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The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage

BACKGROUND: Mosquito and human behaviour interaction is a key determinant of the maximum level of protection against malaria that can be provided by insecticide-treated nets (ITNs). Nevertheless, scant literature focuses on this interaction, overlooking a fundamental factor for efficient malaria con...

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Autores principales: Perugini, Eleonora, Guelbeogo, Wamdaogo M., Guglielmo, Federica, Poggi, Cristiana, Gabrieli, Eugenio, Ranson, Hilary, della Torre, Alessandra, Pombi, Marco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10015820/
https://www.ncbi.nlm.nih.gov/pubmed/36922855
http://dx.doi.org/10.1186/s13071-023-05710-7
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author Perugini, Eleonora
Guelbeogo, Wamdaogo M.
Guglielmo, Federica
Poggi, Cristiana
Gabrieli, Eugenio
Ranson, Hilary
della Torre, Alessandra
Pombi, Marco
author_facet Perugini, Eleonora
Guelbeogo, Wamdaogo M.
Guglielmo, Federica
Poggi, Cristiana
Gabrieli, Eugenio
Ranson, Hilary
della Torre, Alessandra
Pombi, Marco
author_sort Perugini, Eleonora
collection PubMed
description BACKGROUND: Mosquito and human behaviour interaction is a key determinant of the maximum level of protection against malaria that can be provided by insecticide-treated nets (ITNs). Nevertheless, scant literature focuses on this interaction, overlooking a fundamental factor for efficient malaria control. This study aims to estimate malaria transmission risk in a Burkina Faso village by integrating vector biting rhythms with some key information about human habits. METHODS: Indoor/outdoor human landing catches were conducted for 16 h (16:00–08:00) during 8 nights (September 2020) in Goden village. A survey about net usage and sleeping patterns was submitted to half the households (October–December 2020). A subsample of collected specimens of Anopheles gambiae sensu lato was molecularly processed for species identification, Plasmodium detection from heads-thoraxes and L1014F pyrethroid-resistance allele genotyping. Hourly mosquito abundance was statistically assessed by GLM/GAM, and the entomological inoculation rate (EIR) was corrected for the actual ITN usage retrieved from the questionnaire. RESULTS: Malaria transmission was mainly driven by Anopheles coluzzii (68.7%) followed by A. arabiensis (26.2%). The overall sporozoite rate was 2% with L1014F estimated frequency of 0.68 (N = 1070 out of 15,201 A. gambiae s.l. collected). No major shift in mosquito biting rhythms in response to ITN or differences between indoor and outdoor catches were detected. Impressive high biting pressure (mean 30.3 mosquitoes/person/hour) was exerted from 20:00 to 06:00 with a peak at 4:00. Human survey revealed that nearly all inhabitants were awake before 20:00 and after 7:00 and at least 8.7% had no access to bednets. Adjusting for anthropological data, the EIR dropped from 6.7 to 1.2 infective bites/person/16 h. In a scenario of full net coverage and accounting only for the human sleeping patterns, the daily malaria transmission risk not targetable by ITNs was 0.69 infective bites. CONCLUSIONS: The high mosquito densities and interplay between human/vector activities means that an estimated 10% of residual malaria transmission cannot be prevented by ITNs in the village. Locally tailored studies, like the current one, are essential to explore the heterogeneity of human exposure to infective bites and, consequently, to instruct the adoption of new vector control tools strengthening individual and community protection. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05710-7.
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spelling pubmed-100158202023-03-16 The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage Perugini, Eleonora Guelbeogo, Wamdaogo M. Guglielmo, Federica Poggi, Cristiana Gabrieli, Eugenio Ranson, Hilary della Torre, Alessandra Pombi, Marco Parasit Vectors Research BACKGROUND: Mosquito and human behaviour interaction is a key determinant of the maximum level of protection against malaria that can be provided by insecticide-treated nets (ITNs). Nevertheless, scant literature focuses on this interaction, overlooking a fundamental factor for efficient malaria control. This study aims to estimate malaria transmission risk in a Burkina Faso village by integrating vector biting rhythms with some key information about human habits. METHODS: Indoor/outdoor human landing catches were conducted for 16 h (16:00–08:00) during 8 nights (September 2020) in Goden village. A survey about net usage and sleeping patterns was submitted to half the households (October–December 2020). A subsample of collected specimens of Anopheles gambiae sensu lato was molecularly processed for species identification, Plasmodium detection from heads-thoraxes and L1014F pyrethroid-resistance allele genotyping. Hourly mosquito abundance was statistically assessed by GLM/GAM, and the entomological inoculation rate (EIR) was corrected for the actual ITN usage retrieved from the questionnaire. RESULTS: Malaria transmission was mainly driven by Anopheles coluzzii (68.7%) followed by A. arabiensis (26.2%). The overall sporozoite rate was 2% with L1014F estimated frequency of 0.68 (N = 1070 out of 15,201 A. gambiae s.l. collected). No major shift in mosquito biting rhythms in response to ITN or differences between indoor and outdoor catches were detected. Impressive high biting pressure (mean 30.3 mosquitoes/person/hour) was exerted from 20:00 to 06:00 with a peak at 4:00. Human survey revealed that nearly all inhabitants were awake before 20:00 and after 7:00 and at least 8.7% had no access to bednets. Adjusting for anthropological data, the EIR dropped from 6.7 to 1.2 infective bites/person/16 h. In a scenario of full net coverage and accounting only for the human sleeping patterns, the daily malaria transmission risk not targetable by ITNs was 0.69 infective bites. CONCLUSIONS: The high mosquito densities and interplay between human/vector activities means that an estimated 10% of residual malaria transmission cannot be prevented by ITNs in the village. Locally tailored studies, like the current one, are essential to explore the heterogeneity of human exposure to infective bites and, consequently, to instruct the adoption of new vector control tools strengthening individual and community protection. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05710-7. BioMed Central 2023-03-15 /pmc/articles/PMC10015820/ /pubmed/36922855 http://dx.doi.org/10.1186/s13071-023-05710-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Perugini, Eleonora
Guelbeogo, Wamdaogo M.
Guglielmo, Federica
Poggi, Cristiana
Gabrieli, Eugenio
Ranson, Hilary
della Torre, Alessandra
Pombi, Marco
The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage
title The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage
title_full The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage
title_fullStr The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage
title_full_unstemmed The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage
title_short The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage
title_sort interplay between malaria vectors and human activity accounts for high residual malaria transmission in a burkina faso village with universal itn coverage
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10015820/
https://www.ncbi.nlm.nih.gov/pubmed/36922855
http://dx.doi.org/10.1186/s13071-023-05710-7
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