Re-visiting insecticide resistance status in Anopheles gambiae from Côte d'Ivoire: a nation-wide informative survey

Alphonsine A Koffi, Ludovic P Ahoua Alou, Jean-Paul K Kabran, Raphael N'Guessan, Cédric Pennetier, Alphonsine A Koffi, Ludovic P Ahoua Alou, Jean-Paul K Kabran, Raphael N'Guessan, Cédric Pennetier

Abstract

Insecticide resistance constitutes a major threat that may undermine current gain in malaria control in most endemic countries. National Malaria Control Programmes (NMCPs) need as much information as possible on the resistance status of malaria vectors and underlying mechanisms in order to implement the most relevant and efficient control strategy. Bioassays, biochemical and molecular analysis were performed on An. gambiae collected in six sentinel sites in Côte d'Ivoire. The sites were selected on the basis of their bioclimatic status and agricultural practices. An. gambiae populations across sites showed high levels of resistance to organochloride, pyrethroid and carbamate insecticides. The kdr and ace-1(R) mutations were detected in almost all sentinel sites with mosquitoes on the coastal and cotton growing areas mostly affected by these mutations. At almost all sites, the levels of detoxifying enzymes (mixed-function oxidases (MFOs), non-specific esterases (NSE) and glutathione-S-transferases (GSTs)) in An. gambiae populations were significantly higher than the levels found in the susceptible strain Kisumu. Pre-exposure of mosquitoes to PBO, an inhibitor of MFOs and NSEs, significantly increased mortality rates to pyrethroids and carbamates in mosquitoes but resistance in most cases was not fully synergised by PBO, inferring a residual role of additional mechanisms, including kdr and ace-1 site insensitivity. The large distribution of resistance in Côte d'Ivoire raises an important question of whether to continue to deploy pyrethroid-based long-lasting insecticidal nets (LLINs) and insecticide residual spraying (IRS) towards which resistance continues to rise with no guarantee that the level of resistance would not compromise their efficacy. Innovative strategies that combine insecticide and synergists in LLINs or spatially LLIN and an effective non-pyrethroid insecticide for IRS could be in the short term the best practice for the NMCP to manage insecticide resistance in malaria vectors in Côte d'Ivoire and other endemic countries facing resistance.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Map of Côte d'Ivoire showing…
Figure 1. Map of Côte d'Ivoire showing the localities in the different ecological zones where anopheline mosquitoes were collected.
Figure 2. Insecticidal effects of diagnostic concentrations…
Figure 2. Insecticidal effects of diagnostic concentrations of insecticides against Anopheles gambiae mosquitoes from different sentinel sites (60 min contact in WHO tube tests).
Figure 3. Insecticidal effects of diagnostic concentrations…
Figure 3. Insecticidal effects of diagnostic concentrations of one pyrethroid insecticide (permethrin) and one carbamate insecticide (carbosulfan) (60 min contact in WHO tube tests) with or without a 60 min pre-exposition to PBO.

References

    1. WHO (2011) World Malaria Report. Geneva. 259 p.
    1. WHO (2012) WHO recommended long-lastin insecticidal mosquito nets. Geneva. Available: p.
    1. WHO (2009) WHO recommended insecticides for indoor residual spraying against malaria vectors. Geneva. Available: p.
    1. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, et al... (2010) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol.
    1. Lapied B, Pennetier C, Apaire-Marchais V, Licznar P, Corbel V (2009) Innovative applications for insect viruses: towards insecticide sensitization. Trends Biotechnol 27: 190–198.
    1. Rivero A, Vezilier J, Weill M, Read AF, Gandon S (2010) Insecticide control of vector-borne diseases: when is insecticide resistance a problem? PLoS Pathog 6..
    1. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45: 371–391.
    1. Raymond-Delpech V, Matsuda K, Sattelle BM, Rauh JJ, Sattelle DB (2005) Ion channels: molecular targets of neuroactive insecticides. Invert Neurosci 5: 119–133.
    1. Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34: 653–665.
    1. Corbel V, N'Guessan R, Brengues C, Chandre F, Djogbenou L, et al. (2007) Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 101: 207–216.
    1. VectorBase (2012) AnoBase: the Anopheles database. Insecticide resistance database search. Available: . Accessed 2012 Oct 23.
    1. N'Guessan R, Corbel V, Akogbeto M, Rowland M (2007) Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerging Infectious Diseases 13: 199–206.
    1. Asidi A, N'Guessan R, Akogbeto M, Curtis C, Rowland M (2012) Loss of Household Protection from Use of Insecticide-Treated Nets against Pyrethroid-Resistant Mosquitoes, Benin. Emerg Infect Dis 18: 1101–1106.
    1. Corbel V, Akogbeto M, Damien GB, Djenontin A, Chandre F, et al... (2012) Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial. Lancet Infect Dis.
    1. PNLP_Cote_d'Ivoire (2012) Plan stratégique 2012–2015 du programme national de lutte contre le paludisme de la Côte d'Ivoire. Abidjan. 110 p.
    1. Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H (2012) Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d'Ivoire. Emerg Infect Dis 18: 1508–1511.
    1. Ahoua Alou LP, Koffi AA, Adja MA, Assi SB, Kouassi PK, et al. (2012) Status of pyrethroid resistance in Anopheles gambiae s. s. M form prior to the scaling up of Long Lasting Insecticidal Nets (LLINs) in Adzope, Eastern Cote d'Ivoire. Parasit Vectors 5: 289.
    1. Ahoua Alou LP, Koffi AA, Adja MA, Tia E, Kouassi PK, et al. (2010) Distribution of ace-1R and resistance to carbamates and organophosphates in Anopheles gambiae s.s. populations from Cote d'Ivoire. Malar J 9: 167.
    1. Koffi AA, Ahoua Alou LP, Adja AM, Chandre F, Pennetier C (2013) Insecticide Resistance status of Anopheles gambiae s.s. population from M'Bé, a WHOPES labelled experimental hut station, 10 years after the political crisis in Côte d'Ivoire. Malaria Journal 12: 151.
    1. Koffi AA, Alou LP, Adja MA, Kone M, Chandre F, et al. (2012) Update on resistance status of Anopheles gambiae s.s. to conventional insecticides at a previous WHOPES field site, “Yaokoffikro”, 6 years after the political crisis in Cote d'Ivoire. Parasit Vectors 5: 68.
    1. WHO editor (2006) Guidelines for testing mosquito adulticides intended for Indoor Residual Spraying (IRS) and Insecticide Treated Nets (ITNs). WHO/CDS/NTD/WHOPES/GCDDP/2006.3.
    1. Collins FH, Finnerty V, Petrarca V (1988) Ribosomal DNA-probes differentiate five cryptic species in the Anopheles gambiae complex. Parassitologia 30: 231–240.
    1. Scott JA, Brogdon WG, Collins FH (1993) Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520–529.
    1. Favia G, Lanfrancotti A, Spanos L, Siden 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.
    1. Lynd A, Ranson H, McCall PJ, Randle NP, Black WCt, et al. (2005) A simplified high-throughput method for pyrethroid knock-down resistance (kdr) detection in Anopheles gambiae. Malar J 4: 16.
    1. Weill M, Malcolm C, Chandre F, Mogensen K, Berthomieu A, et al. (2004) The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 13: 1–7.
    1. WHO (1998) Techniques to detect resistance mechanisms (Field and laboratory manual). Geneva. 42 p.
    1. WHO (1998) Tests procedures for insecticide resistance monitoring in malaria vectors, bioefficacy and persistence of insecticides on treated surfaces. WHO/CDS/CPC/MAL/1998.12.
    1. Raymond M, Rousset F (1995) GENEPOP Version 1.2 A population genetics software for exact tests and ecumenicism. Journal of Heredity: 248–249.
    1. Lenormand T, Guillemaud T, Bourguet D, Raymond M (1998) Appearance and sweep of the gene duplication: adaptative response and potential for new functions in the mosquito Culex pipiens . Evolution 52: 1705–1712.
    1. Djogbenou L, Labbe P, Chandre F, Pasteur N, Weill M (2009) Ace-1 duplication in Anopheles gambiae: a challenge for malaria control. Malar J 8: 70.
    1. Koffi AA, Chandre F, Ahoua Alou LP, Labbe P, Diabate A, et al.. Agricultural practices and the distribution of ace-1 duplicated alleles in Anopheles gambiae s.s. from Côte-d'Ivoire, West Africa. BMC Infect Dis submitted.
    1. Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H (2012) Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d'Ivoire. Emerg Infect Dis 18: 1508–1511.
    1. Djogbenou L, Pasteur N, Akogbeto M, Weill M, Chandre F (2010) Insecticide resistance in the Anopheles gambiae complex in Benin: a nationwide survey. Med Vet Entomol.
    1. Badolo A, Traore A, Jones CM, Sanou A, Flood L, et al. (2012) Three years of insecticide resistance monitoring in Anopheles gambiae in Burkina Faso: resistance on the rise? Malar J 11: 232.
    1. Dabire RK, Namountougou M, Sawadogo SP, Yaro LB, Toe HK, et al. (2012) Population dynamics of Anopheles gambiae s.l. in Bobo-Dioulasso city: bionomics, infection rate and susceptibility to insecticides. Parasit Vectors 5: 127.
    1. Namountougou M, Simard F, Baldet T, Diabate A, Ouedraogo JB, et al. (2012) Multiple Insecticide Resistance in Anopheles gambiae s.l. Populations from Burkina Faso, West Africa. PLoS ONE 7: e48412.
    1. Namountougou M, Diabate A, Etang J, Bass C, Sawadogo SP, et al... (2012) First report of the L1014S kdr mutation in wild populations of Anopheles gambiae M and S molecular forms in Burkina Faso (West Africa). Acta Trop.
    1. Djegbe I, Boussari O, Sidick A, Martin T, Ranson H, et al. (2011) Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J 10: 261.
    1. Fane M, Cisse O, Traore CS, Sabatier P (2012) Anopheles gambiae resistance to pyrethroid-treated nets in cotton versus rice areas in Mali. Acta Trop 122: 1–6.
    1. Yadouleton A, Martin T, Padonou G, Chandre F, Asidi A, et al. (2011) Cotton pest management practices and the selection of pyrethroid resistance in Anopheles gambiae population in northern Benin. Parasit Vectors 4: 60.
    1. Chouaibou M, Etang J, Brevault T, Nwane P, Hinzoumbe CK, et al. (2008) Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in Northern Cameroon. Trop Med Int Health 13: 476–486.
    1. Muller P, Chouaibou M, Pignatelli P, Etang J, Walker ED, et al. (2008) Pyrethroid tolerance is associated with elevated expression of antioxidants and agricultural practice in Anopheles arabiensis sampled from an area of cotton fields in Northern Cameroon. Mol Ecol 17: 1145–1155.
    1. Diabate A (2002) The Role of Agricultural Uses of Insecticides in Resistance to Prethroids in Anopheles gambiae S.L. in Burkina Faso. Am J Trop Med Hyg 67: 617–622.
    1. Yadouleton A, N'Guessan R, Allagbe H, Asidi A, Boko M, et al. (2010) The impact of the expansion of urban vegetable farming on malaria transmission in major cities of Benin. Parasit Vectors 3: 118.
    1. Tia E, Akogbeto M, Koffi A, Toure M, Adja AM, et al. (2006) [Pyrethroid and DDT resistance of Anopheles gambiae s.s. (Diptera: Culicidae) in five agricultural ecosystems from Cote-d'Ivoire]. Bull Soc Pathol Exot 99: 278–282.
    1. Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, et al. (2011) Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde (Cameroon): influence of urban agriculture and pollution. Malar J 10: 154.
    1. Jones CM, Toe HK, Sanou A, Namountougou M, Hughes A, et al. (2012) Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS ONE 7: e45995.
    1. Bigoga JD, Ndangoh DN, Awono-Ambene PH, Patchoke S, Fondjo E, et al. (2012) Pyrethroid resistance in Anopheles gambiae from the rubber cultivated area of Niete, South Region of Cameroon. Acta Trop 124: 210–214.
    1. Bigoga JD, Nanfack FM, Awono-Ambene PH, Patchoke S, Atangana J, et al. (2012) Seasonal prevalence of malaria vectors and entomological inoculation rates in the rubber cultivated area of Niete, South Region of Cameroon. Parasit Vectors 5: 197.
    1. Henry MC, Assi SB, Rogier C, Dossou-Yovo J, Chandre F, et al. (2005) Protective efficacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Cote d'Ivoire. Am J Trop Med Hyg 73: 859–864.
    1. malERA, Aultman K, Burkot TR, Chandre F, Coetzee M, et al. (2011) A research agenda for malaria eradication: vector control. PLoS Med 8: e1000401.
    1. Moiroux N, Gomez MB, Pennetier C, Elanga E, Djenontin A, et al. (2012) Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis 206: 1622–1629.
    1. Hemingway J (2000) The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochem Mol Biol 30: 1009–1015.
    1. Koudou BG, Koffi AA, Malone D, Hemingway J (2011) Efficacy of PermaNet(R) 2.0 and PermaNet(R) 3.0 against insecticide-resistant Anopheles gambiae in experimental huts in Cote d'Ivoire. Malar J 10: 172.
    1. Corbel V, Chabi J, Dabire RD, Etang J, Nwane P, et al. (2010) Field efficacy of a new mosaic long-lasting mosquito net (PermaNet 3.0) against pyrethroid-resistant malaria vectors: a multi centre study in Western and Central Africa. Malar J 9: 113.
    1. N'Guessan R, Asidi A, Boko P, Odjo A, Akogbeto M, et al. (2010) An experimental hut evaluation of PermaNet((R)) 3.0, a deltamethrin-piperonyl butoxide combination net, against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes in southern Benin. Trans R Soc Trop Med Hyg 104: 758–765.
    1. Van Bortel W, Chinh VD, Berkvens D, Speybroeck N, Trung HD, et al. (2009) Impact of insecticide-treated nets on wild pyrethroid resistant Anopheles epiroticus population from southern Vietnam tested in experimental huts. Malar J 8: 248.
    1. Pennetier C, Bouraima A, Chandre F, Piameu M, Etang J, et al... (2013) Efficacy of Olyset® Plus, a new long-lasting insecticidal net incorporating permethrin and piperonil-butoxide against multi-resistant malaria vectors. PLoS ONE submitted.
    1. Rowland M, Boko P, Odjo A, Asidi A, Akogbeto M, et al. (2013) A new long-lasting indoor residual spray formulation of the organophosphate pirimiphos methyl for prolonged malaria vector control: an experimental hut trial against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus in Southern Benin. PLoS ONE 8: e69516.

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren