Elevated Plasmodium sporozoite infection and multiple insecticide resistance in the principal malaria vectors Anopheles funestus and Anopheles gambiae in a forested locality close to the Yaoundé airport, Cameroon
Francis N. Nkemngo, Leon M. J. Mugenzi, Ebai Terence, Abdoulaye Niang, Murielle J. Wondji, Micareme Tchoupo, Nguiffo D. Nguete, Williams Tchapga, Helen Irving, Jacques Dollon Mbama Ntabi, Romuald Agonhossou, Terence S. Boussougou-Sambe, Romaric Akoton, Félix Koukouikila-Koussounda, Yudi T. Pinilla, Francine Ntoumi, Luc Djogbénou, Stephen Mbigha Ghogomu, Cyrille Ndo, Ayôla Akim Adégnika, Steffen Borrmann, Charles S. Wondji
Abstract
<ns4:p> <ns4:bold>Background:</ns4:bold> Reducing the burden of malaria requires better understanding of vector populations, particularly in forested regions where the incidence remains elevated. Here, we characterized malaria vectors in a locality near the Yaoundé international airport, Cameroon, including species composition, abundance, <ns4:italic>Plasmodium</ns4:italic> infection rate, insecticide resistance profiles and underlying resistance mechanisms. </ns4:p> <ns4:p> <ns4:bold>Methods:</ns4:bold> Blood-fed adult mosquitoes resting indoors were aspirated from houses in April 2019 at Elende, a village located 2 km from the Yaoundé-Nsimalen airport. Female mosquitoes were forced to lay eggs to generate F <ns4:sub>1</ns4:sub> adult progeny. Bioassays were performed to assess resistance profile to insecticides. The threshold of insecticide susceptibility was defined above 98% mortality rate and mortality rates below 90% were indicative of confirmed insecticide resistance. Furthermore, the molecular basis of resistance and <ns4:italic>Plasmodium</ns4:italic> infection rates were investigated. </ns4:p> <ns4:p> <ns4:bold>Results:</ns4:bold> <ns4:italic>Anopheles funestus</ns4:italic> s.s. was most abundant species in Elende (85%) followed by <ns4:italic>Anopheles gambiae</ns4:italic> s.s. (15%) with both having a similar sporozoite rate. Both species exhibited high levels of resistance to pyrethroids (<40% mortality). <ns4:italic>An. gambiae</ns4:italic> s.s. was also resistant to DDT (9.9% mortality) and bendiocarb (54% mortality) while susceptible to organophosphate. <ns4:italic>An. funestus</ns4:italic> s.s. was resistant to dieldrin (1% mortality), DDT (86% mortality) but susceptible to carbamates and organophosphates. The L119F-GSTe2 resistance allele (8%) and G119S <ns4:italic>ace</ns4:italic> -1 resistance allele (15%) were detected in <ns4:italic>An. funestus</ns4:italic> s.s. and <ns4:italic>An. gambiae</ns4:italic> s.s., respectively <ns4:italic>.</ns4:italic> Furthermore, the high pyrethroid/DDT resistances in <ns4:italic>An. gambiae</ns4:italic> s.s. corresponded with an increase frequency of 1014F <ns4:italic>kdr</ns4:italic> allele (95%). Transcriptional profiling of candidate cytochrome P450 genes reveals the over-expression of <ns4:italic>CYP6P5</ns4:italic> , <ns4:italic>CYP6P9a</ns4:italic> and <ns4:italic>CYP6P9b.</ns4:italic> </ns4:p> <ns4:p> <ns4:bold>Conclusion:</ns4:bold> The resistance to multiple insecticide classes observed in these vector populations alongside the high <ns4:italic>Plasmodium</ns4:italic> sporozoite rate highlights the challenges that vector control programs encounter in sustaining the regular benefits of contemporary insecticide-based control interventions in forested areas. </ns4:p>