease to 25% of mosquitoes testing positive for wMel during months in which disease incidence was at its highest. Despite incomplete introgression, we found that the releases were associated with a 38% (95% CI 32-44) reduction in the incidence of dengue and a 10% (4-16) reduction in the incidence of chikungunya.

Interpretation: Stable establishment of wMel in the geographically diverse, urban setting of Rio de Janeiro seems to be more complicated than has been observed elsewhere. However, even intermediate levels of wMel seem to reduce the incidence of disease caused by two arboviruses. These findings will help to guide future release programmes.

Funding: Bill & Melinda Gates Foundation and the European Research Council.

Figure 1

Details of the wMel release programme and the incidence of dengue and chikungunya in Rio de Janeiro, Brazil (A) Map of Rio de Janeiro with a detailed view of the project area, showing the different project subareas. The top-left inset shows the location of Rio de Janeiro within Brazil. (B) Proportion of wMel-infected Aedes aegypti mosquitoes found in traps in each spatiotemporal cell. (C) Number of mosquitoes released and the level of introgression. The black line shows the total number of mosquitoes released per month. The red line shows the proportion of A aegypti captured in traps that were infected by wMel (mean and 95% CI). (D) Number of cases of dengue and chikungunya reported in Rio de Janeiro between 2014 and 2020, including both the project area and the rest of the city. The inset shows the number of cases of these diseases recorded between Jan 1, 2010, and Sept 25, 2019, for dengue and between Jan 1, 2016, and Sept 25, 2019, for chikungunya.

Figure 2

Seasonal pattern of dengue and chikungunya cases and mosquito levels (A) Monthly distribution of dengue cases (2010–19) and chikungunya cases (2016–19). (B) Monthly distribution of Aedes aegypti and Aedes albopictus mosquitoes found in traps (average values from 2017–19). Data are mean and 95% CI. (C) Proportion of trapped female A aegypti mosquitoes that were infected with wMel by month across the project area (average values from 2017–19). Data are mean and 95% CI.

Figure 3

Introgression success as a function of historical and future dengue and chikungunya case incidence The average monthly introgression of wMel within a 500 m × 500 m cell and the standardised incidences of dengue (A) and chikungunya (B) in that location and month. Each line represents the incidence from a different year. Dashed lines are years before the start of the release programme (2010–17 for dengue 2016–17 for chikungunya). Solid lines represent the years 2018 and 2019, which are after the release programme started. We standardised the incidence of dengue and chikungunya by dividing by the overall mean incidence in that year; this method enables us to compare years with large disease outbreaks with years with smaller disease outbreaks on the same plot.

Figure 4

Results of spatiotemporal models (A) Estimated overall relative incidence of dengue and chikungunya in space–time units in which wMel was recorded compared with those in which wMel was not recorded. (B) Relative incidence of dengue and chikungunya in space–time units as a function of the proportion of Aedes aegypti mosquitoes that were infected with wMel. Space–time units within the study area in which no wMel was detected are the reference. Error bars show 95% CI.