CoChat
Sign Up
Cited by 7Malaria Research and ControlInsect Resistance and GeneticsDengue and Mosquito Control Research

The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.

Can neonicotinoid and pyrrole insecticides manage malaria vector resistance in high pyrethroid resistance areas in Côte d'Ivoire?

Open access
Ekra, Armand K., Edi, Constant A. V., Gbalegba, Guy Constant N., Zahouli, Julien Z. B., Danho, Mathias, Koudou, Benjamin G.·2024·Malaria Journal
DOI 10.1186/s12936-024-04917-yPMC PMC11112771

Published version of a preprint

Open this paper in CoChat — free account

Abstract

BACKGROUND: Anopheles mosquito resistance to insecticide remains a serious threat to malaria vector control affecting several sub-Sahara African countries, including Côte d'Ivoire, where high pyrethroid, carbamate and organophosphate resistance have been reported. Since 2017, new insecticides, namely neonicotinoids (e.g.; clothianidin) and pyrroles (e.g.; chlorfenapyr) have been pre-qualified by the World Health Organization (WHO) for use in public health to manage insecticide resistance for disease vector control. METHODS: Clothianidin and chlorfenapyr were tested against the field-collected Anopheles gambiae populations from Gagnoa, Daloa and Abengourou using the WHO standard insecticide susceptibility biossays. Anopheles gambiae larvae were collected from several larval habitats, pooled and reared to adulthood in each site in July 2020. Non-blood-fed adult female mosquitoes aged 2 to 5 days were exposed to diagnostic concentration deltamethrin, permethrin, alpha-cypermethrin, bendiocarb, and pirimiphos-methyl. Clothianidin 2% treated papers were locally made and tested using WHO tube bioassay while chlorfenapyr (100 µg/bottle) was evaluated using WHO bottle assays. Furthermore, subsamples of exposed mosquitoes were identified to species and genotyped for insecticide resistance markers including the knock-down resistance (kdr) west and east, and acetylcholinesterase (Ace-1) using molecular techniques. RESULTS: High pyrethroid resistance was recorded with diagnostic dose in Abengourou (1.1 to 3.4% mortality), in Daloa (15.5 to 33.8%) and in Gagnoa (10.3 to 41.6%). With bendiocarb, mortality rates ranged from 49.5 to 62.3%. Complete mortality (100% mortality) was recorded with clothianidin in Gagnoa, 94.9% in Daloa and 96.6% in Abengourou, while susceptibility (mortality > 98%) to chlorfenapyr 100 µg/bottle was recorded at all sites and to pirimiphos-methyl in Gagnoa and Abengourou. Kdr-west mutation was present at high frequency (0.58 to 0.73) in the three sites and Kdr-east mutation frequency was recorded at a very low frequency of 0.02 in both Abengourou and Daloa samples and absent in Gagnoa. The Ace-1 mutation was present at frequencies between 0.19 and 0.29 in these areas. Anopheles coluzzii represented 100% of mosquitoes collected in Daloa and Gagnoa, and 72% in Abengourou. CONCLUSIONS: This study showed that clothianidin and chlorfenapyr insecticides induce high mortality in the natural and pyrethroid-resistant An. gambiae populations in Côte d'Ivoire. These results could support a resistance management plan by proposing an insecticide rotation strategy for vector control interventions.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s12936-024-04917-y

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 40

  1. Miller LH, Baruch DI, Marsh K, Doumbo OK. The pathogenic basis of malaria. Nature. 2002;415:673–9. · DOI
  2. Edi AVC, N’Dri BP, Chouaibou M, Kouadio FB, Pignatelli P, Raso G, et al. First detection of N1575Y mutation in pyrethroid resistant Anopheles gambiae in Southern Côte d’Ivoire. Wellcome Open Research. 2017;2:71. · DOI
  3. Keïta M, Kané F, Thiero O, Traoré B, Zeukeng F, Sodio AB, et al. Acetylcholinesterase (ace-1R) target site mutation G119S and resistance to carbamates in Anopheles gambiae (sensu lato) populations from Mali. Parasit Vectors. 2020;13:283. · DOI
  4. Koudou BG, Adja AM, Matthys B, Doumbia M, Cissé G, Koné M, et al. [Agricultural activities and malaria transmission in two eco-epidemiological settings in central Côte d’Ivoire](in French). Bull Soc Pathol Exot. 2007;100:124–6.
  5. Soro S, Hgaza VK, Edi AVC, Chouaibou M, Koudou GB, Dao D, et al. The role of agricultural and public health insecticides in the development of the multi-resistance in An. Gambiae in Tiassalé and Toumodi (Côte d’Ivoire). J Entomol Zool Studies. 2014;2:4–10.
  6. Chouaibou M, Fodjo B, Fokou G, Ouattara A, Koudou B, David J-P, et al. Influence of the agrochemicals used for rice and vegetable cultivation on insecticide resistance in malaria vectors in southern Côte d’Ivoire. Malar J. 2016;15:426. · DOI
  7. Chandre F, Darriet F, Manguin S, Brengues C, Carnevale P, Guillet P. Pyrethroid cross resistance spectrum among populations of Anopheles gambiae s.s. from Côte d’Ivoire. J Am Mosq Control Assoc. 1999;15:53–9.
  8. Tia E, Akogbeto M, Koffi A, Toure M, Adja AM, Moussa K, et al. [Pyrethroid and DDT resistance of Anopheles gambiae s.s. (Diptera: Culicidae) in five agricultural ecosystems from Côte d’Ivoire] (in French). Bull Soc Pathol Exot. 2006;99:278–82.
  9. Konan KG, Koné AB, Konan YL, Fofana D, Konan KL, Diallo A, et al. [Resistance of Anopheles gambiae s.l. to pyrethroids and DDT in Tiassalékro, an irrigated rice-growing village in the south forest zone of Côte d’Ivoire] (in French). Bull Soc Pathol Exot. 2011;104:303–6. · DOI
  10. Edi CV, Djogbénou L, Jenkins AM, Regna K, Muskavitch MAT, Poupardin R, et al. CYP6 P450 enzymes and ACE-1 duplication produce extreme and multiple insecticide resistance in the malaria mosquito Anopheles gambiae. PLoS Genet. 2014;10: e1004236. · DOI
  11. Edi AVC, N’Dri BP, Chouaibou M, Kouadio FB, Pignatelli P, Raso G, et al. First detection of N1575Y mutation in pyrethroid resistant Anopheles gambiae in Southern Côte d’Ivoire. Wellcome Open Res. 2017;2:71. · DOI
  12. Sadia CG, Kouadio FPA, Fodjo BK, Oyou SK, Beatrice AGA, Koudou BG, et al. Short-term metabolic resistance inductive effect of different agrochemical groups on Anopheles gambiae mosquitoes. Wellcome Open Res. 2021;6:147. · DOI
  13. Namountougou M, Simard F, Baldet T, Diabaté A, Ouédraogo JB, Martin T, et al. Multiple insecticide resistance in Anopheles gambiae sl populations from Burkina Faso. West Africa PLoS One. 2012;7:e48412. · DOI
  14. Alemayehu E, Asale A, Eba K, Getahun K, Tushune K, Bryon A, et al. Mapping insecticide resistance and characterization of resistance mechanisms in Anopheles arabiensis (Diptera: Culicidae) in Ethiopia. Parasit Vectors. 2017;10:407. · DOI
  15. Bayili K, Ndo S, Namountougou M, Sanou R, Ouattara A, Dabiré RK, et al. Evaluation of efficacy of Interceptor® G2, a long-lasting insecticide net coated with a mixture of chlorfenapyr and alpha-cypermethrin, against pyrethroid resistant Anopheles gambiae sl in Burkina Faso. Malar J. 2017;16:190. · DOI
  16. Camara S, Ahoua Alou LP, Koffi AA, Clegban YCM, Kabran J-P, Koffi FM, et al. Efficacy of Interceptor ® G2, a new long-lasting insecticidal net against wild pyrethroid-resistant Anopheles gambiae s.s. from Côte d’Ivoire: a semi-field trial. Parasite. 2018;25:42. · DOI
  17. Ngufor C, Critchley J, Fagbohoun J, N’Guessan R, Todjinou D, Rowland M. Chlorfenapyr (a pyrrole insecticide) applied alone or as a mixture with alpha-cypermethrin for indoor residual spraying against pyrethroid resistant Anopheles gambiae s.l.: an experimental hut study in Cove. Benin PLoS One. 2016;11:e0162210. · DOI
  18. Raghavendra K, Barik TK, Sharma P, Bhatt RM, Srivastava HC, Sreehari U, et al. Chlorfenapyr: a new insecticide with novel mode of action can control pyrethroid resistant malaria vectors. Malar J. 2011;10:16. · DOI
  19. Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, et al. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res Int. 2015;22:5–34. · DOI
  20. Oxborough RM, Seyoum A, Yihdego Y, Chabi J, Watsenga F, Agossa FR, et al. Determination of the discriminating concentration of chlorfenapyr (pyrrole) and Anopheles gambiae sensu lato susceptibility testing in preparation for distribution of Interceptor® G2 insecticide-treated nets. Malar J. 2021;20:316. · DOI
  21. Dagg K, Irish S, Wiegand RE, Shililu J, Yewhalaw D, Messenger LA. Evaluation of toxicity of clothianidin (neonicotinoid) and chlorfenapyr (pyrrole) insecticides and cross-resistance to other public health insecticides in Anopheles arabiensis from Ethiopia. Malar J. 2019;18:49. · DOI
  22. Tungu PK, Michael E, Sudi W, Kisinza WW, Rowland M. Efficacy of interceptor® G2, a long-lasting insecticide mixture net treated with chlorfenapyr and alpha-cypermethrin against Anopheles funestus: experimental hut trials in north-eastern Tanzania. Malar J. 2021;20:180. · DOI
  23. Fongnikin A, Houeto N, Agbevo A, Odjo A, Syme T, N’Guessan R, et al. Efficacy of Fludora® Fusion (a mixture of deltamethrin and clothianidin) for indoor residual spraying against pyrethroid-resistant malaria vectors: laboratory and experimental hut evaluation. Parasit Vectors. 2020;13:466. · DOI
  24. Marti-Soler H, Máquina M, Opiyo M, Alafo C, Sherrard-Smith E, Malheia A, et al. Effect of wall type, delayed mortality and mosquito age on the residual efficacy of a clothianidin-based indoor residual spray formulation (SumiShieldTM 50WG) in southern Mozambique. PLoS ONE. 2021;16: e0248604. · DOI
  25. Service MW. Mosquito ecology: field sampling methods. 2nd edn. London; New York: Elsevier Applied Science; 1993. · DOI
  26. Gillies MT, de Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region). Johannesburg; South African Institute for Medical Research. 1968;54:1–343.
  27. Hopkins GH, Mattingly P. The mosquitoes of Ethiopian Region, vol. 1: Larval bionomics of mosquitoes and taxonomy of Culicine larvaie. London, Truestees British Museum. 1952.
  28. Raghavendra K, Barik TK, Bhatt RM, Srivastava HC, Sreehari U, Dash AP. Evaluation of the pyrrole insecticide chlorfenapyr for the control of Culex quinquefasciatus Say. Acta Trop. 2011;118:50–5. · DOI
  29. Livak KJ. Organization and mapping of a sequence on the Drosophyla melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics. 1984;107:611–34. · DOI
  30. Mouhamadou CS, de Souza SS, Fodjo BK, Zoh MG, Bli NK, Koudou BG. Evidence of insecticide resistance selection in wild Anopheles coluzzii mosquitoes due to agricultural pesticide use. Infect Dis Poverty. 2019;8:64. · DOI
  31. Fodjo BK, Koudou BG, Tia E, Saric J, N’dri PB, Zoh MG, et al. Insecticides resistance status of An gambiae in areas of varying agrochemical use in Côte d’Ivoire. BioMed Res Int. 2018;2018:e2874160. · DOI
  32. Keïta M, Traoré S, Sogoba N, Dicko AM, Coulibaly B, Sacko A, et al. [Susceptibility of Anopheles gambiae sensu lato to insecticides commonly used in vector control in Mali](in French). Bull Soc Pathol Exot. 2016;109:39–45. · DOI
  33. Cisse MBM, Keita C, Dicko A, Dengela D, Coleman J, Lucas B, et al. Characterizing the insecticide resistance of Anopheles gambiae in Mali. Malar J. 2015;14:327. · DOI
  34. Moussa Amadou B, Idi A, Benabdeljelil K. Characterization of traditional poultry farming in Niger. World’s Poultry Sci J. 2011;67:517–30. · DOI
  35. Agossa FR, Padonou GG, Koukpo CZ, Zola-Sahossi J, Azondekon R, Akuoko OK, et al. Efficacy of a novel mode of action of an indoor residual spraying product, SumiShield® 50WG against susceptible and resistant populations of Anopheles gambiae (s.l.) in Benin. West Africa Parasit Vectors. 2018;11:293. · DOI
  36. Kouassi BL, Edi C, Ouattara AF, Ekra AK, Bellai LG, Gouaméné J, et al. Entomological monitoring data driving decision-making for appropriate and sustainable malaria vector control in Côte d’Ivoire. Malar J. 2023;22:14. · DOI
  37. Black BC, Hollingworth RM, Ahammadsahib KI, Kukel CD, Donovan S. Insecticidal action and mitochondrial uncoupling activity of AC-303,630 and related halogenated pyrroles. Pestic Biochem Physiol. 1994;50:115–28. · DOI
  38. Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Bergé JB, Devonshire AL, et al. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 1998;7:179–84. · DOI · Paper page
  39. Chouaïbou MS, Fodjo BK, Fokou G, Allassane OF, Koudou BG, David J-P, et al. Influence of the agrochemicals used for rice and vegetable cultivation on insecticide resistance in malaria vectors in southern Côte d’Ivoire. Malar J. 2016;15:426. · DOI
  40. Chouaïbou M, Kouadio FB, Tia E, Djogbenou L. First report of the East African kdr mutation in an Anopheles gambiae mosquito in Côte d’Ivoire. Wellcome Open Res. 2017;2:8. · DOI

Cited by

Sorted by citations

Metadata

Authors
Ekra, A. K., Edi, C. A. V., Gbalegba, G. C. N., Zahouli, J. Z. B., Danho, M., & Koudou, B. G.
Affiliations
  • Swiss Centre for Scientific Research (CI)
  • Université Alassane Ouattara (CI)
  • Institut National Polytechnique Félix Houphouët-Boigny (CI)
  • Université Nangui Abrogoua (CI)
Corresponding author
Ekra, Armand K.
ORCID
Venue
Malaria Journal
Publisher
Springer Science and Business Media LLC
Published
2024-05-22
Volume
23
Issue
1
Pages
160-160
ISSN
1475-2875 (ISSN-L)
DOI
10.1186/s12936-024-04917-y
PMC
PMC11112771
OpenAlex
W4398196391
Cited by
7
References
5
Citations by year
2026: 2 · 2025: 3 · 2024: 2
FWCI
2.90
Type
journal article
Language
en
Open access
Licence
Locations
  • Malaria Journal (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Greater South Information System
Funders
  • United States Agency for International Development
  • Centers for Disease Control and Prevention
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
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Dengue and Mosquito Control Research
Keywords
neonicotinoids, pyrrole, clothianidin, chlorfenapyr, Anopheles gambiae, insecticide resistance, malaria vector control, pyrethroid resistance, kdr mutation, ace-1 mutation, bendiocarb, pirimiphos-methyl, insecticide susceptibility, Côte d'Ivoire, insecticide resistance management, larval habitat
MeSH terms
Mosquito Vectors, Neonicotinoids, Animals, Anopheles, Female, Guanidines, Insecticide Resistance, Insecticides, Cote d'Ivoire, Larva, Malaria, Mosquito Control, Pyrethrins, Pyrroles, Thiazoles

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review