Abstract
BackgroundThe success of current control tools in combatting malaria vectors is well established. However, sustained residual transmission of Plasmodium parasites persists. Mass drug administration (MDA) to humans of the endectocide ivermectin for vector control is receiving increasing attention. However, vectors feeding upon animals escape this promising approach. Zoophagy of mosquitoes sustains both the vector population and endemic population of vector-borne pathogens. Therefore, only a strategy that will combine ivermectin MDAs targeted at humans and their peridomestic animals could be successful at controlling residual malaria transmission.MethodsBurkinabé cattle have been treated with injectable therapeutic dose of ivermectin (0.2 mg/kg of body weight) to render blood meals toxic to field representative populations of Anopheles coluzzii carrying the kdr mutation. Direct skin-feeding assays were performed from 2 to 28 days after injection (DAI) and mosquitoes were followed for their survival, ability to become gravid and fecundity. Membrane feeding assays were further performed to test if an ivermectin blood meal taken at 28 DAI impacts gametocyte establishment and development in females fed with infectious blood.ResultsThe mosquitocidal effect of ivermectin is complete for 2 weeks after injection, whether 12 days cumulative mortalities were of 75 and 45 % the third and fourth weeks, respectively. The third week, a second ivermectin blood meal at sub-lethal concentrations further increased mortality to 100 %. Sub-lethal concentrations of ivermectin also significantly decreased egg production by surviving females, increasing further the detrimental effect of the drug on vector densities. Although females fitness was impaired by sub-lethal ivermectin blood meals, these did not diminish nor increase their susceptibility to infection.ConclusionThis study demonstrates the potential of integrated MDA of ivermectin to both human and peridomestic cattle to target vector reservoirs of residual malaria transmission. Such integration lies in ‘One-Health’ efforts being implemented around the globe, and would be especially relevant in rural communities in Africa where humans are also at risk of common zoonotic diseases.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-015-1001-z) contains supplementary material, which is available to authorized users.
Highlights
The success of current control tools in combatting malaria vectors is well established
Survival Experiments investigating the toxic effect of a blood meal taken from ivermectin-treated cattle included 960 females followed after their blood meal and until their death
For the females fed on cattle before injection of ivermectin, the Cox proportional hazards model revealed no significant effect of cattle identity on survival (χ23 = 1.42, p = 0.69), which was on average 17.77 ± 1.52 days, 19.80 ± 0.88, 20.14 ± 1.22, and 21.32 ± 0.73 days
Summary
The success of current control tools in combatting malaria vectors is well established. Insecticide avoidance, exophily, exophagy, and zoophagy [4], are all behaviours that minimize the contact between the mosquito and the insecticides, and contribute to the build-up of reservoirs of vector populations responsible for residual transmission of diseases In this context, mass drug administration (MDA) of endectocidal drugs to humans for human malaria control is receiving increasing attention [5, 6]. Endectocides are drugs that have activity against endo- and ectoparasites among which ivermectin was first introduced for commercial use as an anti-parasitic drug for animal (livestock and pets) use in 1981 This molecule shares with other avermectins and mylbemicins a pharmacophore consisting on 16-membered macrocyclic lactone, and is an agonist of specific chloride ion channels (primarily glutamate-gated chloride channels). The straightforward rationale of using ivermectin MDA for vector control lies on the fact that the treated human directly delivers the toxic molecule to any human-feeding mosquito regardless of its genus, species, and possibly for a large spectrum of the behavioural resistance it might display, i.e., mosquitoes of diurnal or nocturnal activities, resting indoors or outdoors, feeding indoors or outdoors, could be targeted
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