Quantifying the mosquito's sweet tooth: modelling the effectiveness of attractive toxic sugar baits (ATSB) for malaria vector control

Abstract

Background: Current vector control strategies focus largely on indoor measures, such as long-lasting insecticide treated nets (LLINs) and indoor residual spraying (IRS); however mosquitoes frequently feed on sugar sources outdoors, inviting the possibility of novel control strategies. Attractive toxic sugar baits (ATSB), either sprayed on vegetation or provided in outdoor bait stations, have been shown to significantly reduce mosquito densities in these settings.

Methods: Simple models of mosquito sugar-feeding behaviour were fitted to data from an ATSB field trial in Mali and used to estimate sugar-feeding rates and the potential of ATSB to control mosquito populations. The model and fitted parameters were then incorporated into a larger integrated vector management (IVM) model to assess the potential contribution of ATSB to future IVM programmes.

Results: In the Mali experimental setting, the model suggests that about half of female mosquitoes fed on ATSB solution per day, dying within several hours of ingesting the toxin. Using a model incorporating the number of gonotrophic cycles completed by female mosquitoes, a higher sugar-feeding rate was estimated for younger mosquitoes than for older mosquitoes. Extending this model to incorporate other vector control interventions suggests that an IVM programme based on both ATSB and LLINs may substantially reduce mosquito density and survival rates in this setting, thereby substantially reducing parasite transmission. This is predicted to exceed the impact of LLINs in combination with IRS provided ATSB feeding rates are 50% or more of Mali experimental levels. In addition, ATSB is predicted to be particularly effective against Anopheles arabiensis, which is relatively exophilic and therefore less affected by IRS and LLINs.

Conclusions: These results suggest that high coverage with a combination of LLINs and ATSB could result in substantial reductions in malaria transmission in this setting. Further field studies of ATSB in other settings are needed to assess the potential of ATSB as a component in future IVM malaria control strategies.

Figure 1

Schematic of the basic ATSB sugar-feeding model in the experimental setting. Female and male mosquitoes emerge at rate b into the unmarked class, U, and become marked, M, when feeding on ATSB-sprayed vegetation at rate s. In the control setting, marked and unmarked mosquitoes die at the same rate, μ, while in the experimental setting, marked mosquitoes die at a faster rate due to the effects of the toxin, μ_ATSB.

Figure 2

Basic model fits for both male and female mosquito catch data in the experimental and control settings. Dots represent mosquito catches, solid lines represent model predictions and shaded regions represent 95% of the model predicted variation in mosquito catch numbers.

Figure 3

Proportions of female mosquitoes having completed zero to two or more than two gonotrophic cycles in the experimental setting. Dots represent observed results, solid lines represent model predictions and shaded regions represent 95% of the model-predicted variation in mosquito catch numbers. Although mosquito numbers in all categories decline after the addition of ATSB, females having completed zero to two gonotrophic cycles decline fastest initially because they have the highest sugar-feeding rate; however, the age distribution quickly shifts towards younger mosquitoes.

Figure 4

Sugar-feeding and integrated vector management. A) Life cycle of the female mosquito depicting the centrality of sugar-feeding and opportunities for vector control in red. B) Data on the pattern of activity of female An. gambiae mosquitoes. Mosquito catches on flowers peaked at 9 pm and 5 am, while catches on socks peaked around 1 am.

Figure 5

Time-series depicting the effects of vector control strategies on vector density in isolation. Solid lines represent total female mosquito density, dashed lines represent females having completed three or more gonotrophic cycles. Coverage levels are assumed to be 80% for all interventions (i.e. 80% of people sleeping under nets, 80% of houses sprayed with insecticide, and 80% of breeding sites treated with BTI). ATSB is assumed to be implemented at analogous levels to that in the Mali experimental setting, and at levels such that the exposure rate would be half that of the Mali experimental setting.

Figure 6

Expected impact of IVM strategies on mosquito density.

Figure 7

Expected impact of IVM strategies on EIR. Model predictions are shown for three transmission settings with pre-intervention EIRs of 100 (very high transmission), 50 (high transmission) and 10 (moderate transmission).

Figure 8

ATSB coverage required to achieve the same reduction in transmission as IRS (given an LLIN coverage of 80%).