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 investigat...

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Main Authors: Athanase Badolo, Aboubacar Sombié, Patricia M Pignatelli, Aboubakar Sanon, Félix Yaméogo, Dimitri W Wangrawa, Antoine Sanon, Hirotaka Kanuka, Philip J McCall, David Weetman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-05-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0007439
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author Athanase Badolo
Aboubacar Sombié
Patricia M Pignatelli
Aboubakar Sanon
Félix Yaméogo
Dimitri W Wangrawa
Antoine Sanon
Hirotaka Kanuka
Philip J McCall
David Weetman
author_facet Athanase Badolo
Aboubacar Sombié
Patricia M Pignatelli
Aboubakar Sanon
Félix Yaméogo
Dimitri W Wangrawa
Antoine Sanon
Hirotaka Kanuka
Philip J McCall
David Weetman
author_sort Athanase Badolo
collection DOAJ
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 doaj.art-57eded53fbb345979d691d4c031e32ad2022-12-21T23:10:14ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352019-05-01135e000743910.1371/journal.pntd.0007439Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso.Athanase BadoloAboubacar SombiéPatricia M PignatelliAboubakar SanonFélix YaméogoDimitri W WangrawaAntoine SanonHirotaka KanukaPhilip J McCallDavid WeetmanBACKGROUND: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.https://doi.org/10.1371/journal.pntd.0007439
spellingShingle Athanase Badolo
Aboubacar Sombié
Patricia M Pignatelli
Aboubakar Sanon
Félix Yaméogo
Dimitri W Wangrawa
Antoine Sanon
Hirotaka Kanuka
Philip J McCall
David Weetman
Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso.
PLoS Neglected Tropical Diseases
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
url https://doi.org/10.1371/journal.pntd.0007439
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