Insecticide resistance in disease vectors from Mayotte: an opportunity for integrated vector management

Abstract

Background: Mayotte, a small island in the Indian Ocean, has been affected for many years by vector-borne diseases. Malaria, Bancroftian filariasis, dengue, chikungunya and Rift Valley fever have circulated or still circulate on the island. They are all transmitted by Culicidae mosquitoes. To limit the impact of these diseases on human health, vector control has been implemented for more than 60 years on Mayotte. In this study, we assessed the resistance levels of four major vector species (Anopheles gambiae, Culex pipiens quinquefasciatus, Aedes aegypti and Aedes albopictus) to two types of insecticides: i) the locally currently-used insecticides (organophosphates, pyrethroids) and ii) alternative molecules that are promising for vector control and come from different insecticide families (bacterial toxins or insect growth regulators). When some resistance was found to one of these insecticides, we characterized the mechanisms involved.

Methods: Larval and adult bioassays were used to evaluate the level of resistance. When resistance was found, we tested for the presence of metabolic resistance through detoxifying enzyme activity assays, or for target-site mutations through molecular identification of known resistance alleles.

Results: Resistance to currently-used insecticides varied greatly between the four vector species. While no resistance to any insecticides was found in the two Aedes species, bioassays confirmed multiple resistance in Cx. p. quinquefasciatus (temephos: ~ 20 fold and deltamethrin: only 10% mortality after 24 hours). In An. gambiae, resistance was scarce: only a moderate resistance to temephos was found (~5 fold). This resistance appears to be due only to carboxyl-esterase overexpression and not to target modification. Finally, and comfortingly, none of the four species showed resistance to any of the new insecticides.

Conclusions: The low resistance observed in Mayotte's main disease vectors is particularly interesting, because it leaves a range of tools useable by vector control services. Together with the relative isolation of the island (thus limited immigration of mosquitoes), it provides us with a unique place to implement an integrated vector management plan, including all the good practices learned from previous experiences.

Figure 1

Sampled populations in Mayotte. Sampling was carried out in Dzoumogné for the DZOU colony of An. gambiae, in Tsoundzou 1 for TZ1 colony of Cx. p. quinquefasciatus, in Kaweni for KWI colony of Ae. albopictus and in Petite Terre for PT colony of Ae. aegypti.

Figure 2

Insecticide resistance in vector mosquitoes from Mayotte. The resistance ratios (RR₅₀, i.e. the ratios of LC₅₀ of the tested colonies over the LC₅₀ of the susceptible reference strain), of colonies from field populations of Ae. aegypti (gray), Ae. albopictus (purple) Cx. p. quinquefasciatus (red) and An. gambiae (orange) to different tested insecticides are presented. The error bars represent the confidence interval of RR at 95%. The solid red line represents RR = 1 (i.e. a LC₅₀ equal to that of the susceptible reference) and the dotted red line represents RR = 3 (resistance is considered of biological significance when above). RR significantly higher than 1 (i.e. when CI₉₅ does not include 1) are indicated by a star.

Figure 3

Temephos resistance in the DZKIS strain. The graph shows the evolution of the resistance level to temephos of the DZKIS strain in the 1^st, 6^th and 10^th (i.e. the last) generations of selection. The dose-mortality of the DZOU original colony and of the KIS and AcerKIS reference strains (respectively susceptible and resistant to OPs through the G119S ace-1 mutation) are also presented.

Figure 4

Comparison of detoxification enzyme quantities or activities in single mosquitoes of KIS and DZOU. The amount of cytochrome P450 oxidase (A) (MFO) is expressed in pmol of P450 Equivalent Unit per mg of protein for each mosquito. Activities of α (B) and β-esterases (C) (COE) are expressed as nmol of product formed (α or β-naphthol) per minute and per mg of protein.