Impact of three years of large scale Indoor Residual Spraying (IRS) and Insecticide Treated Nets (ITNs) interventions on insecticide resistance in Anopheles gambiae s.l. in Benin

Particle and Fibre Toxicology

Martin Akogbéto²  Ghélus Gbédjissi²  Olivier Oussou¹  Frédéric Oké-Agbo¹  Nazaire Aizoun²  Razaki Ossé²  Michel Sezonlin²  Gil Germain Padonou² 

[1] Faculté des Sciences et Techniques de l'Université d'Abomey Calavi, Calavi, Bénin;Centre de Recherche Entomologique de Cotonou (CREC), Cotonou, Bénin

关键词: Benin;    Anopheles gambiae;    Ace-1^R;    Kdr;    Resistance;    Deltamethrin;    Bendiocarb;    LLIN;    IRS;   

Others  :  1232500
DOI  :  10.1186/1756-3305-5-72

 received in 2012-02-12, accepted in 2012-04-10,  发布年份 2012

【 摘 要 】

Background

In Benin, Indoor Residual Spraying (IRS) and long-lasting insecticidal nets (LLINs) are the cornerstones of malaria prevention. In the context of high resistance of Anopheles gambiae to pyrethroids, The National Malaria Control Program (NMCP) has undertaken a full coverage of IRS in a no-flood zone in the Oueme region, coupled with the distribution of LLINs in a flood zone. We assessed the impact of this campaign on phenotypic resistance, kdr (knock-down resistance) and ace-1^R (insensitive acetylcholinesterase) mutations.

Methods

Insecticides used for malaria vector control interventions were bendiocarb WP (0.4 g/m²) and deltamethrin (55 mg/m²), respectively for IRS and LLINs. Susceptibility status of An. gambiae was assessed using World Health Organization bioassay tests to DDT, permethrin, deltamethrin and bendiocarb in the Oueme region before intervention (2007) and after interventions in 2008 and 2010. An. gambiae specimens were screened for identification of species, molecular M and S forms and for the detection of the West African kdr (L1014F) as well as ace-1^R mutations using PCR techniques.

Results

The univariate logistic regression performed showed that kdr frequency has increased significantly during the three years in the intervention area and in the control area. Several factors (LLINs, IRS, mosquito coils, aerosols, use of pesticides for crop protection) could explain the selection of individual resistant An. gambiae. The Kdr resistance gene could not be the only mechanism of resistance observed in the Oueme region. The high susceptibility to bendiocarb is in agreement with a previous study conducted in Benin. However, the occurrence of ace-1^R heterozygous individuals even on sites far from IRS areas, suggests other factors may contribute to the selection of resistance other than those exerted by the vector control program.

Conclusion

The results of this study have confirmed that An.gambiae have maintained and developed the resistance to pyrethroids, but are still susceptible to bendiocarb. Our data clearly shows that selection of resistant individuals was caused by other insecticides than those used by the IRS and LLINs.

【 授权许可】

   
2012 Padonou et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 1.

Figure 2.

【 参考文献 】

• [1]Akogbeto M, Chippaux JP, Coluzzi M: Le paludisme urbain côtier à Cotonou (Republique du Benin). Revue Epidemiologie et Sante Publique. Rev Epidemiol Sante Publique 1992, 40:233-239.
• [2]Favia G, Lanfrancotti A, Spanos L, Sideen-Kiamos I, Louis C: Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol Biol 2001, 10(1):19-23.
• [3]Curtis CF, Myamba J, Wilkes TJ: Comparison of different insecticides and fabrics for antimosquito bednets and curtains. Med Vet Entomol 1996, 10:1-11.
• [4]Kleinschmidt I, Schwabe C, Shiva M, Segura JL, Sima V, Mabunda SJA, Coleman M: Combining indoor residual spraying and insecticide-treated net interventions. AmJTrop Med Hyg 2009, 81(3):519-524.
• [5]Roll Back Malaria Partnership: [http://rbm.who.int/partnership/wg/wg_LLIN/docs/RBMWIN StatementVector.pdf] webciteConsensus Statement on Insecticide-Treated Netting and Indoor Residual Spraying. Geneva, World Health Organization; 2004.
• [6]Hemingway J, Ranson H: Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 2000, 45:371-391.
• [7]Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Bergé JB, Devonshire AL, Guillet P, Pasteur N, Pauron D: Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 1998, 7:179-184.
• [8]Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH: Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol 2000, 9:491-497.
• [9]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, 15:53-59.
• [10]Diabate A, Brengues C, Baldet T, Dabiré KR, Hougard JM, Akogbeto M, Kengne P, Simard F, Guillet P, Hemingway J, Chandre F: The spread of the Leu-Phe kdr mutation through Anopheles gambiae complex in Burkina Faso: genetic introgression and de novo phenomena. Trop Med Int Health 2004, 9:1267-1273.
• [11]Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P, Chouaibou M, Ndjemai H, Simard F: First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. AmJTrop Med Hyg 2006, 74(5):795-797.
• [12]Tripet F, Wright J, Cornel A, Fofana A, McAbee R, Meneses C, Reimer L, Slotman M, Thiemann T, Dolo G, Traoré S, Lanzaro G: Longitudinal survey of knockdown resistance to pyrethroid (kdr) in Mali, West Africa, and evidence of its emergence in the Bamako form of Anopheles gambiae s.s. AmJTrop Med Hyg 2007, 76:81-87.
• [13]Chouaibou M, Etang J, Brevault T, Nwane P, Hinzoumbe CK, Mimpfoundi R, Simard F: 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 2008, 13:476-486.
• [14]Kristan M, Fleischmann H, Della Torre A, Stich A, Curtis Curtis CF: Pyrethroid resistance/susceptibility and differential urban/rural distribution of Anopheles arabiensis and An. gambiae s.s. malaria vectors in Nigeria and Ghana. Med Vet Entomol 2003, 17:326-332.
• [15]Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, Donnelly MJ, Petrarca V, Simard F, Pinto J, Della Torre A: Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 2008, 7:74. BioMed Central Full Text
• [16]Tia E, Akogbeto M, Koffi A, Toure M, Adja AM, Moussa K, Yao T, Carnevale P, Chandre E: Pyrethroid and DDT resistance of Anopheles gambiae s.s. (Diptera: Culicidae) in five agricultural ecosystems from Côte-d'Ivoire. Bull Soc Pathol Exot 2006, 99:278-282.
• [17]Reimer LJ, Tripet F, Slotman M, Spielman A, Fondjo E, Lanzaro GC: An unusual distribution of the kdr gene among populations of Anopheles gambiae on the island of Bioko, Equatorial Guinea. Insect Mol Biol 2005, 14:683-688.
• [18]Akogbeto M, Yakoubou S: Resistance of malaria vectors to pyrethroids used for impregnating mosquito nets in Benin, West Africa. Bull Soc Pathol Exot 1999, 92(2):123-130.
• [19]Corbel V, N'Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, Akogbéto M, Hougard JM, Rowland M: Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 2007, 101:207-216.
• [20]Akogbeto MC, Padonou GG, Gbenou D, Irish S, Yadouleton A: Bendiocarb, a potential alternative against pyrethroid resistant Anopheles gambiae in Benin, West Africa. Malar J 2010, 9:204. BioMed Central Full Text
• [21]Padonou GG, Sezonlin M, Gbedjissi GL, Ayi I, Azondekon R, Djenontin A, Bio-Bangana S, Oussou O, Yadouleton A, Boakye D, Akogbeto M: Biology of Anopheles gambiae and insecticide resistance: Entomological study for a large scale of indoor residual spraying in South East Benin. J Parasitol Vector Biol 2011, 3(4):59-68.
• [22]Vulule JM, Beach RF, Atieli FK, Mount DL, Roberts JM, Mwangi RW: Long-term use of permethrin-impregnated nets does not increase Anopheles gambiae permethrin tolerance. Med Vet Entomol 1996, 10:71-79.
• [23]Kulkarni MA, Malima R, Mosha FW, Msangi S, Mrema E: Efficacy of pyrethroid-treated nets against malaria vectors and nuisance- biting mosquitoes in Tanzania in areas with long-term insecticide-treated net use. Trop Med Int Health 2007, 12:1061-1073.
• [24]Stump AD, Atieli FK, Vulule JM, Besansky NJ: Dynamics of the pyrethroid knockdown resistance allele in western Kenyan populations of Anopheles gambiae in response to insecticide- treated bed net trials. AmJTrop Med Hyg 2004, 70:591-596.
• [25]Czeher C, Labbo R, Arzika I, Duchemin JB: Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation. Malar J 2008, 7:189. BioMed Central Full Text
• [26]Corbel V, Chandre F, Brengues C, Akogbeto M, Lardeux F: Dosage-dependent effects of permethrin-treated nets on the behaviour of Anopheles gambiae and the selection of pyrethroid resistance. Malar J 2004, 3:22. BioMed Central Full Text
• [27]Asidi AN, N'Guessan R, Koffi AA, Curtis CF, Hougard JM: Experimental hut evaluation of bednets treated with an organophosphate (chlorpyrifos-methyl) or a pyrethroid (lambdacyhalothrin) alone and in combination against insecticide-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes. Malar J 2005, 4:25. BioMed Central Full Text
• [28]Akogbeto M, Padonou GG, Bankole HS, Gazard DK, Gbedjissi GL: Dramatic decrease in malaria transmission after large-scale indoor residual spraying with Bendiocarb in Benin, an area of high resistance of Anopheles gambiae to Pyrethroids. AmJTrop Med Hyg 2011, 85(4):586-593.
• [29]Gillies MT, De Meillon B: The Anophelinae of Africa south of the Sahara. Publication of the South African Institute for Medical Research, Johannesburg; 1968:54.
• [30]Scott JA, Brogdon WG, Collins FH: Identification of single specimens of Anopheles gambiae complex by polymerase chain reaction. AmJTrop Med Hyg 1993, 49:520-529.
• [31]Favia G, Della Torre A, Bagayoko M, Lanfrancotti , Sagnon NF, Toure Y, Coluzzi M: Molecular identification of sympatric chromosomal forms of Anopheles gambiae and further evidence of their reproductive isolation. Insect Mol Biol 1997, 6:377-383.
• [32]Weill M, Malcolm C, Chandre F, Mogensen K, Berthomieu A, Marquine M, Raymond M: The unique mutation in Ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 2004, 13:1-7.
• [33]World Health Organisation: Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces. [http://whqlibdoc.who.int/hq/1998/WHO_CDS_CPC_MAL_98.12.pdf] webciteDocument WHO/CDS/CPC/MAL/98.12 Geneva, Switzerland 1998.
• [34]R Development Core Team: R A language and environment for statistical computing. 2.11.1. ed. Vienna Austria 2010.
• [35]Raymond M, Rousset F: GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 1995, 86:248-249.
• [36]Berzosa PJ, Cano J, Roche J, Rubia JM, Garcia L, Moyano E, Guerra A, Mateos JC, Petraca V, Do Rosaria V, Benito A: Malaria vectors in Bioko island (Equatorial Guinea): PCR determination of the members of Anopheles gambiae Giles complex (Diptera: Culicidae) and pyrethoid knockdown resistance (kdr) in An. gambiae sensu stricto. J Vector. Ecology 2002, 27:102-106.
• [37]Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I: Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko. Equatorial Guinea Malar J 2007, 6:52.
• [38]Djègbè I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, Akogbéto M, Corbel V: 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 2011, 10:261. BioMed Central Full Text
• [39]N'Guessan R, Corbel V, Akogbéto M, Rowland M: Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg Infect Dis 2007, 13:199-206.
• [40]Balkew M, Ibrahim M, Koekemoer LL, Brooke BD, Engers H, Aseffa A, Gebre-Michael T, Elhassen I: Insecticide resistance in Anopheles arabiensis (Diptera: Culicidae) from villages in central, northern and south west Ethiopia and detection of kdr mutation. Parasit Vectors 2010, 3(1):40. BioMed Central Full Text
• [41]Lines JD: Do agricultural insecticides select for insecticide resistance in mosquitoes, a look at the evidence. Parasitol Today 1988, 4:17-20.
• [42]Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, D'Alessandro U, Coosemans M: A high increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands. Trop Med Int Health 2008, 13:1479-1487.
• [43]Yewhalaw D, Wassie F, Steurbaut W, Spanoghe P, Van Bortel W, Denis L, Tessema DA, Getachew Y, Coosemans M, Duchateau , Speybroeck N: Multiple insecticide resistance: an impediment to insecticide-based malaria vector control program. PLoS One 2011, 6(1):16066.
• [44]Djogbenou L, Pasteur N, Akogbeto M, Weill M, Chandre F: Insecticide resistance in the Anopheles gambiae complex in Benin: a nationwide survey. Med Vet Entomol 2009, 69:160-164.
• [45]Raymond M, Berticat C, Weill M, Pasteur N, Chevillon C: Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation? Genetica 2001, 112:287-296.
• [46]Labbé P, Berthomieu A, Berticat C, Alout H, Raymond M, Lenormand T, Weill M: Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Mol Biol Evol 2007, 24(4):1056-1067.
• [47]Djogbenou L, Noel V, Agnew P: Costs of insensitive acetylcholinesterase insecticide resistance for the malaria vector Anopheles gambiae homozygous for the G119S mutation. Malar J 2010, 9:12. BioMed Central Full Text
• [48]Yadouleton WA, Padonou G, Asidi A, Moiroux N, Banganna S, Corbel V, N'guessan R, Gbenou D, Yacoubou I, Gazard Kinde D, Akogbeto CM: Insecticide resistance status in Anopheles gambiae in southern Benin. Malar J 2010, 9:83. BioMed Central Full Text
• [49]Ngufor C, N'Guessan R, Boko P, Odjo A, Vigninou E, Asidi A, Akogbeto M, Rowland M: Combining indoor residual spraying with chlorfenapyr and long-lasting insecticidal bed nets for improved control of pyrethroid-resistant Anopheles gambiae: an experimental hut trial in Benin. Malar J 2011, 10:343. BioMed Central Full Text
• [50]Corbel V, Henry MC: Prevention and control of malaria and sleeping sickness in Africa: where are we and where are we going? Parasit Vectors 2011, 4:37. BioMed Central Full Text