Anopheles bionomics, insecticide resistance mechanisms, and malaria transmission in the Korhogo area, northern Côte d’Ivoire: a pre-intervention study
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Abstract
A better understanding of malaria transmission at a local scale is essential for developing and implementing effective control strategies. In the framework of a randomized controlled trial (RCT), we aimed to provide an updated description of malaria transmission in the Korhogo area, northern Côte d’Ivoire, and to obtain baseline data for the trial. We performed human landing collections (HLCs) in 26 villages in the Korhogo area during the rainy season (September–October 2016, April–May 2017) and the dry season (November–December 2016, February–March 2017). We used PCR techniques to ascertain the species of the Anopheles gambiae complex, Plasmodium falciparum sporozoite infection, and insecticide resistance mechanisms in a subset of Anopheles vectors. Anopheles gambiae s.l. was the predominant malaria vector in the Korhogo area. Overall, more vectors were collected outdoors than indoors ( p < 0.001). Of the 774 An. gambiae s.l. tested in the laboratory, 89.65% were An. gambiae s.s. and 10.35% were An. coluzzii . The frequencies of the kdr allele were very high in An. gambiae s.s. but the ace-1 allele was found at moderate frequencies. An unprotected individual living in the Korhogo area received an average of 9.04, 0.63, 0.06 and 0.12 infected bites per night in September–October, November–December, February–March, and April–May, respectively. These results demonstrate that the intensity of malaria transmission is extremely high in the Korhogo area, especially during the rainy season. Malaria control in highly endemic areas such as Korhogo needs to be strengthened with complementary tools in order to reduce the burden of the disease.
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The lower frequency of resistance alleles in An. coluzzii was associated with a higher proportion of heterozygotes, implying that An. gambiae is better adapted to insecticide pressure.
“The lower frequency the resistance alleles in An. coluzzii was associated with higher proportion of heterozygous, implying that An. gambiae is better adapted to insecticide pressure as evidenced elsewhere in Côte d’Ivoire [8, 37] and other parts of sub-Saharan Africa [24, 38, 39].”
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 [24]
The Discussion reports that both resistance alleles were more frequent in An. gambiae s.s. than in An. coluzzii. Results Table 5 also shows a higher proportion of kdr heterozygotes in An. coluzzii in several surveys, but Table 6 does not show that pattern for ace-1. The paper does not establish that An. gambiae s.s. is better adapted to insecticide pressure. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn Côte d'Ivoire, four vector species, An. gambiae s.s, An. coluzzii, An. funestus and An. nili, are responsible for malaria transmission.
“Several studies have shown that four vector species, An. gambiae s.s, An. coluzzii, An. funestus and An. nili, are responsible for malaria transmission (Diakité et al. 2015; Zogo et al. 2019).”
From Resting and feeding behaviour of malaria vectors, in two areas of high long-lasting insecticidal nets coverage in Côte d'Ivoire (2024) · cites this paper as Zogo et al. 2019
The Conclusions identify all four named vector categories as contributing to malaria transmission in the Korhogo area, with An. gambiae s.s. and An. coluzzii playing the main roles. The study does not establish that these are the four responsible species throughout Côte d’Ivoire; it identifies the other two only as members of the An. funestus group and An. nili complex. (LLM, conf=0.88)
Experimental — accuracy not yet measuredA total of 8 species of Anopheles genus were identified in all villages, including three malaria vectors: An. gambiae s.l., An. funestus and An. nili.
“A total of 8 species of Anopheles genus were identified in all villages, including three malaria vectors that are An. gambiae s.l., An. funestus and An. nili, already reported for their involvement in malaria transmission in Côte d'Ivoire (Zogo et al. 2019; Assouho et al. 2020; Adja et al. 2020).”
From Resting and feeding behaviour of malaria vectors, in two areas of high long-lasting insecticidal nets coverage in Côte d'Ivoire (2024) · cites this paper as Zogo et al. 2019
This observation is in line with studies conducted in the western, eastern, northern and central parts of Côte d'Ivoire, which found high levels of malaria transmission.
“This observation is in line with studies conducted in the western [16], eastern [42], northern [43] and central parts of Côte d’Ivoire [44], which found high levels of malaria transmission.”
From Characterization and abundance of malaria vectors in Sakassou, Central Côte d'Ivoire (2025) · cites this paper as [43]
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Cites
Characterizing, controlling and eliminating residual malaria transmission
Killeen, G. F. (2014) · Malaria Journal · doi:10.1186/1475-2875-13-330 · Cited by 506 · see citing works
Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa.
Beier, J. C., Killeen, G. F., & Githure, J. I. (1999) · The American journal of tropical medicine and hygiene · doi:10.4269/ajtmh.1999.61.109 · Cited by 399 · see citing works
Moiroux, N., Gomez, M. B., Pennetier, C., Elanga, E., Djènontin, A., Chandre, F., Djègbé, I., Guis, H., & Corbel, V. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis565 · Cited by 383 · see citing works
Self-citationMathias, D. K., Ochomo, E., Atieli, F., Ombok, M., Nabie Bayoh, M., Olang, G., Muhia, D., Kamau, L., Vulule, J. M., Hamel, M. J., et al. (2011) · Malaria Journal · doi:10.1186/1475-2875-10-10 · Cited by 158 · see citing works
Mapping insecticide resistance in Anopheles gambiae (s.l.) from Côte d'Ivoire
Camara, S., Koffi, A. A., Ahoua Alou, L. P., Koffi, K., Kabran, J.-P. K., Koné, A., Koffi, M. F., N’Guessan, R., & Pennetier, C. (2018) · Parasites & Vectors · doi:10.1186/s13071-017-2546-1 · Cited by 99 · see citing works
Self-citationKoffi, A. A., Ahoua Alou, L. P., Kabran, J.-P. K., N'Guessan, R., & Pennetier, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082387 · Cited by 46 · see citing works
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Research works printed but not linked: 32
- [1]Awolola TS, Oduola AO, Oyewole IO, Obansa JB, Amajoh CN, Koekemoer LL, Coetzee M. 2007 Dynamics of knockdown pyrethroid insecticide resistance alleles in a field population of Anopheles gambiae s.s. in southwestern Nigeria. Journal of Vector Borne Diseases, 44, 181– 188. 17896620
- [2]Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, Ball A, Vontas J, Field LM. 2007 Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malaria Journal, 6, 111. 17697325 PMC1971715
- [4]Boissière A, Gimonneau G, Tchioffo MT, Abate L, Bayibeki A, Awono-Ambéné PH, Nsango SE, Morlais I. 2013 Application of a qPCR Assay in the investigation of susceptibility to malaria infection of the m and s molecular forms of An. gambiae s.s. in Cameroon. PLoS One, 8, e54820. 23349974 PMC3551906
- [5]Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM. 2017 glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9(2), 378– 400.
- [7]Dabiré KR, Diabaté A, Namontougou M, Djogbenou L, Kengne P, Simard F, Bass C, Baldet T. 2009 Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa). Tropical Medicine and International Health, 14, 396– 403. 19254231
- [8]Dabiré RK, Namountougou M, Diabaté A, Soma DD, Bado J, Toé HK, Bass C, Combary P. 2014 Distribution and frequency of kdr mutations within Anopheles gambiae s.l. populations and first report of the ace.1g119 s mutation in Anopheles arabiensis from Burkina Faso (West Africa). PLoS One, 9, e101484. 25077792 PMC4117487
- [9]Dao A, Yaro AS, Diallo M, Timbine S, Huestis DL, Kassogue Y, Traore AI, Sanogo ZL, Samake D, Lehmann T. 2014 Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature, 516, 387– 390. 25470038 PMC4306333
- [10]Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM. 2002 The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. American Journal of Tropical Medicine and Hygiene, 67, 617– 622. 12518852
- [11]Djogbénou L, Weill M, Hougard JM, Raymond M, Akogbéto M, Chandre F. 2007 Characterization of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance. Journal of Medical Entomology, 44, 805– 810. 17915512
- [12]Essandoh J, Yawson AE, Weetman D. 2013 Acetylcholinesterase (Ace-1) target site mutation 119S is strongly diagnostic of carbamate and organophosphate resistance in Anopheles gambiae s.s. and Anopheles coluzzii across southern Ghana. Malaria Journal, 12, 404. 24206629 PMC3842805
- [13]Favia G, Lanfrancotti A, Spanos L, Sidén-Kiamos I, Louis C. 2001 Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Molecular Biology, 10, 19– 23. 11240633
- [14]Fornadel CM, Norris LC, Glass GE, Norris DE. 2010 Analysis of Anopheles arabiensis blood feeding behavior in southern Zambia during the two years after introduction of insecticide-treated bed nets. American Journal of Tropical Medicine and Hygiene, 83, 848– 853. 20889878 PMC2946755
- [18]Goudet J, Raymond M, de Meeüs T, Rousset F. 1996 Testing differentiation in diploid populations. Genetics, 144, 1933– 1940. 8978076 PMC1207740
- [19]Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, Bousema T, Drakeley CJ, Ferguson NM, Basáñez M-G, Ghani AC. 2010 Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Medicine, 7, e1000324. 20711482 PMC2919425
- [20]Ijumba JN, Lindsay SW. 2001 Impact of irrigation on malaria in Africa: paddies paradox. Medical and Veterinary Entomology, 15, 1– 11. 11297093
- [22]Kleinschmidt I, Bradley J, Knox TB, Mnzava AP, Kafy HT, Mbogo C, Ismail BA, Bigoga JD, Adechoubou A, Raghavendra K, Cook J, Malik EM, Nkuni ZJ, Macdonald M, Bayoh N, Ochomo E, Fondjo E, Awono-Ambene HP, Etang J, Akogbeto M, Bhatt RM, Chourasia MK, Swain DK, Kinyari T, Subramaniam K, Massougbodji A, Okê-Sopoh M, Ogouyemi-Hounto A, Kouambeng C, Abdin MS, West P, Elmardi K, Cornelie S, Corbel V, Valecha N, Mathenge E, Kamau L, Lines J, Donnelly MJ. 2018 Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: a WHO-coordinated, prospective, international, observational cohort study. Lancet Infectious Diseases, 18, 640– 649. 29650424 PMC5968369
- [23]Kliot A, Ghanim M. 2012 Fitness costs associated with insecticide resistance. Pest Management Science, 68, 1431– 1437. 22945853
- [25]Livak KJ. 1984 Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics, 107, 611– 634. 6430749 PMC1202380
- [26]Maliti DV, Marsden CD, Main BJ, Govella NJ, Yamasaki Y, Collier TC, Kreppel K, Chiu JC, Lanzaro GC, Ferguson HM, Lee Y. 2016 Investigating associations between biting time in the malaria vector Anopheles arabiensis Patton and single nucleotide polymorphisms in circadian clock genes: support for sub-structure among An. arabiensis in the Kilombero valley of Tanzania. Parasites & Vectors, 9, 109. 26920563 PMC4769569
- [28]Moiroux N, Damien GB, Egrot M, Djenontin A, Chandre F, Corbel V, Killeen GF, Pennetier C. 2014 Human exposure to early morning Anopheles funestus biting behavior and personal protection provided by long-lasting insecticidal nets. PLoS One, 9, e104967. 25115830 PMC4130624
- [30]Mourou J-R, Coffinet T, Jarjaval F, Cotteaux C, Pradines E, Godefroy L, Kombila M, Pagès F. 2012 Malaria transmission in Libreville: results of a one year survey. Malaria Journal, 11, 40. 22321336 PMC3310827
- [31]Ngowo HS, Kaindoa EW, Matthiopoulos J, Ferguson HM, Okumu FO. 2017 Variations in household microclimate affect outdoor-biting behaviour of malaria vectors. Wellcome Open Research, 2, 102. 29552642 PMC5829465
- [32]Ojuka P, Boum Y, Denoeud-Ndam L, Nabasumba C, Muller Y, Okia M, Mwanga-Amumpaire J, De Beaudrap P, Protopopoff N, Etard JF. 2015 Early biting and insecticide resistance in the malaria vector Anopheles might compromise the effectiveness of vector control intervention in Southwestern Uganda. Malaria Journal, 14, 1– 8. 25879539 PMC4416237
- [34]Raymond MRF. 1995 GENEPOP Version 1.2. A population genetics software for exact tests and ecumenicism. Journal of Heredity, 26, 248– 249.
- [35]Robert V, Macintyre K, Keating J, Trape JF, Duchemin JB, Warren M, Beier JC. 2003 Malaria transmission in urban subsaharian Africa. American Journal of Tropical Medicine and Hygiene, 68, 169– 176. 12641407
- [36]Sadia-Kacou CMA, Alou LPA, Edi AVC, Yobo CM, Adja MA, Ouattara AF, Malone D, Koffi AA, Tano Y, Koudou BG. 2017 Presence of susceptible wild strains of Anopheles gambiae in a large industrial palm farm located in Aboisso, South-Eastern of Côte d’Ivoire. Malaria Journal, 16, 157. 28427450 PMC5397756
- [37]Scott JA, Brogdon WG, Collins FH. 1993 Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. American Journal of Tropical Medicine and Hygiene, 49, 520– 529. 8214283
- [38]Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, Burkot TR, Harbach RE, Hay SI. 2012 A global map of dominant malaria vectors. Parasites & Vectors, 5, 69. 22475528 PMC3349467
- [39]Trape JF, Tall A, Sokhna C, Ly AB, Diagne N, Ndiath O, Mazenot C, Richard V, Badiane A, Dieye-Ba F, Faye J, Ndiaye G, Diene Sarr F, Roucher C, Bouganali C, Bassène H, Touré-Baldé A, Roussilhon C, Perraut R, Spiegel A, Sarthou JL, da Silva LP, Mercereau-Puijalon O, Druilhe P, Rogier C. 2014 The rise and fall of malaria in a west African rural community, Dielmo, Senegal, from 1990 to 2012: a 22 year longitudinal study. Lancet Infectious Diseases, 14, 476– 488. 24813159
- [40]Verhaeghen K, Van Bortel W, Roelants P, Okello PE, Talisuna A, Coosemans M. 2010 Spatio-temporal patterns in kdr frequency in permethrin and DDT resistant Anopheles gambiae s.s. from Uganda. American Journal of Tropical Medicine and Hygiene, 82, 566– 573. 20348500 PMC2844549
- [42]Zogo B, Soma DD, Tchiekoi BN, Somé A, Alou LPA, Koffi AA, Fournet F, Dahounto A, Coulibaly B, Kandé S, Dabiré RK, Baba-Moussa L, Moiroux N, Pennetier C. 2019 Anopheles bionomics, insecticide resistance mechanisms and malaria transmission in the Korhogo area, northern Côte d’Ivoire: a pre-intervention study. BioRxiv, 589556. PMC6625791 31298995
- [43]Zoh DD, Ahoua Alou LP, Toure M, Pennetier C, Camara S, Traore DF, Koffi AA, Adja AM, Yapi A, Chandre F. 2018 The current insecticide resistance status of Anopheles gambiae (s.l.) (Culicidae) in rural and urban areas of Bouaké, Côte d’Ivoire. Parasites & Vectors, 11, 118. 29499720 PMC5834858
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Characterization and abundance of malaria vectors in Sakassou, Central Côte d'Ivoire
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- Authors
- Zogo, B., Soma, D. D., Tchiekoi, B. N., Somé, A., Ahoua Alou, L. P., Koffi, A. A., Fournet, F., Dahounto, A., Coulibaly, B., Kandé, S., Dabiré, R. K., Baba-Moussa, L., Moiroux, N., & Pennetier, C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Nazi Boni University (BF)
- Institut National de Santé Publique (CI)
- Institut de Recherche en Sciences de la Santé (BF)
- Corresponding author
- Zogo, Barnabas
- ORCID
- Venue
- Parasite
- Publisher
- EDP Sciences
- Published
- 2019
- Volume
- 26
- Pages
- 40
- ISSN
- 1252-607X (ISSN-L)
- 1776-1042
- PMC
- PMC6625791
- OpenAlex
- W2961516233
- Cited by
- 41
- References
- 6
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 11 · 2023: 8 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 2
- FWCI
- 2.53
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Parasite (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
- Greater South Information System
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
- Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
- Keywords
- insecticide resistance mechanisms, malaria transmission, Anopheles gambiae s.l., Anopheles coluzzii, kdr allele, seasonal variation, Korhogo, malaria vector control
- MeSH terms
- Mosquito Vectors, Animals, Anopheles, Bites and Stings, Ecology, Female, Humans, Insecticide Resistance, Insecticides, Cote d'Ivoire, Malaria, Mosquito Control, Plasmodium falciparum, Seasons, Randomized Controlled Trials as Topic
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