Mosquito and human characteristics influence natural Anopheline biting behavior andPlasmodium falciparumtransmission

Abstract

AbstractThe human infectious reservoir ofPlasmodium falciparummalaria parasites is governed by the efficiency of parasite transmission during vector human contact as well as mosquito biting preferences. Understanding mosquito biting bias in a natural setting can help inform precise targeting of interventions to efficiently interrupt transmission. In a 15-month longitudinal cohort study in a high transmission setting in western Kenya, we investigated human and mosquito factors associated with differential mosquito biting by matching human DNA in single- and multi-sourceAnophelesbloodmeals to the individuals they bit. We employed risk factor analyses and econometric models of probabilistic choice to assess mosquito biting behavior with respect to both human-to-mosquito transmission and mosquito-to-human transmission. We observed thatP. falciparum-infected school-age boys accounted for 50% of bites potentially leading to onward transmission to mosquitoes and had an entomological inoculation rate 6.4x higher than any other group, that infectious mosquitoes were 2.8x more likely to bite cohort members harboringP. falciparumparasites compared to noninfectious mosquitoes, and that this preference to feed on infected people was enhanced by the presence of higher sporozoite loads in the mosquito head-thorax. Taken together, these results suggest that school-age boys disproportionately contribute to theP. falciparumtransmission cycle and thatP. falciparumsporozoites modify mosquito biting preferences to favor feeding on infected people.SignificanceThe malaria parasite transmission cycle is doubly-dependent on mosquito-human contact rates. To efficiently deploy transmission-reducing interventions, it is important to understand how mosquito biting preferences shape the human infectious reservoir. Here, we match human DNA in mosquito bloodmeals to the people they bit to quantify mosquito biting preferences and understand how mosquito characteristics shape these preferences. We observed that school-age boys were bitten the most and contributed most to onward transmission to mosquitoes. We also observed that, compared to non-infectious mosquitoes, mosquitoes harboring infectiousPlasmodium falciparumwere more likely to biteP. falciparum-infected people. These observations increase our understanding of malaria parasite transmission and evolution and provide a foundation for developing effective transmission-reducing interventions.