Differential effect of human ivermectin treatment on blood feeding Anopheles gambiae and Culex quinquefasciatus

Abstract

Background: Widespread and large scale use of ivermectin in humans and domestic animals can have unexpected effects on non-target organisms. As a search for a possible explanation for an observed longitudinal decline in density of anopheline vector mosquitoes, but not in Culex quinquefasciatus, in an area of north-eastern Tanzania which has been exposed to ivermectin mass drug administration, this study assessed and compared the effect of human ivermectin treatment on blood feeding Anopheles gambiae and Cx. quinquefasciatus.

Methods: Consenting adult volunteers were randomized into two groups to receive either ivermectin or placebo. Twenty four hours after treatment, one volunteer from each group was concurrently exposed to 50 laboratory reared An. gambiae on one arm and 50 laboratory reared Cx. quinquefasciatus on the other arm for 15-30 minutes. Engorged mosquitoes were maintained on 10% glucose solution for 12 days and observed for survival and fecundity. The experiment was repeated 15 times.

Results: Two days after the blood meals, nearly half (average 47.7% for the 15 experiments) of the blood fed An. gambiae in the ivermectin group had died while almost all in the placebo group were alive (97.2%), and the difference in survival between these two groups continued to widen on the following days. There was no clear effect of ivermectin on Cx. quinquefasciatus, which had high survival in both ivermectin and placebo group on day 2 (95.7% and 98.4%, respectively) as well as on the following days. Ivermectin completely inhibited egg laying in An. gambiae, while egg laying and subsequent development of immature stages appeared normal in the other three groups.

Conclusion: Blood meals taken on ivermectin treated volunteers significantly reduced survival and halted fecundity of An. gambiae but had only limited or no effect on Cx. quinquefasciatus. The result suggests that widespread use of ivermectin may have contributed to the observed decline in density of An. gambiae, without similar decrease in Cx. quinquefasciatus, in north-eastern Tanzania.

Figure 1

Survival of Anopheles gambiae and Culex quinquefasciatus after taking a blood meal on human volunteers who had ingested ivermectin (150–200 μg/kg) or placebo. Graphs show mean of % survival in the individual experiments for the four groups during the first 8 days. 15 experiments were carried out, but data were excluded from both ivermectin and placebo group of the same mosquito species when the mortality in the placebo group exceeded 20%. Thus, for the two An. gambiae groups, data on days 7 and 8 are based on 13 and 6 experiments, while for the two Cx. quinquefasciatus groups, data on days 6, 7 and 8 are all based on 13 experiments (see also Table 3).