Ivermectin-treated cattle reduces blood digestion, egg production and survival of a free-living population of Anopheles arabiensis under semi-field condition in south-eastern Tanzania

Abstract

Background: Anopheles arabiensis feed on cattle and contributes to residual transmission of malaria in areas with high coverage of long-lasting insecticide-treated nets and indoor residual spraying in East Africa. This study aimed to evaluate the effects of ivermectin-treated cattle as a complementary vector control tool against population of An. arabiensis under the semi-field conditions in south-eastern Tanzania.

Methods: The free-living population of An. arabiensis was allowed to forage on untreated or ivermectin-treated cattle in alternating nights within the semi-field system in south-eastern Tanzania. Fresh blood fed mosquitoes were collected in the morning using mouth aspirators and assessed for their blood meal digestion, egg production, and survivorship. The residual activity of ivermectin-treated cattle was also determined by exposing mosquitoes to the same treatments after every 2 days until day 21 post-treatments. These experiments were replicated 3 times using different individual cattle.

Results: Overall, the ivermectin-treated cattle reduced blood meal digestion in the stomach of An. arabiensis, and their subsequent egg production and survival over time. The ivermectin-treated cattle halved blood meal digestion in mosquitoes, but reduced their egg production for up to 15 days. The ivermectin-treated cattle reduced the survival, and median survival times (1-3 days) of An. arabiensis than control cattle. The daily mortality rates of mosquitoes fed on ivermectin-treated cattle increased by five-fold relative to controls in the first week, and it gradually declined up to 21 days after treatment.

Conclusion: This study demonstrates that long-lasting effects of ivermectin-treated cattle on egg production and survival of An. arabiensis may sustainably suppress their vector density, and reduce residual transmission of malaria. This study suggests that ivermectin-treated non-lactating cattle (i.e. calves, heifers and bulls) could be suitable option for large-scale malaria vector control without limiting consumption of milk and meat by communities in rural settings. Furthermore, simulation models are underway to predict the impact of ivermectin-treated cattle alone, or in combination with LLIN/IRS, the frequency of treatment, and their coverage required to significantly suppress population of An. arabiensis and reduce residual transmission of malaria.

Keywords: Anopheles arabiensis; Blood-digestion; Cattle; Egg-production; Exophagy; Haematin; Ivermectin; Residual-transmission; Survival; Vector–control; Zoophagy.

Fig. 1

Picture of a semi-field system showing: a the outside view of the chamber where free living population of Anopheles arabiensis was established, b the inside of the experimental chamber with established vegetations, breeding and resting habitats for mosquitoes, and c the shelter with cattle as the source of blood meal for An. arabiensis

Fig. 2

Estimated mass of haematin defecated (±1 s.e) by An. arabiensis population after feeding on control and ivermectin-treated cattle across time. The relationship between the effects of ivermectin treated cattle and post-treatments time on mass of haematin defecated by mosquitoes at the end of blood meal digestion

Fig. 3

Estimated proportion (±1 s.e) of An. arabiensis laid eggs after blood feeding on control and untreated cattle: a the effects of ivermectin-treated cattle on proportion of mosquitoes laid eggs, and b the relationship between the effects of ivermectin-treated cattle and post-treatment time on proportion of mosquitoes laid eggs

Fig. 4

Estimates (±1 s.e) of the mean number of eggs laid by An. arabiensis after obtaining blood meal from control and ivermectin-treated cattle: a effects of ivermectin-treated cattle on fecundity of mosquitoes, and b the relationship between the effects of ivermectin-treated cattle and post-treatment time on fecundity of mosquitoes

Fig. 5

Estimates of the survival of An. arabiensis after blood feeding on control and ivermectin-treated cattle. The effects of ivermectin-treated cattle on survival of mosquitoes were estimated at different time points: a Day zero, b Day 3, c Day 6, d Day 9, e Day 12, f Day 15, g Day 18, and h Day 21 post-treatment. The lines represent the survival function as estimated from the fitting Cox proportional hazard model (controlling for random variation of between individual cattle)

Fig. 6

Estimates of odds of mortality of An. arabiensis after blood feeding on control and ivermectin-treated cattle