Reduced performance of community bednets against pyrethroid-resistant Anopheles funestus and Anopheles gambiae, major malaria vectors in Cameroon

Abstract

Background Long-lasting insecticidal nets (LLINs) are a vital tool in the fight against malaria vectors. However, their efficacy in the field can be impacted by several factors, including patterns of usage, net age, mosquito resistance and the delayed mortality effect, all of which could influence malaria transmission. We have investigated the effectiveness of the various brands of LLINs available in markets and households in Cameroon on pyrethroid-resistant mosquitoes and assessed their post-exposure effect. Methods Following quality control assessment on a susceptible laboratory mosquito strain, we evaluated the immediate and delayed mortality effects of exposure to LLINs (both newly bough LLINst and used ones collected from households in Elende village, Cameroon, in 2019) using standard WHO cone tests on Anopheles gambiae and Anopheles funestus populations collected from the Centre region of Cameroon. Alive female mosquitoes were genotyped for various resistance markers at different time points post-exposure to evaluate the impact of insecticide resistance on the efficacy of bednets. Results The laboratory-susceptible strain experienced high mortality rates when exposed to all pyrethroid-only brands of purchased nets (Olyset® Net, Super Net, PermaNet® 2.0, Yorkool®, Royal Sentry®) (Mean±SEM: 68.66 ± 8.35% to 93.33 ± 2.90%). However, low mortality was observed among wild An. funestus mosquitoes exposed to the bednets (0 ± 0 to 28 ± 6.7%), indicating a reduced performance of these nets against field mosquitoes. Bednets collected from households also showed reduced efficacy on the laboratory strain (mortality: 19–66%), as well as displaying a significant loss of efficacy against the local wild strains (mortality: 0 ± 0% to 4 ± 2.6% for An. gambiae sensu lato and 0 ± 0% to 8 ± 3.2% for An. funestus). However, compared to the unexposed group, mosquitoes exposed to bednets showed a significantly reduced longevity, indicating that the efficacy of these nets was not completely lost. Mosquitoes with the CYP6P9a-RR and L119F-GSTe2 mutations conferring pyrethroid resistance showed greater longevity after exposure to the Olyset net than their susceptible counterparts, indicating the impact of resistance on bednet efficacy and delayed mortality. Conclusion These findings show that although standard bednets drastically lose their efficacy against pyrethroid-resistant field mosquitoes, they still are able to induce delayed mortality in exposed populations. The results of this study also provide evidence of the actual impact of resistance on the quality and efficacy of LLINs in use in the community, with mosquitoes carrying the CYP6P9a-RR and L119F-GSTe2 mutations conferring pyrethroid resistance living longer than their susceptible counterparts. These results highlight the need to use new-generation nets that do not rely solely on pyrethroids. Graphical Abstract

Distribution and insecticide resistance profile of the major malaria vector Anopheles funestus group across the African continent

“…This insecticide resistance involving different mechanisms may lead to the loss of insecticide efficacy, and subsequently partial operational failure of malaria control, and increased malaria transmission. Pyrethroid resistance accumulation reduces bed net efficacy by compromising the killing effect associated with insecticides (Ngongang‐Yipmo et al, 2022; Tchouakui, Mugenzi, Menze B, et al, 2021), even though there is inconsistent evidence as to whether such failures actually lead to loss of effectiveness of the nets in the field.…”

“…In eastern Africa, pyrethroid and carbamate resistances were recorded in Zambia and Zimbabwe (Choi et al, 2014); and pyrethroid and dichlorodiphenyltrichloroethane (DDT) resistances were recorded in Uganda, Malawi, Tanzania and Kenya (Mulamba, Irving, et al, 2014; Mulamba, Riveron, et al, 2014; Pinda et al, 2022; Riveron et al, 2015). In Central Africa, pyrethroid, dieldrin and DDT resistances were reported in Cameroon (Antonio‐Nkondjio et al, 2017; Menze et al, 2022; Ngongang‐Yipmo et al, 2022). Pyrethroid resistance was recorded in South Africa (Venter et al, 2017).…”

Pyrethroid-treated bed nets impair blood feeding performance in insecticide resistant mosquitoes

“…The effectiveness of an ITN depends not only on its ability to rapidly kill the mosquito shortly after its exposure to the insecticide but also on the sub-lethal effects of the insecticide on host-seeking, feeding, egg laying or longevity 4 , 6 – 8 . In the last decade, studies have shown that ITNs reduce blood feeding success and limit the number of mosquitoes that live long enough to enable the completion of the parasite extrinsic incubation period 9 – 13 . These effects of ITNs might be minimal in some conditions 14 or may be enhanced by repeated exposures to insecticide 9 , 11 , 15 .…”

Transcriptomics analysis of ethanol treatment of male Aedes aegypti reveals a small set of putative radioprotective genes

“…As more evidence emerges to demonstrate the spread of insects with evolved resistance to many commonly used chemical agents, novel mechanisms are necessary to prevent the spread of insect pests ( Liu et al, 2000 ; Moyes et al, 2017 ; Amelia-Yap et al, 2018 ; Fotakis et al, 2018 ; Macoris et al, 2018 ; Chen et al, 2019 ; Kandel et al, 2019 ; Ngongang-Yipmo et al, 2022 ; Pichler et al, 2022 ; Pudasaini et al, 2022 ). Sterile Insect Technique (SIT) is an effective biological control mechanism that has been successfully used to eliminate populations of a variety of insect pest species ( Vargas-Terán et al, 1994 ; Vreysen et al, 2000 ; Ant et al, 2012 ; Hyseni et al, 2012 ).…”