Abstract

BackgroundInsecticide resistance is threatening the effectiveness of efforts to control malaria vectors in Benin. This study explores the levels and mechanisms of insecticide resistance in An. gambiae s.l. to pyrethroids.MethodsLarvae were collected from August 2017 to July 2018 in five communes in southern Benin (Adjohoun, Allada, Bohicon, Cotonou, and Porto-Novo) representing diverse ecological regions, and were reared in Benin’s insectary. Two- to five-day-old female mosquitoes from each district were exposed to multiple doses of deltamethrin and permethrin (1×, 2×, 5×, and 10×) using the WHO insecticide resistance intensity bioassay. The effect of pre-exposure to the synergist, piperonyl butoxide (PBO), was also tested at different pyrethroid doses. Molecular allele frequencies of kdr (1014F) and ace-1R (119S) insecticide resistance mutations and levels of detoxification enzymes were determined for mosquitoes sampled from each study area.ResultsAn. gambiae s.l. were resistant to pyrethroid-only exposure up to 10× the diagnostic doses in all the study sites for both deltamethrin and permethrin. Mortality was significantly higher in An. gambiae s.l. pre-exposed to PBO followed by exposure to deltamethrin or permethrin compared to mosquitoes exposed to deltamethrin or permethrin only (p < 0.001). The difference in mortality between deltamethrin only and PBO plus deltamethrin was the smallest in Cotonou (16–64%) and the greatest in Bohicon (12–93%). The mortality difference between permethrin only and PBO plus permethrin was the smallest in Cotonou (44–75%) and the greatest in Bohicon (22–72%). In all the study sites, the kdr resistance allele (1014F) frequency was high (75–100%), while the ace-1 resistance allele (G119S) frequency was low (0–3%). Analysis of the metabolic enzymatic activity of An. gambiae s.l. showed overexpression of nonspecific esterases and glutathione S-transferases (GST) in all study sites. In contrast to the PBO results, oxidase expression was low and was similar to the susceptible An. gambiae s.s. Kisumu strain in all sites.ConclusionThere is high-intensity resistance to pyrethroids in southern Benin. However, pre-exposure to PBO significantly increased susceptibility to the pyrethroids in the different An. gambiae s.l. populations sampled. The use of PBO insecticide-treated bed nets may help maintain the gains in An. gambiae (s.l.) control in southern Benin.Graphical

Highlights

  • Insecticide resistance is threatening the effectiveness of efforts to control malaria vectors in Benin

  • A total of 1697 female An. gambiae s.l. were exposed to different deltamethrin doses in all study sites

  • This study showed a high intensity of deltamethrin and permethrin resistance in An. gambiae s.l. using different insecticide doses in southern Benin

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Summary

Introduction

Insecticide resistance is threatening the effectiveness of efforts to control malaria vectors in Benin. This study explores the levels and mechanisms of insecticide resistance in An. gambiae s.l. to pyrethroids. In Benin, IRS and LLINs are the main vector control interventions implemented by the National Malaria Control Program (NMCP). The most widely studied pyrethroid resistance mechanisms of An. gambiae s.l. are (1) modification of the insecticide target site by kdr mutation [11,12,13] and (2) overexpression of the detoxification enzymes using oxidases or glutathione S-transferases (GSTs) [14,15,16]. The kdr insecticide resistance mutation—a replacement of leucine by phenylalanine in the kdr 1014 gene (L1014F)—is widespread in West Africa [17,18,19], while the replacement with serine (L1014S) is widespread in some regions of Central and East Africa [20,21,22]

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