The frequency of kdr and ace-1 alleles in Anopheles gambiae s.l. before and during indoor residual spraying (IRS) implementation and four years after IRS withdrawal in three districts in Atacora, Benin.

Anopheles gambiae Benin Genetic structure IRS withdrawal Resistance

Journal

Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774

Informations de publication

Date de publication:
07 Mar 2024
Historique:
received: 29 09 2023
accepted: 18 02 2024
medline: 8 3 2024
pubmed: 8 3 2024
entrez: 8 3 2024
Statut: epublish

Résumé

Indoor residual spraying (IRS) was first implemented in the Atacora department, Benin from 2011 to 2012 using bendiocarb (carbamate) followed by annual spraying with pirimiphos-methyl (organophosphate) from 2013 to 2018. Before and after IRS implementation in Atacora, standard pyrethroid insecticide-treated bed nets were the main method of vector control in the area. This study investigated the knockdown resistance (kdr) gene (L1014F) and the acetylcholinesterase (ace-1) gene (G119S), before and during IRS implementation, and 4-years after IRS withdrawal from Atacora. This was done to assess how changes in insecticide pressure from indoor residual spraying may have altered the genotypic resistance profile of Anopheles gambiae s.l. Identification of sibling species of An. gambiae s.l. and detection of the L1014F mutation in the kdr gene and G119S mutation in ace-1 genes was done using molecular analysis. Allelic and genotypic frequencies were calculated and compared with each other before and during IRS implementation and 4 years after IRS withdrawal. The Hardy-Weinberg equilibrium and genetic differentiation within and between populations were assessed. Prevalence of the L1014F mutation in all geographic An. gambiae s.l. (An. gambiae s.s., Anopheles. coluzzii, Anopheles. arabiensis, and hybrids of "An. gambiae s.s. and An. coluzzii") populations increased from 69% before IRS to 87% and 90% during and after IRS. The G119S allele frequency during IRS (20%) was significantly higher than before IRS implementation (2%). Four years after IRS withdrawal, allele frequencies returned to similar levels as before IRS (3%). Four years after IRS withdrawal, the populations showed excess heterozygosity at the ace-1 gene and deficit heterozygosity at the kdr gene, whereas both genes had excess heterozygosity before and during IRS (F This study shows that the withdrawal of IRS with bendiocarb and pirimiphos-methyl may have slowed down the selection of individual mosquitoes with ace-1 resistance alleles in contrast to populations of An. gambiae s.l. with the L1014F resistance allele of the kdr gene. This may suggest that withdrawing the use of carbamates or organophosphates from IRS or rotating alternative insecticides with different modes of action may slow the development of ace-1 insecticide-resistance mutations. The increase in the prevalence of the L1014F mutation of the kdr gene in the population, despite the cessation of IRS, could be explained by the growing use of pyrethroids and DDT in agriculture and for other domestic use. More observational studies in countries where carbamates or organophosphates are still being used as public health insecticides may provide additional insights into these associations.

Sections du résumé

BACKGROUND BACKGROUND
Indoor residual spraying (IRS) was first implemented in the Atacora department, Benin from 2011 to 2012 using bendiocarb (carbamate) followed by annual spraying with pirimiphos-methyl (organophosphate) from 2013 to 2018. Before and after IRS implementation in Atacora, standard pyrethroid insecticide-treated bed nets were the main method of vector control in the area. This study investigated the knockdown resistance (kdr) gene (L1014F) and the acetylcholinesterase (ace-1) gene (G119S), before and during IRS implementation, and 4-years after IRS withdrawal from Atacora. This was done to assess how changes in insecticide pressure from indoor residual spraying may have altered the genotypic resistance profile of Anopheles gambiae s.l.
METHOD METHODS
Identification of sibling species of An. gambiae s.l. and detection of the L1014F mutation in the kdr gene and G119S mutation in ace-1 genes was done using molecular analysis. Allelic and genotypic frequencies were calculated and compared with each other before and during IRS implementation and 4 years after IRS withdrawal. The Hardy-Weinberg equilibrium and genetic differentiation within and between populations were assessed.
RESULTS RESULTS
Prevalence of the L1014F mutation in all geographic An. gambiae s.l. (An. gambiae s.s., Anopheles. coluzzii, Anopheles. arabiensis, and hybrids of "An. gambiae s.s. and An. coluzzii") populations increased from 69% before IRS to 87% and 90% during and after IRS. The G119S allele frequency during IRS (20%) was significantly higher than before IRS implementation (2%). Four years after IRS withdrawal, allele frequencies returned to similar levels as before IRS (3%). Four years after IRS withdrawal, the populations showed excess heterozygosity at the ace-1 gene and deficit heterozygosity at the kdr gene, whereas both genes had excess heterozygosity before and during IRS (F
CONCLUSIONS CONCLUSIONS
This study shows that the withdrawal of IRS with bendiocarb and pirimiphos-methyl may have slowed down the selection of individual mosquitoes with ace-1 resistance alleles in contrast to populations of An. gambiae s.l. with the L1014F resistance allele of the kdr gene. This may suggest that withdrawing the use of carbamates or organophosphates from IRS or rotating alternative insecticides with different modes of action may slow the development of ace-1 insecticide-resistance mutations. The increase in the prevalence of the L1014F mutation of the kdr gene in the population, despite the cessation of IRS, could be explained by the growing use of pyrethroids and DDT in agriculture and for other domestic use. More observational studies in countries where carbamates or organophosphates are still being used as public health insecticides may provide additional insights into these associations.

Identifiants

pubmed: 38454494
doi: 10.1186/s13071-024-06206-8
pii: 10.1186/s13071-024-06206-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

115

Informations de copyright

© 2024. The Author(s).

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Auteurs

Esdras Mahoutin Odjo (EM)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin. esdrasmahoutino@gmail.com.
Faculté des Sciences et Techniques-Université d'Abomey-Calavi, Abomey Calavi, Bénin. esdrasmahoutino@gmail.com.

Daniel Impoinvil (D)

U.S. President's Malaria Initiative (PMI), U.S. Centers for Disease Control and Prevention, Atlanta, GA, USA.

Arsène Jacques Y H Fassinou (AJYH)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.

Gil Germain Padonou (GG)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.
Faculté des Sciences et Techniques-Université d'Abomey-Calavi, Abomey Calavi, Bénin.

Rock Aïkpon (R)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.
Ecole Normale Supérieure de Natitingou, Université Nationale des Sciences, Technologies, Ingénierie et Mathématiques (UNSTIM) d'Abomey, Abomey, Bénin.

Albert Sourou Salako (AS)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.

André Aimé Sominahouin (AA)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.

Constantin Adoha (C)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.
Faculté des Sciences et Techniques-Université d'Abomey-Calavi, Abomey Calavi, Bénin.

Boulais Yovogan (B)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.
Faculté des Sciences et Techniques-Université d'Abomey-Calavi, Abomey Calavi, Bénin.

Razaki Osse (R)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.
Université Nationale d'Agriculture de Porto-Novo, Porto-Novo, Bénin.

Olivier Oussou (O)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.

Filémon Tokponnon (F)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.

Virgile Gnanguénon (V)

US President's Malaria Initiative (PMI), U.S. Agency for International Development (USAID), Cotonou, Benin.

Ahmed Saadani Hassani (AS)

US President's Malaria Initiative (PMI), U.S. Centers for Disease Control and Prevention (CDC), Cotonou, Benin.

Martin C Akogbeto (MC)

Centre de Recherche Entomologique de Cotonou, Cotonou, Bénin.

Classifications MeSH