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

Author

Listed:
  • 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
    Duke University School of Medicine)

  • Wendy Prudhomme O’Meara

    (Duke University
    Duke University School of Medicine)

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.

Suggested Citation

  • 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 Wesol, 2024. "Plasmodium falciparum infection in humans and mosquitoes influence natural Anopheline biting behavior and transmission," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49080-9
    DOI: 10.1038/s41467-024-49080-9
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    References listed on IDEAS

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    1. Kelsey M. Sumner & Elizabeth Freedman & Lucy Abel & Andrew Obala & Brian W. Pence & Amy Wesolowski & Steven R. Meshnick & Wendy Prudhomme-O’Meara & Steve M. Taylor, 2021. "Genotyping cognate Plasmodium falciparum in humans and mosquitoes to estimate onward transmission of asymptomatic infections," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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