Species composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’Ivoire

Abstract Background Knowing the species composition and insecticide resistance status of the target vector population is important to guide malaria vector control. The aim of this study was to characterize the malaria vector population in terms of species composition, insecticide susceptibility stat...

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Main Authors: Bédjou P. N’Dri, Nadja C. Wipf, Jasmina Saric, Behi K. Fodjo, Giovanna Raso, Jürg Utzinger, Pie Müller, Chouaïbou S. Mouhamadou
Format: Article
Language:English
Published: BMC 2023-03-01
Series:Malaria Journal
Subjects:
Online Access:https://doi.org/10.1186/s12936-023-04456-y
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author Bédjou P. N’Dri
Nadja C. Wipf
Jasmina Saric
Behi K. Fodjo
Giovanna Raso
Jürg Utzinger
Pie Müller
Chouaïbou S. Mouhamadou
author_facet Bédjou P. N’Dri
Nadja C. Wipf
Jasmina Saric
Behi K. Fodjo
Giovanna Raso
Jürg Utzinger
Pie Müller
Chouaïbou S. Mouhamadou
author_sort Bédjou P. N’Dri
collection DOAJ
description Abstract Background Knowing the species composition and insecticide resistance status of the target vector population is important to guide malaria vector control. The aim of this study was to characterize the malaria vector population in terms of species composition, insecticide susceptibility status and potential underlying resistance mechanisms in Ellibou, southern Côte d’Ivoire. Methods A 1-year longitudinal entomological survey was conducted using light traps and pyrethroid spray catches to sample adult mosquitoes in combination with larval sampling. The susceptibility status of Anopheles gambiae sensu lato (s.l.) to bendiocarb, deltamethrin, DDT and malathion was assessed using the World Health Organization insecticide susceptibility test. Additionally, An. gambiae specimens were screened for knockdown (kdr) and acetylcholineesterase (ace1) target site resistance alleles, and the expression levels of eight metabolic resistance genes, including seven cytochrome P450 monooxygenases (P450s) and one glutathione S-transferase (GST), measured with reverse transcription quantitative real-time polymerase chain reaction (qPCR). Results Overall, 2383 adult mosquitoes from 12 different taxa were collected with Culex quinquefasciatus and An. gambiae being the predominant taxa. Molecular identification of An. gambiae s.l. revealed the presence of Anopheles arabiensis, Anopheles coluzzii, An. gambiae sensu stricto (s.s.) and Anopheles coluzzii/An. gambiae s.s. hybrids. Anopheles gambiae mosquitoes were resistant to all insecticides except malathion. PCR diagnostics revealed the presence of ace1-G280S and the kdr L995F, L995S and N1570Y target-site mutations. Additionally, several genes were upregulated, including five P450s (i.e., CYP6P3, CYP6M2, CYP9K1, CYP6Z1, CYP6P1) and GSTE2. Conclusion This is the first documented presence of An. arabiensis in Côte d’Ivoire. Its detection – together with a recent finding further north of the country – confirms its existence in the country, which is an early warning sign, as An. arabiensis shows a different biology than the currently documented malaria vectors. Because the local An. gambiae population was still susceptible to malathion, upregulation of P450s, conferring insecticide resistance to pyrethroids, together with the presence of ace1, suggest negative cross-resistance. Therefore, organophosphates could be an alternative insecticide class for indoor residual spraying in the Ellibou area, while additional tools against the outdoor biting An. arabiensis will have to be considered.
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spelling doaj.art-7cbc9dd645424800ba8c435ece520ab62023-03-22T10:29:04ZengBMCMalaria Journal1475-28752023-03-0122111310.1186/s12936-023-04456-ySpecies composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’IvoireBédjou P. N’Dri0Nadja C. Wipf1Jasmina Saric2Behi K. Fodjo3Giovanna Raso4Jürg Utzinger5Pie Müller6Chouaïbou S. Mouhamadou7Centre Suisse de Recherches Scientifiques en Côte d’IvoireSwiss Tropical and Public Health InstituteSwiss Tropical and Public Health InstituteCentre Suisse de Recherches Scientifiques en Côte d’IvoireSwiss Tropical and Public Health InstituteSwiss Tropical and Public Health InstituteSwiss Tropical and Public Health InstituteCentre Suisse de Recherches Scientifiques en Côte d’IvoireAbstract Background Knowing the species composition and insecticide resistance status of the target vector population is important to guide malaria vector control. The aim of this study was to characterize the malaria vector population in terms of species composition, insecticide susceptibility status and potential underlying resistance mechanisms in Ellibou, southern Côte d’Ivoire. Methods A 1-year longitudinal entomological survey was conducted using light traps and pyrethroid spray catches to sample adult mosquitoes in combination with larval sampling. The susceptibility status of Anopheles gambiae sensu lato (s.l.) to bendiocarb, deltamethrin, DDT and malathion was assessed using the World Health Organization insecticide susceptibility test. Additionally, An. gambiae specimens were screened for knockdown (kdr) and acetylcholineesterase (ace1) target site resistance alleles, and the expression levels of eight metabolic resistance genes, including seven cytochrome P450 monooxygenases (P450s) and one glutathione S-transferase (GST), measured with reverse transcription quantitative real-time polymerase chain reaction (qPCR). Results Overall, 2383 adult mosquitoes from 12 different taxa were collected with Culex quinquefasciatus and An. gambiae being the predominant taxa. Molecular identification of An. gambiae s.l. revealed the presence of Anopheles arabiensis, Anopheles coluzzii, An. gambiae sensu stricto (s.s.) and Anopheles coluzzii/An. gambiae s.s. hybrids. Anopheles gambiae mosquitoes were resistant to all insecticides except malathion. PCR diagnostics revealed the presence of ace1-G280S and the kdr L995F, L995S and N1570Y target-site mutations. Additionally, several genes were upregulated, including five P450s (i.e., CYP6P3, CYP6M2, CYP9K1, CYP6Z1, CYP6P1) and GSTE2. Conclusion This is the first documented presence of An. arabiensis in Côte d’Ivoire. Its detection – together with a recent finding further north of the country – confirms its existence in the country, which is an early warning sign, as An. arabiensis shows a different biology than the currently documented malaria vectors. Because the local An. gambiae population was still susceptible to malathion, upregulation of P450s, conferring insecticide resistance to pyrethroids, together with the presence of ace1, suggest negative cross-resistance. Therefore, organophosphates could be an alternative insecticide class for indoor residual spraying in the Ellibou area, while additional tools against the outdoor biting An. arabiensis will have to be considered.https://doi.org/10.1186/s12936-023-04456-yAnopheles arabiensisAnopheles gambiaeCôte d’IvoireInsecticide resistanceMetabolic resistanceMalaria
spellingShingle Bédjou P. N’Dri
Nadja C. Wipf
Jasmina Saric
Behi K. Fodjo
Giovanna Raso
Jürg Utzinger
Pie Müller
Chouaïbou S. Mouhamadou
Species composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’Ivoire
Malaria Journal
Anopheles arabiensis
Anopheles gambiae
Côte d’Ivoire
Insecticide resistance
Metabolic resistance
Malaria
title Species composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’Ivoire
title_full Species composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’Ivoire
title_fullStr Species composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’Ivoire
title_full_unstemmed Species composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’Ivoire
title_short Species composition and insecticide resistance in malaria vectors in Ellibou, southern Côte d’Ivoire and first finding of Anopheles arabiensis in Côte d’Ivoire
title_sort species composition and insecticide resistance in malaria vectors in ellibou southern cote d ivoire and first finding of anopheles arabiensis in cote d ivoire
topic Anopheles arabiensis
Anopheles gambiae
Côte d’Ivoire
Insecticide resistance
Metabolic resistance
Malaria
url https://doi.org/10.1186/s12936-023-04456-y
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