A matter of timing: Biting by malaria-infected Anopheles mosquitoes and the use of interventions during the night in rural south-eastern Tanzania

Isaac Haggai Namango; Sarah J Moore; Carly Marshall; Adam Saddler; David Kaftan; Frank Chelestino Tenywa; Noely Makungwa; Alex J Limwagu; Salum Mapua; Olukayode G Odufuwa; Godfrey Ligema; Hassan Ngonyani; Isaya Matanila; Jameel Bharmal; Jason Moore; Marceline Finda; Fredros Okumu; Manuel W Hetzel; Amanda Ross

doi:10.1371/journal.pgph.0003864

A matter of timing: Biting by malaria-infected Anopheles mosquitoes and the use of interventions during the night in rural south-eastern Tanzania

PLOS Glob Public Health. 2024 Dec 31;4(12):e0003864. doi: 10.1371/journal.pgph.0003864. eCollection 2024.

Authors

Isaac Haggai Namango^{1

2}, Sarah J Moore^{1

2

3

4}, Carly Marshall^{3

5}, Adam Saddler^{1

3

6}, David Kaftan^{3

7}, Frank Chelestino Tenywa^{1

2

3}, Noely Makungwa³, Alex J Limwagu⁸, Salum Mapua^{8

9}, Olukayode G Odufuwa^{1

2

3

10}, Godfrey Ligema³, Hassan Ngonyani³, Isaya Matanila³, Jameel Bharmal¹¹, Jason Moore³, Marceline Finda^{8

12}, Fredros Okumu^{4

8

12

13}, Manuel W Hetzel^{1

2}, Amanda Ross^{1

2}

Affiliations

¹ Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Allschwil, Switzerland.
² University of Basel, Basel, Switzerland.
³ Vector Control Product Testing Unit, Ifakara Health Institute, Bagamoyo, Tanzania.
⁴ School of Life Science and Biotechnology, Nelson Mandela African Institute of Science and Technology, Arusha, Tanzania.
⁵ British Columbia Centre for Excellence in HIV/AIDS, British Columbia, Vancouver, Canada.
⁶ Telethon Kids Institute, Perth, Australia.
⁷ New York University Grossman School of Medicine, New York, New York, United States of America.
⁸ Environmental Health and Ecological Sciences Department, Ifakara Health Institute, Ifakara, Tanzania.
⁹ University of Salford, Manchester, United Kingdom.
¹⁰ London School of Hygiene and Tropical Medicine, London, United Kingdom.
¹¹ Innovative Vector Control Consortium, Dar es Salaam, Tanzania.
¹² Faculty of Health Sciences, School of Public Health, University of the Witwatersrand, Johannesburg, South Africa.
¹³ School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Abstract

Knowing when and where infected mosquitoes bite is required for estimating accurate measures of malaria risk, assessing outdoor exposure, and designing intervention strategies. This study combines secondary analyses of a human behaviour survey and an entomological survey carried out in the same area to estimate human exposure to malaria-infected Anopheles mosquitoes throughout the night in rural villages in south-eastern Tanzania. Mosquitoes were collected hourly from 6PM to 6AM indoors and outdoors by human landing catches in 2019, and tested for Plasmodium falciparum sporozoite infections using ELISA. In nearby villages, a trained member in each selected household recorded the whereabouts and activities of the household members from 6PM to 6AM in 2016 and 2017. Vector control use was high: 99% of individuals were reported to use insecticide-treated nets and a recent trial of indoor residual spraying had achieved 80% coverage. The risk of being bitten by infected mosquitoes outdoors, indoors in bed, and indoors but not in bed, and use of mosquito nets was estimated for each hour of the night. Individuals were mainly outdoors before 9PM, and mainly indoors between 10PM and 5AM. The main malaria vectors caught were Anopheles funestus sensu stricto and An. arabiensis. Biting rates were higher in the night compared to the evening or early morning. Due to the high use of ITNs, an estimated 85% (95% CI 81%, 88%) of all exposure in children below school age and 76% (71%, 81%) in older household members could potentially be averted by ITNs under current use patterns. Outdoor exposure accounted for an estimated 11% (8%, 15%) of infective bites in children below school age and 17% (13%, 22%) in older individuals. Maintaining high levels of ITN access, use and effectiveness remains important for reducing malaria transmission in this area. Interventions against outdoor exposure would provide additional protection.

Copyright: © 2024 Namango et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Grants and funding

IHN was supported by a Swiss Government Excellence Scholarship. SJM was supported in part by the generous support of the American people through the United States Agency for International Development (USAID). The “Accelerate to Eliminate Malaria” program is a five-year cooperative agreement funded by the U.S. Agency for International Development under Agreement No. 7200AA23CA000025, beginning October 2023. It is implemented by the Innovative Vector Control Consortium (IVCC). The information provided in this document is not official U.S. Government information and does not necessarily represent the views or positions of the U.S. Agency for International Development.