Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana

Abstract

Background Aggravation of insecticide resistance in malaria vectors is threatening the efforts to control malaria by reducing the efficacy of insecticide-based interventions hence needs to be closely monitored. This study investigated the intensity of insecticide resistance of two major malaria vectors An. funestus sensu stricto (s.s.) and An. gambiae sensu lato (s.l.) collected in southern Ghana and assessed the bio-efficacy of several long-lasting insecticidal nets (LLINs) against these mosquito populations. Methods The insecticide susceptibility profiles of Anopheles funestus s.s. and Anopheles gambiae s.l. populations from Obuasi region (Atatam), southern Ghana were characterized and the bio-efficacy of some LLINs was assessed to determine the impact of insecticide resistance on the effectiveness of these tools. Furthermore, molecular markers associated with insecticide resistance in both species were characterized in the F0 and F1 populations using PCR and qPCR methods. Results Anopheles funestus s.s. was the predominant species and was resistant to pyrethroids, organochlorine and carbamate insecticides, but fully susceptible to organophosphates. An. gambiae s.l. was resistant to all four insecticide classes. High intensity of resistance to 5 × and 10 × the discriminating concentration (DC) of pyrethroids was observed in both species inducing a considerable loss of efficacy of long-lasting insecticidal nets (LLINs). Temporal expression analysis revealed a massive 12-fold increase in expression of the CYP6P4a cytochrome P450 gene in An. funestus s.s., initially from a fold change of 41 (2014) to 500 (2021). For both species, the expression of candidate genes did not vary according to discriminating doses. An. gambiae s.l. exhibited high frequencies of target-site resistance including Vgsc-1014F (90%) and Ace-1 (50%) while these mutations were absent in An. funestus s.s. Conclusions The multiple and high intensity of resistance observed in both malaria vectors highlights the need to implement resistance management strategies and the introduction of new insecticide chemistries.

Distribution and insecticide resistance profile of the major malaria vectorAnopheles funestusgroup across theAfricancontinent

“…funestus populations are resistant to DDT, permethrin, deltamethrin and bendiocarb, and decreased susceptibility to dieldrin was noted (Akoton et al, 2018; Djouaka et al, 2011; Djouaka et al, 2017; Djouaka, Riveron, et al, 2016). Similar results were observed in Ghana but with susceptibility to malathion and organophosphates (Mugenzi et al, 2022; Riveron et al, 2016). In Nigeria, resistance to dieldrin (8%) and DDT (10%), permethrin (68%), deltamethrin (87%) and bendiocarb (84%) have been recorded (Djouaka, Atoyebi, et al, 2016).…”

“…In West Africa, An. funestus resistance to dieldrin was recorded in Burkina Faso (Dabiré et al, 2007) and pyrethroids, organochlorine and carbamate resistance were recorded in Ghana (Mugenzi et al, 2022). 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).…”

Two highly selected mutations in the tandemly duplicatedCYP6P4aandCYP6P4bdrive pyrethroid resistance inAnopheles funestus

“…S8E). These mortalities are far higher than the 11.6±5% for permethrin 1× and 1.25±1.25% for alpha-cypermethrin 1x, previously recorded in the field mosquitoes in the same year 21 , highlighting the potential association between these markers and the phenotype. S6).…”

Contrasting Patterns of Asaia Association with Pyrethroid Resistance Escalation between the Malaria Vectors Anopheles funestus and Anopheles gambiae

“…Even so, increasing reports of elevated levels of pyrethroid resistance in the major vectors, including Anopheles gambiae and Anopheles funestus, are threatening to derail the efficacy of these control tools [ 4 ]. In several countries, including Malawi [ 5 ], Uganda [ 6 ], and Ghana [ 7 ], An. funetus and An.…”