Assessing the effects of three anthropogenic activities on the mosquito, Anopheles gambiae s.l. species composition and pyrethroid resistance mechanisms in Abidjan city, Côte d'Ivoire

Med Vet Entomol. 2024 Sep 16. doi: 10.1111/mve.12759. Online ahead of print.

Abstract

Pyrethroid resistance and mechanisms for resistance for Anopheles gambiae sensus lato (s.l.) (Diptera: Culicidae) Giles, were assessed in three urban areas (vegetable farming, industrial and residential) of Abidjan. Susceptibility to pyrethroids (deltamethrin, permethrin and alphacypermethrin), with and without piperonyl butoxide (PBO) pre-exposure was evaluated. Anopheles gambiae complex members were identified using Short Interspersed Nuclear Elements PCR (SINE PCR), and resistance mechanisms (kdr-west, kdr-east and ace-1) and metabolic gene expression (CYP6P5, CYP6M2, CYP6P3, CYP6P4) were determined by real-time polymerase chain reaction (PCR). High resistance to deltamethrin, permethrin and alphacypermethrin was observed in Port-Bouet (vegetable farming) and Treichville (industrial site), whereas moderate resistance to deltamethrin and high resistance to alphacypermethrin and permethrin were found in Abobo (residential site). Pre-exposure to PBO with pyrethroid increased mortalities in all sites. In Treichville, pre-exposure to PBO restored susceptibility to deltamethrin, but not in Port-Bouet or Abobo. In Treichville, An. gambiae Giles sensu stricto (s.s.) was predominant (92.9%), whereas in Abobo and Port-Bouet, An. coluzzii Giles was predominant (73.6% and 66.4%, respectively). The highest kdr-west mutation frequency was in An. gambiae s.s. (42.8%) from Abobo, followed by An. gambiae s.s. (40%) from Port-Bouet and An. gambiae s.s. (35.6%) from Treichville. In An. coluzzii, the highest kdr-west mutation frequency was in Port-Bouet (48.2%), followed by Abobo (28.00%) and Treichville (21.4%). Mutation frequencies of kdr-east were lower in An. gambiae s.s. from Treichville (4.1%) and Port-Bouet (2.1%) and absent in An. gambiae from Abobo. In industrial and vegetable farming areas, CYP6P3 and CYP6M2 were overexpressed compared with Kisumu. The study suggests An. gambiae s.l. distribution and pyrethroid resistance are influenced by human activities. Treichville's industrial area favoured An. gambiae s.s., whereas Abobo's residential and Port-Bouet's vegetable farming areas were dominated by An. coluzzii. Resistance in Treichville and Port-Bouet was associated with kdr (west and east) genes and metabolic genes, whereas in residential areas, only kdr-west genes were observed. These data suggest that PBO + deltamethrin impregnated nets could aid malaria control, benefiting industrial areas of Côte d'Ivoire and other African cities.

Keywords: Anopheles gambiae s.l.; Côte d'Ivoire; anthropogenic activity; city; malaria; pyrethroid resistance; species composition.