Insecticide resistance profiles of Anopheles arabiensis and relationship with Microsporidia MB infection in two rice agroecosystems in Kenya

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Abstract

Background Insecticide resistance has emerged as a serious threat to malaria control in sub-Saharan Africa. Knowing the insecticide susceptibility status of vector populations is crucial for designing evidence-based insecticide resistance management plans. This study assessed susceptibility status of Anopheles arabiensis populations from Mwea and Ahero rice irrigation schemes to six insecticides. The association between insecticide resistance and Microsporidia MB infection, a symbiont known to block malaria transmission in An. arabiensis was also investigated. Methods Three to five-day old F1 An. arabiensis females were exposed to permethrin, deltamethrin, alphacypermethrin, malathion, bendiocarb, and DDT using CDC bottle bioassay. Resistance intensity assays and synergist bioassays with piperonyl butoxide (PBO) were conducted to evaluate the strength of pyrethroids resistance and the contribution of cytochrome P450s to pyrethroids resistance, respectively. qPCR was used to detect and quantify Microsporidia MB infection following permethrin exposure. Results Anopheles arabiensis populations from both study sites were fully susceptible to bendiocarb but showed resistance to all the three pyrethroids. Resistance intensity to permethrin was markedly higher in Ahero, reaching 10x the diagnostic dose. The Ahero population showed high susceptibility to malathion but reduced susceptibility to DDT, while the Mwea population displayed the opposite pattern. Pre-exposure to PBO fully restored pyrethroid susceptibility in the Mwea population indicating metabolic resistance. It partially restored pyrethroid susceptibility in the Ahero population, indicating the presence of other resistance mechanisms. Microsporidia MB was detected in the Ahero population, with infection density higher in mosquitoes that survived 2x and 5x permethrin dose compared to those that succumbed to these doses. Conclusions Anopheles arabiensis populations from irrigated ecosystems exhibit heterogeneous yet high levels of insecticides resistance, particularly to pyrethroids driven mostly by detoxification enzymes. These findings highlight the need to incorporate synergist-based interventions into resistance management strategies. The high intensity of Microsporidia MB infection in Ahero mosquitoes that survived 2x and 5x discriminating doses of permethrin warrants further investigation to determine if there is a direct link between the symbiont and mosquito’s resistance mechanisms.

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