Characterizing the Aedes aegypti population in a Vietnamese village in preparation for a Wolbachia-based mosquito control strategy to eliminate dengue

Abstract

Background: A life-shortening strain of the obligate intracellular bacteria Wolbachia, called wMelPop, is seen as a promising new tool for the control of Aedes aegypti. However, developing a vector control strategy based on the release of mosquitoes transinfected with wMelPop requires detailed knowledge of the demographics of the target population.

Methodology/principal findings: In Tri Nguyen village (611 households) on Hon Mieu Island in central Vietnam, we conducted nine quantitative entomologic surveys over 14 months to determine if Ae. aegypti populations were spatially and temporally homogenous, and to estimate population size. There was no obvious relationship between mosquito (larval, pupal or adult) abundance and temperature and rainfall, and no area of the village supported consistently high numbers of mosquitoes. In almost all surveys, key premises produced high numbers of Ae. aegypti. However, these premises were not consistent between surveys. For an intervention based on a single release of wMelPop-infected Ae. aegypti, release ratios of infected to uninfected adult mosquitoes of all age classes are estimated to be 1.8-6.7ratio1 for gravid females (and similarly aged males) or teneral adults, respectively. We calculated that adult female mosquito abundance in Tri Nguyen village could range from 1.1 to 43.3 individuals of all age classes per house. Thus, an intervention could require the release of 2-78 wMelPop-infected gravid females and similarly aged males per house, or 7-290 infected teneral female and male mosquitoes per house.

Conclusions/significance: Given the variability we encountered, this study highlights the importance of multiple entomologic surveys when evaluating the spatial structure of a vector population or estimating population size. If a single release of wMelPop-infected Ae. aegypti were to occur when wild Ae. aegypti abundance was at its maximum, a preintervention control program would be necessary to ensure that there was no net increase in mosquito numbers. However, because of the short-term temporal heterogeneity, the inconsistent spatial structure and the impact of transient key premises that we observed, the feasibility of multiple releases of smaller numbers of mosquitoes also needs to be considered. In either case, fewer wMelPop-infected mosquitoes would then need to be released, which will likely be more acceptable to householders.

Figure 1. Map showing the location of the study site.

A) Khanh Hoa province, central Vietnam. B) Nha Trang city, Khanh Hoa province. Hon Mieu island is marked with an arrow. C) Hon Mieu island, and the 611 houses that make up Tri Nguyen village.

Figure 2. Temporal abundance of Aedes aegypti in Tri Nguyen village during different seasons.

A) Mean monthly minimum and maximum temperatures (°C), and total monthly rainfall (mm), recorded during the survey period from Nha Trang weather station. B–D). Box plots of the number of Ae. aegypti III/IV instars and pupae per house, and female Ae. aegypti per BG-trap, for each of the surveys in Tri Nguyen village. Central line = median, dotted line = mean, box = 25^th/75^th percentiles, whiskers = 10^th/90^th percentiles, dots = 5^th/95^th percentiles. Boxed text shows the different seasons in central Vietnam based on 5 year historical weather data.

Figure 3. The percent contribution of the top 10, 5, 3, and highest households (HH) for each survey to the production of Ae. aegypti.

A) III/IV instars, B) pupae and C) adult females.

Figure 4. Spatial clusters of Ae. aegypti III/IV instar and pupae positive and negative houses in Tri Nguyen village.

Horizontally hashed circles or shaded circles represent clusters of III/IV instar positive houses or pupae positive houses (P<0.01), respectively, after taking into consideration the structure of the houses sampled (black dots) (P<0.01). Clear circles represent statistically significant clusters of houses negative for III/IV instars. There was no significant spatial structure amongst houses negative for pupae, or amongst houses positive or negative for Ae. aegypti females (collected with BG-traps).

Figure 5. Spatial abundance of Ae. aegypti pupae and adult females in Tri Nguyen village.

Shaded circles or diagonally-hashed circles represent statistically significant clusters of houses with high numbers of pupae (P<0.01), or adult females per BG-trap (P<0.01), respectively, after taking into consideration the structure of the houses sampled (black dots) (P<0.01). Letters refer to clusters whose statistics are outlined in Table 3. There was no significant spatial structure in the abundance of Ae. aegypti III/IV instars.

Figure 6. Ninety-five percent confidence limits for estimated numbers of adult female Ae. aegypti in Tri Nguyen village (Nov 2006 – Dec 2007).

Confidence limits based on extrapolating pupal survey data from 100 households to 611 households 999 times, and assuming a pupal daily development rate (PDD) of 0.30 or 0.49, a pupal survival rate of 0.83, a female∶male sex ratio of 1∶1, and a probability of daily survival (PDS) for adults of 0.8 or 0.9.