Evaluation of the interaction between insecticide resistance-associated genes and malaria transmission in Anopheles gambiae sensu lato in central Côte d’Ivoire

Wolie, Rosine Z.; Koffi, Alphonsine A.; Ahoua Alou, Ludovic P.; Sternberg, Eleanore D.; N’Nan-Alla, Oulo; Dahounto, Amal; Yapo, Florent H. A.; Kanh, Kpahe M. H.; Camara, Soromane; Oumbouke, Welbeck A.; Tia, Innocent Z.; Nguetta, Simon-Pierre A.; Thomas, Matthew B.; NGuessan, Raphael

doi:10.1186/s13071-021-05079-5

Cited by 26Malaria Research and ControlInsect Resistance and GeneticsBird parasitology and diseases

Evaluation of the interaction between insecticide resistance-associated genes and malaria transmission in Anopheles gambiae sensu lato in central Côte d’Ivoire

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Wolie, Rosine Z., Koffi, Alphonsine A., Ahoua Alou, Ludovic P., Sternberg, Eleanore D., N’Nan-Alla, Oulo, Dahounto, Amal, Yapo, Florent H. A., Kanh, Kpahe M. H. +6 more·2021·Parasites & Vectors

DOI 10.1186/s13071-021-05079-5PMC PMC8605510

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Abstract

Abstract Background There is evidence that the knockdown resistance gene (Kdr) L1014F and acetylcholinesterase-1 gene (Ace-1R) G119S mutations involved in pyrethroid and carbamate resistance in Anopheles gambiae influence malaria transmission in sub-Saharan Africa. This is likely due to changes in the behaviour, life history and vector competence and capacity of An. gambiae. In the present study, performed as part of a two-arm cluster randomized controlled trial evaluating the impact of household screening plus a novel insecticide delivery system (In2Care Eave Tubes), we investigated the distribution of insecticide target site mutations and their association with infection status in wild An. gambiae sensu lato (s.l.) populations. Methods Mosquitoes were captured in 40 villages around Bouaké by human landing catch from May 2017 to April 2019. Randomly selected samples of An. gambiae s.l. that were infected or not infected with Plasmodium sp. were identified to species and then genotyped for Kdr L1014F and Ace-1R G119S mutations using quantitative polymerase chain reaction assays. The frequencies of the two alleles were compared between Anopheles coluzzii and Anopheles gambiae and then between infected and uninfected groups for each species. Results The presence of An. gambiae (49%) and An. coluzzii (51%) was confirmed in Bouaké. Individuals of both species infected with Plasmodium parasites were found. Over the study period, the average frequency of the Kdr L1014F and Ace-1R G119S mutations did not vary significantly between study arms. However, the frequencies of the Kdr L1014F and Ace-1R G119S resistance alleles were significantly higher in An. gambiae than in An. coluzzii [odds ratio (95% confidence interval): 59.64 (30.81–131.63) for Kdr, and 2.79 (2.17–3.60) for Ace-1R]. For both species, there were no significant differences in Kdr L1014F or Ace-1R G119S genotypic and allelic frequency distributions between infected and uninfected specimens (P > 0.05). Conclusions Either alone or in combination, Kdr L1014F and Ace-1R G119S showed no significant association with Plasmodium infection in wild An. gambiae and An. coluzzii, demonstrating the similar competence of these species for Plasmodium transmission in Bouaké. Additional factors including behavioural and environmental ones that influence vector competence in natural populations, and those other than allele measurements (metabolic resistance factors) that contribute to resistance, should be considered when establishing the existence of a link between insecticide resistance and vector competence. Graphical Abstract

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There was a high frequency of both kdr and ace1R genes in An. gambiae and An. coluzzii, with a higher frequency for An. gambiae.
“Consistent with recent studies carried out in the area of Bouaké [7, 9, 13, 36], there was a high frequency of both kdr and ace1R genes in An. gambiae and An. coluzzii, with a higher frequency for An. gambiae; probably due to selection pressure through the use of insecticide.”
From Entomological indicators of malaria transmission prior to a cluster-randomized controlled trial of a 'lethal house lure' intervention in central Côte d'Ivoire (2022) · cites this paper as [36]
The Results table reports higher frequencies of both resistance alleles in An. gambiae than in An. coluzzii. It supports a high Kdr frequency, but Ace-1R allele frequencies were 6.67–21.07% across the two species and study arms, so describing both genes as highly frequent overstates the finding. The Discussion presents insecticide-driven selection as a possibility, not an established cause. No page number is provided in our copy. (LLM, conf=0.88)
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Additional file 2 of The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics
Sadia, C. G., Bonneville, J., Zoh, M. G., Fodjo, B. K., Kouadio, F.-P. A., Oyou, S. K., Koudou, B. G., Adepo-Gourene, B. A., Reynaud, S., David, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25347274
Additional file 5 of The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics
Sadia, C. G., Bonneville, J., Zoh, M. G., Fodjo, B. K., Kouadio, F.-P. A., Oyou, S. K., Koudou, B. G., Adepo-Gourene, B. A., Reynaud, S., David, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26689430
Additional file 3 of Small-scale field evaluation of PermaNet® Dual (a long-lasting net coated with a mixture of chlorfenapyr and deltamethrin) against pyrethroid-resistant Anopheles gambiae mosquitoes from Tiassalé, Côte d’Ivoire
Zahouli, J. Z. B., Edi, C., Yao, L. A., Lisro, E. G., Adou, M., Koné, I., Small, G. J., Sternberg, E. D., & Koudou, B. G. (2023) · Figshare · doi:10.6084/m9.figshare.22608358
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Additional file 2 of Small-scale field evaluation of PermaNet® Dual (a long-lasting net coated with a mixture of chlorfenapyr and deltamethrin) against pyrethroid-resistant Anopheles gambiae mosquitoes from Tiassalé, Côte d’Ivoire
Zahouli, J. Z. B., Edi, C., Yao, L. A., Lisro, E. G., Adou, M., Koné, I., Small, G. J., Sternberg, E. D., & Koudou, B. G. (2023) · Figshare · doi:10.6084/m9.figshare.22608355
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Additional file 1 of The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics
Sadia, C. G., Bonneville, J., Zoh, M. G., Fodjo, B. K., Kouadio, F.-P. A., Oyou, S. K., Koudou, B. G., Adepo-Gourene, B. A., Reynaud, S., David, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25347052
Additional file 3 of The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics
Sadia, C. G., Bonneville, J., Zoh, M. G., Fodjo, B. K., Kouadio, F.-P. A., Oyou, S. K., Koudou, B. G., Adepo-Gourene, B. A., Reynaud, S., David, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26689424
Additional file 1 of Small-scale field evaluation of PermaNet® Dual (a long-lasting net coated with a mixture of chlorfenapyr and deltamethrin) against pyrethroid-resistant Anopheles gambiae mosquitoes from Tiassalé, Côte d’Ivoire
Zahouli, J. Z. B., Edi, C., Yao, L. A., Lisro, E. G., Adou, M., Koné, I., Small, G. J., Sternberg, E. D., & Koudou, B. G. (2023) · Figshare · doi:10.6084/m9.figshare.22608352
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Additional file 5 of Small-scale field evaluation of PermaNet® Dual (a long-lasting net coated with a mixture of chlorfenapyr and deltamethrin) against pyrethroid-resistant Anopheles gambiae mosquitoes from Tiassalé, Côte d’Ivoire
Zahouli, J. Z. B., Edi, C., Yao, L. A., Lisro, E. G., Adou, M., Koné, I., Small, G. J., Sternberg, E. D., & Koudou, B. G. (2023) · Figshare · doi:10.6084/m9.figshare.22608364
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Additional file 4 of The impact of agrochemical pollutant mixtures on the selection of insecticide resistance in the malaria vector Anopheles gambiae: insights from experimental evolution and transcriptomics
Sadia, C. G., Bonneville, J., Zoh, M. G., Fodjo, B. K., Kouadio, F.-P. A., Oyou, S. K., Koudou, B. G., Adepo-Gourene, B. A., Reynaud, S., David, J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26689427
Additional file 4 of Small-scale field evaluation of PermaNet® Dual (a long-lasting net coated with a mixture of chlorfenapyr and deltamethrin) against pyrethroid-resistant Anopheles gambiae mosquitoes from Tiassalé, Côte d’Ivoire
Zahouli, J. Z. B., Edi, C., Yao, L. A., Lisro, E. G., Adou, M., Koné, I., Small, G. J., Sternberg, E. D., & Koudou, B. G. (2023) · Figshare · doi:10.6084/m9.figshare.22608361
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Wolie, R. Z., Koffi, A. A., Alou, L. P. A., Sternberg, E. D., N’Nan-Alla, O., Dahounto, A., Yapo, F. H. A., Kanh, K. H. M., Camara, S., Oumbouke, W. A., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-637056/v1
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Distribution and Frequency of kdr Mutations within Anopheles gambiae s.l. Populations and First Report of the Ace.1G119S Mutation in Anopheles arabiensis from Burkina Faso (West Africa)
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The current distribution and characterization of the L1014F resistance allele of the kdr gene in three malaria vectors (Anopheles gambiae, Anopheles coluzzii, Anopheles arabiensis) in Benin (West Africa)
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Authors: Wolie, R. Z., Koffi, A. A., Ahoua Alou, L. P., Sternberg, E. D., N’Nan-Alla, O., Dahounto, A., Yapo, F. H. A., Kanh, K. M. H., Camara, S., Oumbouke, W. A., Tia, I. Z., Nguetta, S.-P. A., Thomas, M. B., & NGuessan, R.
Affiliations: Institut National de Santé Publique (CI)
Pennsylvania State University (US)
Université Félix Houphouët-Boigny (CI)
Innovative Vector Control Consortium (GB)
Université Alassane Ouattara (CI)
Corresponding author: Wolie, Rosine Z.
ORCID: Wolie, Rosine Z.
Koffi, Alphonsine A.
Sternberg, Eleanore D.
Oumbouke, Welbeck A.
Thomas, Matthew B.
Venue: Parasites & Vectors
Publisher: Springer Science and Business Media LLC
Published: 2021-11-20
Volume: 14
Issue: 1
Pages: 581-581
ISSN: 1756-3305 (ISSN-L)
DOI: 10.1186/s13071-021-05079-5
PMC: PMC8605510
OpenAlex: W3214926804
Cited by: 24
References: 53
Citations by year: 2026: 4 · 2025: 2 · 2024: 5 · 2023: 9 · 2022: 4
FWCI: 4.33
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Parasites & Vectors (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Greater South Information System
Funders: Bill and Melinda Gates Foundation (OPP1131603)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
Keywords: Anopheles gambiae s.l., Anopheles coluzzii, insecticide resistance, acetylcholinesterase 1, malaria transmission, malaria, vector competence
MeSH terms: Mosquito Vectors, Animals, Anopheles, Insecticide Resistance, Insecticides, Cote d'Ivoire, Malaria, Mosquito Control, Plasmodium, Genes, Insect

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Evaluation of the interaction between insecticide resistance-associated genes and malaria transmission in Anopheles gambiae sensu lato in central Côte d’Ivoire

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