Effects of ivermectin treatment of backyard chickens on mosquito dynamics and West Nile virus transmission

PLOS NEGLECTED TROPICAL DISEASES(2022)

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Abstract
BackgroundVector control strategies typically rely on pesticides to target mosquitoes involved in enzootic and zoonotic transmission of West Nile virus (WNV). Nevertheless, increasing insecticide resistance and a desire to reduce pesticide usage provide the impetus for developing alternative strategies. Ivermectin (IVM), an antiparasitic drug which is widely used in human and veterinary medicine, is a potential alternative for targeted control because Culex mosquitoes experience increased mortality following ingestion of IVM in bloodmeals. Methodology/Principal findingsWe conducted a randomized field trial to investigate the impact of treating backyard chicken flocks with IVM in urban neighborhoods across Davis, California on mosquito populations and WNV transmission dynamics. We observed a significant reduction in WNV seroconversions in treated vs. untreated chickens, suggesting a reduction in WNV transmission intensity around treated flocks. We also detected a reduction in parity rates of Cx. tarsalis near treated vs. untreated flocks and increased mortality in wild mosquitoes following a bloodmeal on treated chickens (IVM serum concentration > 5ng/mL) vs. chickens with IVM serum concentrations < 5 ng/mL. However, we did not find a significant difference in abundance or infection prevalence in mosquitoes between treatment groups associated with the reductions in seroconversions. Mosquito immigration from surrounding larval habitat, relatively low WNV activity in the study area, and variable IVM serum concentrations likely contributed to uncertainty about the impact. Conclusions/SignificanceTaken together, our results point to a reduction in WNV transmission due to the impact of IVM on Culex mosquito populations and support the ongoing investigation of oral administration of IVM to wild birds for local control of WNV transmission, although further work is needed to optimize dosing and understand effects on entomological endpoints. Author summaryCurrent mosquito control strategies aimed to prevent pathogen transmission to humans have limited ability to target mosquitoes involved in amplification and spillover transmission of pathogens like West Nile virus (WNV). Additionally, growing prevalence of insecticide resistance in mosquito populations limit the efficacy of these insecticide-based control strategies. Ivermectin (IVM) provides an alternative avenue for control by increasing the mortality of mosquitoes that ingest this drug in bloodmeals. Therefore, IVM treatment of avian species that account for the majority of mosquito bloodmeals during the WNV transmission season could be an effective control strategy. Building on pilot studies indicating the efficacy and feasibility of IVM-deployment for WNV control, we performed a randomized field trial to investigate the impact of IVM-treatment of backyard chickens on local population dynamics of Culex mosquitoes and WNV transmission. We were able to link changes in mosquito populations to reduction in WNV transmission, as measured by chicken seroconversions, through IVM-induced mortality in mosquitoes. However, further work is needed to identify the impact of treatment on mosquito abundance and infection prevalence to fully attribute observed changes to IVM administration. Overall, our results support IVM treatment as a potentially effective alternative to insecticide-based vector control strategies and one that can be used to target WNV transmission on the local scale.
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