Plasmodium falciparum infection in humans and mosquitoes influence natural Anopheline biting behavior and transmission

Christine F. Markwalter, Zena Lapp, Lucy Abel, Emmah Kimachas, Evans Omollo, Elizabeth Freedman, Tabitha Chepkwony, Mark Amunga, Tyler McCormick, Sophie Bérubé, Judith N. Mangeni, Amy Wesolowski, Andrew A. Obala, Steve M. Taylor () and Wendy Prudhomme O’Meara ()
Additional contact information
Christine F. Markwalter: Duke University
Zena Lapp: Duke University
Lucy Abel: Moi Teaching and Referral Hospital
Emmah Kimachas: Moi Teaching and Referral Hospital
Evans Omollo: Duke Global Inc
Elizabeth Freedman: Duke University School of Medicine
Tabitha Chepkwony: Moi Teaching and Referral Hospital
Mark Amunga: Moi Teaching and Referral Hospital
Tyler McCormick: University of Washington
Sophie Bérubé: Johns Hopkins Bloomberg School of Public Health
Judith N. Mangeni: Moi University
Amy Wesolowski: Johns Hopkins Bloomberg School of Public Health
Andrew A. Obala: Moi University
Steve M. Taylor: Duke University
Wendy Prudhomme O’Meara: Duke University

Nature Communications, 2024, vol. 15, issue 1, 1-11

Abstract: Abstract The human infectious reservoir of Plasmodium falciparum is governed by transmission efficiency during vector-human contact and mosquito biting preferences. Understanding biting bias in a natural setting can help target interventions to interrupt transmission. In a 15-month cohort in western Kenya, we detected P. falciparum in indoor-resting Anopheles and human blood samples by qPCR and matched mosquito bloodmeals to cohort participants using short-tandem repeat genotyping. Using risk factor analyses and discrete choice models, we assessed mosquito biting behavior with respect to parasite transmission. Biting was highly unequal; 20% of people received 86% of bites. Biting rates were higher on males (biting rate ratio (BRR): 1.68; CI: 1.28–2.19), children 5–15 years (BRR: 1.49; CI: 1.13–1.98), and P. falciparum-infected individuals (BRR: 1.25; CI: 1.01–1.55). In aggregate, P. falciparum-infected school-age (5–15 years) boys accounted for 50% of bites potentially leading to onward transmission and had an entomological inoculation rate 6.4x higher than any other group. Additionally, infectious mosquitoes were nearly 3x more likely than non-infectious mosquitoes to bite P. falciparum-infected individuals (relative risk ratio 2.76, 95% CI 1.65–4.61). Thus, persistent P. falciparum transmission was characterized by disproportionate onward transmission from school-age boys and by the preference of infected mosquitoes to feed upon infected people.

Date: 2024
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DOI: 10.1038/s41467-024-49080-9

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