Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from Cameroon

Abstract Background Cameroon is considering the implementation of indoor residual spraying (IRS) as a complementary measure to control malaria in the context of high pyrethroid resistance in major malaria vectors. Non-pyrethroid insecticide classes such as organophosphates and carbamates may be util...

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Main Authors: Achille Jerome Binyang, Emmanuel Elanga-Ndille, Billy Tene-Fossog, Cyrille Ndo, Lynda Nouage, Tatiane Assatse, Yvan Fotso-Toguem, Raymond Tabue, Francis Zeukeng, Daniel Nguete Nguiffo, Josiane Etang, Flobert Njiokou, Charles S. Wondji
Format: Article
Language:English
Published: BMC 2022-02-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-022-05174-1
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author Achille Jerome Binyang
Emmanuel Elanga-Ndille
Billy Tene-Fossog
Cyrille Ndo
Lynda Nouage
Tatiane Assatse
Yvan Fotso-Toguem
Raymond Tabue
Francis Zeukeng
Daniel Nguete Nguiffo
Josiane Etang
Flobert Njiokou
Charles S. Wondji
author_facet Achille Jerome Binyang
Emmanuel Elanga-Ndille
Billy Tene-Fossog
Cyrille Ndo
Lynda Nouage
Tatiane Assatse
Yvan Fotso-Toguem
Raymond Tabue
Francis Zeukeng
Daniel Nguete Nguiffo
Josiane Etang
Flobert Njiokou
Charles S. Wondji
author_sort Achille Jerome Binyang
collection DOAJ
description Abstract Background Cameroon is considering the implementation of indoor residual spraying (IRS) as a complementary measure to control malaria in the context of high pyrethroid resistance in major malaria vectors. Non-pyrethroid insecticide classes such as organophosphates and carbamates may be utilized in IRS due to widespread pyrethroid resistance. However, the success of this strategy depends on good knowledge of the resistance status of malaria vectors to carbamates and organophosphates. Here, we assessed the susceptibility profile of Anopheles gambiae sensu lato with respect to carbamates and organophosphate and the distribution of the molecular mechanism underlying resistance to these insecticides. Methods Anopheles gambiae s.l. mosquitoes were collected from nine settings across the country and bio-assayed with bendiocarb, propoxur and pirimiphos-methyl. The Ace-1 target-site G119S mutation was genotyped using a TaqMan assay. To investigate the polymorphism in the Ace-1 gene, a region of 924 base pairs in a sequence of the gene was amplified from both live and dead females of An. gambiae exposed to bendiocarb. Results Pirimiphos-methyl induced full mortality in An. gambiae s.l. from all study sites, whereas for carbamates, resistance was observed in four localities, with the lowest mortality rate recorded in Mangoum (17.78 ± 5.02% for bendiocarb and 18.61 ± 3.86% for propoxur) in the southern part of Cameroon. Anopheles coluzzii was found to be the predominant species in the northern tropical part of the country where it is sympatric with Anopheles arabiensis. In the localities situated in southern equatorial regions, this species was predominant in urban settings, while An. gambiae was the most abundant species in rural areas. The G119S Ace-1 target-site mutation was detected only in An. gambiae and only in the sites located in southern Cameroon. Phylogenetic analyses showed a clustering according to the phenotype. Conclusion The occurrence of the Ace-1 target-site substitution G119S in An. gambiae s.l. populations highlights the challenge associated with the impending deployment of IRS in Cameroon using carbamates or organophosphates. It is therefore important to think about a resistance management plan including the use of other insecticide classes such as neonicotinoids or pyrrole to guarantee the implementation of IRS in Cameroon. Graphical Abstract
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spelling doaj.art-fd9281efc5b543f6800982bf1349bddf2022-12-21T17:23:38ZengBMCParasites & Vectors1756-33052022-02-0115111310.1186/s13071-022-05174-1Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from CameroonAchille Jerome Binyang0Emmanuel Elanga-Ndille1Billy Tene-Fossog2Cyrille Ndo3Lynda Nouage4Tatiane Assatse5Yvan Fotso-Toguem6Raymond Tabue7Francis Zeukeng8Daniel Nguete Nguiffo9Josiane Etang10Flobert Njiokou11Charles S. Wondji12Department of Medical Entomology, Centre for Research in Infectious Diseases (CRID)Department of Medical Entomology, Centre for Research in Infectious Diseases (CRID)Department of Medical Entomology, Centre for Research in Infectious Diseases (CRID)Department of Parasitology and Microbiology, Centre for Research in Infectious Diseases (CRID)Department of Medical Entomology, Centre for Research in Infectious Diseases (CRID)Department of Medical Entomology, Centre for Research in Infectious Diseases (CRID)Department of Medical Entomology, Centre for Research in Infectious Diseases (CRID)Ministry of Public Health, National Malaria Control ProgrammeNational Reference Unit for Vector Control, The Biotechnology Centre, University of Yaoundé IDepartment of Parasitology and Microbiology, Centre for Research in Infectious Diseases (CRID)Department of Biological Science, Faculty of Medicine and Pharmaceutical Sciences, University of DoualaDepartment of Animal Biology and Physiology, Faculty of Science, University of Yaoundé 1Department of Medical Entomology, Centre for Research in Infectious Diseases (CRID)Abstract Background Cameroon is considering the implementation of indoor residual spraying (IRS) as a complementary measure to control malaria in the context of high pyrethroid resistance in major malaria vectors. Non-pyrethroid insecticide classes such as organophosphates and carbamates may be utilized in IRS due to widespread pyrethroid resistance. However, the success of this strategy depends on good knowledge of the resistance status of malaria vectors to carbamates and organophosphates. Here, we assessed the susceptibility profile of Anopheles gambiae sensu lato with respect to carbamates and organophosphate and the distribution of the molecular mechanism underlying resistance to these insecticides. Methods Anopheles gambiae s.l. mosquitoes were collected from nine settings across the country and bio-assayed with bendiocarb, propoxur and pirimiphos-methyl. The Ace-1 target-site G119S mutation was genotyped using a TaqMan assay. To investigate the polymorphism in the Ace-1 gene, a region of 924 base pairs in a sequence of the gene was amplified from both live and dead females of An. gambiae exposed to bendiocarb. Results Pirimiphos-methyl induced full mortality in An. gambiae s.l. from all study sites, whereas for carbamates, resistance was observed in four localities, with the lowest mortality rate recorded in Mangoum (17.78 ± 5.02% for bendiocarb and 18.61 ± 3.86% for propoxur) in the southern part of Cameroon. Anopheles coluzzii was found to be the predominant species in the northern tropical part of the country where it is sympatric with Anopheles arabiensis. In the localities situated in southern equatorial regions, this species was predominant in urban settings, while An. gambiae was the most abundant species in rural areas. The G119S Ace-1 target-site mutation was detected only in An. gambiae and only in the sites located in southern Cameroon. Phylogenetic analyses showed a clustering according to the phenotype. Conclusion The occurrence of the Ace-1 target-site substitution G119S in An. gambiae s.l. populations highlights the challenge associated with the impending deployment of IRS in Cameroon using carbamates or organophosphates. It is therefore important to think about a resistance management plan including the use of other insecticide classes such as neonicotinoids or pyrrole to guarantee the implementation of IRS in Cameroon. Graphical Abstracthttps://doi.org/10.1186/s13071-022-05174-1Ace-1 G119S mutationInsecticide resistanceAn. gambiae s.l.Cameroon
spellingShingle Achille Jerome Binyang
Emmanuel Elanga-Ndille
Billy Tene-Fossog
Cyrille Ndo
Lynda Nouage
Tatiane Assatse
Yvan Fotso-Toguem
Raymond Tabue
Francis Zeukeng
Daniel Nguete Nguiffo
Josiane Etang
Flobert Njiokou
Charles S. Wondji
Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from Cameroon
Parasites & Vectors
Ace-1 G119S mutation
Insecticide resistance
An. gambiae s.l.
Cameroon
title Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from Cameroon
title_full Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from Cameroon
title_fullStr Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from Cameroon
title_full_unstemmed Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from Cameroon
title_short Distribution of acetylcholinesterase (Ace-1 R ) target-site G119S mutation and resistance to carbamates and organophosphates in Anopheles gambiae sensu lato populations from Cameroon
title_sort distribution of acetylcholinesterase ace 1 r target site g119s mutation and resistance to carbamates and organophosphates in anopheles gambiae sensu lato populations from cameroon
topic Ace-1 G119S mutation
Insecticide resistance
An. gambiae s.l.
Cameroon
url https://doi.org/10.1186/s13071-022-05174-1
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