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Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso

BACKGROUND: Recent outbreaks of dengue and other Aedes aegypti-borne arboviruses highlight the importance of a rapid response for effective vector control. Data on insecticide resistance and underlying mechanisms are essential for outbreak preparedness, but are sparse in much of Africa. We investiga...

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Autores principales: Badolo, Athanase, Sombié, Aboubacar, Pignatelli, Patricia M., Sanon, Aboubakar, Yaméogo, Félix, Wangrawa, Dimitri W., Sanon, Antoine, Kanuka, Hirotaka, McCall, Philip J., Weetman, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6550433/
https://www.ncbi.nlm.nih.gov/pubmed/31120874
http://dx.doi.org/10.1371/journal.pntd.0007439
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author Badolo, Athanase
Sombié, Aboubacar
Pignatelli, Patricia M.
Sanon, Aboubakar
Yaméogo, Félix
Wangrawa, Dimitri W.
Sanon, Antoine
Kanuka, Hirotaka
McCall, Philip J.
Weetman, David
author_facet Badolo, Athanase
Sombié, Aboubacar
Pignatelli, Patricia M.
Sanon, Aboubakar
Yaméogo, Félix
Wangrawa, Dimitri W.
Sanon, Antoine
Kanuka, Hirotaka
McCall, Philip J.
Weetman, David
author_sort Badolo, Athanase
collection PubMed
description BACKGROUND: Recent outbreaks of dengue and other Aedes aegypti-borne arboviruses highlight the importance of a rapid response for effective vector control. Data on insecticide resistance and underlying mechanisms are essential for outbreak preparedness, but are sparse in much of Africa. We investigated the levels and heterogeneity of insecticide resistance and mechanisms of Ae. aegypti from contrasting settings within and around Ouagadougou, Burkina Faso. METHODOLOGY/PRINCIPAL FINDINGS: Bioassays were performed on larvae and adults to diagnose prevalence of resistance, and to assess levels where resistance was detected. Investigation of resistance mechanisms was performed using synergist bioassays, knockdown resistance (kdr) target site mutation genotyping and quantitative PCR expression analysis of candidate P450 genes. Larval dose-response assays indicated susceptibility to the organophosphates tested. Adult females were also susceptible to organophosphates, but resistance to carbamates was suspected in urban and semi-urban localities. Females from all localities showed resistance to pyrethroids but resistance prevalence and level were higher in urban and especially in semi-urban areas, compared to the rural population. Environment was also associated with susceptibility: adults reared from larvae collected in tires from the semi-urban site were significantly less resistant to pyrethroids than those collected from large outdoor drinking water containers (‘drums’). Susceptibility to both pyrethroids tested was largely restored by pre-exposure to Piperonyl Butoxide (PBO), suggesting a strong metabolic basis to resistance. The 1534C kdr mutation was nearly fixed in semi-urban and urban areas but was far less common in the rural area, where the 1016I kdr mutation frequency was also significantly lower. P450 gene analysis detected limited over-expression of single candidates but significantly elevated average expression in the semi-urban site compared to both a susceptible laboratory colony, and females from the other collection sites. CONCLUSIONS/SIGNIFICANCE: Our results reveal pyrethroid resistance and paired kdr mutations in both urban and semi-urban sites at levels that are unprecedented for mainland Africa. The combination of target site and metabolic mechanisms is common in Ae. aegypti populations from other continents but is a worrying finding for African populations. However, organophosphate insecticides are still active against both larvae and adults of Ae. aegypti, providing useful insecticidal options for control and resistance management.
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spelling pubmed-65504332019-06-17 Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso Badolo, Athanase Sombié, Aboubacar Pignatelli, Patricia M. Sanon, Aboubakar Yaméogo, Félix Wangrawa, Dimitri W. Sanon, Antoine Kanuka, Hirotaka McCall, Philip J. Weetman, David PLoS Negl Trop Dis Research Article BACKGROUND: Recent outbreaks of dengue and other Aedes aegypti-borne arboviruses highlight the importance of a rapid response for effective vector control. Data on insecticide resistance and underlying mechanisms are essential for outbreak preparedness, but are sparse in much of Africa. We investigated the levels and heterogeneity of insecticide resistance and mechanisms of Ae. aegypti from contrasting settings within and around Ouagadougou, Burkina Faso. METHODOLOGY/PRINCIPAL FINDINGS: Bioassays were performed on larvae and adults to diagnose prevalence of resistance, and to assess levels where resistance was detected. Investigation of resistance mechanisms was performed using synergist bioassays, knockdown resistance (kdr) target site mutation genotyping and quantitative PCR expression analysis of candidate P450 genes. Larval dose-response assays indicated susceptibility to the organophosphates tested. Adult females were also susceptible to organophosphates, but resistance to carbamates was suspected in urban and semi-urban localities. Females from all localities showed resistance to pyrethroids but resistance prevalence and level were higher in urban and especially in semi-urban areas, compared to the rural population. Environment was also associated with susceptibility: adults reared from larvae collected in tires from the semi-urban site were significantly less resistant to pyrethroids than those collected from large outdoor drinking water containers (‘drums’). Susceptibility to both pyrethroids tested was largely restored by pre-exposure to Piperonyl Butoxide (PBO), suggesting a strong metabolic basis to resistance. The 1534C kdr mutation was nearly fixed in semi-urban and urban areas but was far less common in the rural area, where the 1016I kdr mutation frequency was also significantly lower. P450 gene analysis detected limited over-expression of single candidates but significantly elevated average expression in the semi-urban site compared to both a susceptible laboratory colony, and females from the other collection sites. CONCLUSIONS/SIGNIFICANCE: Our results reveal pyrethroid resistance and paired kdr mutations in both urban and semi-urban sites at levels that are unprecedented for mainland Africa. The combination of target site and metabolic mechanisms is common in Ae. aegypti populations from other continents but is a worrying finding for African populations. However, organophosphate insecticides are still active against both larvae and adults of Ae. aegypti, providing useful insecticidal options for control and resistance management. Public Library of Science 2019-05-23 /pmc/articles/PMC6550433/ /pubmed/31120874 http://dx.doi.org/10.1371/journal.pntd.0007439 Text en © 2019 Badolo et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Badolo, Athanase
Sombié, Aboubacar
Pignatelli, Patricia M.
Sanon, Aboubakar
Yaméogo, Félix
Wangrawa, Dimitri W.
Sanon, Antoine
Kanuka, Hirotaka
McCall, Philip J.
Weetman, David
Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso
title Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso
title_full Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso
title_fullStr Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso
title_full_unstemmed Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso
title_short Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso
title_sort insecticide resistance levels and mechanisms in aedes aegypti populations in and around ouagadougou, burkina faso
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6550433/
https://www.ncbi.nlm.nih.gov/pubmed/31120874
http://dx.doi.org/10.1371/journal.pntd.0007439
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