Malaria control programs are being jeopardized by the spread of insecticide resistance in mosquito vector populations. The situation in Burkina Faso is emblematic with Anopheles gambiae populations showing high levels of resistance to most available compounds. Although the frequency of insecticide target-site mutations including knockdown resistance (kdr) and insensitive acetylcholinesterase (Ace-1R) alleles has been regularly monitored in the area, it is not known whether detoxifying enzymes contribute to the diversity of resistance phenotypes observed in the field. Here, we propose an update on the phenotypic diversity of insecticide resistance in An. gambiae populations sampled from 10 sites in Burkina Faso in 2010. Susceptibility to deltamethrin, permethrin, DDT, bendiocarb and fenithrotion was assessed. Test specimens (N = 30 per locality) were identified to species and molecular form and their genotype at the kdr and Ace-1 loci was determined. Detoxifying enzymes activities including non-specific esterases (NSEs), oxydases (cytochrome P450) and Glutathione S-Transferases (GSTs) were measured on single mosquitoes (N = 50) from each test locality and compared with the An. gambiae Kisumu susceptible reference strain. In all sites, mosquitoes demonstrated multiple resistance phenotypes, showing reduced mortality to several insecticidal compounds at the same time, although with considerable site-to-site variation. Both the kdr 1014L and Ace-1R 119S resistant alleles were detected in the M and the S forms of An. gambiae, and were found together in specimens of the S form. Variation in detoxifying enzyme activities was observed within and between vector populations. Elevated levels of NSEs and GSTs were widespread, suggesting multiple resistance mechanisms segregate within An. gambiae populations from this country. By documenting the extent and diversity of insecticide resistance phenotypes and the putative combination of their underlying mechanisms in An. gambiae mosquitoes, our work prompts for new alternative strategies to be urgently developed for the control of major malaria vectors in Burkina Faso.
References
[1]
World Health Organization. Launch of the Global Plan for Insecticide Resistance Management in malaria vectors. Available at: http://www.who.int/malaria/vector_contro？l/gpirm_event_report_2012.pdf. Accessed 2012 May 15.
[2]
Lengeler C (2004) Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev 2: CD000363.
Kelly-Hope L, Ranson H, Hemingway J (2008) Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis 8: 387–389.
[5]
Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, et al. (2000) Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14: 181–189.
[6]
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. Emerg Infect Dis 13: 199–206.
[7]
Hamon J, Subra R, Sales S, Coz J (1968) Presence in the southwestern part of Upper Volta of a population of Anopheles gambiae “A” resistant to DDT. Med Trop 28: 521–528.
[8]
Hamon J, Sales S, Venard P, Coz J, Brengues J (1968) The presence in southwest Upper Volta of populations of Anopheles funestus Giles resistant to dieldrin. Med Trop 28: 221–226.
[9]
Dabire KR, Diabate A, Namountougou M, Toe KH, Ouari A, et al. (2009a) Distribution of pyrethroid and DDT resistance and the L1014F kdr mutation in Anopheles gambiae s.l. from Burkina Faso (West Africa). Trans R Soc Trop Med Hyg 103: 1113–1120.
[10]
Diabate A, Brengues C, Baldet T, Dabire KR, Hougard JM, et al. (2004) 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 9: 1267–1273.
[11]
Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, et al. (2002) The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg 67: 617–622.
[12]
Mittal PK, Adak T, Sharma VP (1991) Acute toxicity of certain organochlorine, organophosphorus, synthetic pyrethroid and microbial insecticides to the mosquito fish Gambusia affinis (Baird and Girard). Indian J malariol 28: 167–170.
[13]
Zaim M, Aitio A, Nakashima N (2000) Safety of pyrethroid-treated mosquito nets. Med Vet Entomol 14: 1–5.
[14]
Casimiro S, Coleman M, Hemingway J, Sharp B (2006) Insecticide resistance in Anopheles arabiensis and Anopheles gambiae from Mozambique. J Med Entomol 43: 276–282.
[15]
Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, et al. (2009) Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J 8: 299.
[16]
Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34: 653–665.
[17]
Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, et al. (2008) Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 7: 74.
[18]
Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, et al. (2000) 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 9: 491–497.
[19]
Ndjemai HN, Patchoke S, Atangana J, Etang J, Simard F, et al. (2009) The distribution of insecticide resistance in Anopheles gambiae s.l. populations from Cameroon: an update. Trans R Soc Trop Med Hyg 103: 1127–1138.
[20]
Nwane P, Etang J, Chouaibou M, Toto JC, Kerah-Hinzoumbe C, et al. (2009) Trends in DDT and pyrethroid resistance in Anopheles gambiae s.s. populations from urban and agro-industrial settings in southern Cameroon. BMC Infect Dis 9: 163.
[21]
Janeira F, Vicente JL, Kanganje Y, Moreno M, Do Rosario VE, et al. (2008) A primer-introduced restriction analysis-polymerase chain reaction method to detect knockdown resistance mutations in Anopheles gambiae. J Med Entomol 45: 237–241.
[22]
Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C, et al. (2006) Co-occurrence of East and West African kdr mutations suggests high levels of resistance to pyrethroid insecticides in Anopheles gambiae from Libreville, Gabon. Med Vet Entomol 20: 27–32.
[23]
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. Malaria J 10: 261.
[24]
Guillet P, N'Guessan R, Darriet F, Traore-Lamizana M, Chandre F, et al. (2001) Combined pyrethroid and carbamate ‘two-in-one’ treated mosquito nets: field efficacy against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus. Med Vet Entomol 15: 105–112.
[25]
Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, et al. (2003) Comparative genomics: Insecticide resistance in mosquito vectors. Nature 423: 136–137.
[26]
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.
[27]
Chandre F, Darriet F, Doannio JM, Riviere F, Pasteur N, et al. (1997) Distribution of organophosphate and carbamate resistance in Culex pipiens quinquefasciatus (Diptera: Culicidae) in West Africa. J Med Entomol 34: 664–671.
[28]
N'Guessan R, Darriet F, Guillet P, Carnevale P, Traore-Lamizana M, et al. (2003) Resistance to carbosulfan in Anopheles gambiae from Ivory Coast, based on reduced sensitivity of acetylcholinesterase. Med Vet Entomol 17: 19–25.
[29]
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.
[30]
Djogbenou L, Dabire R, Diabate A, Kengne P, Akogbeto M, et al. (2008) Identification and geographic distribution of the ACE-1R mutation in the malaria vector Anopheles gambiae in south-western Burkina Faso, West Africa. Am J Trop Med Hyg 78: 298–302.
[31]
Dabire KR, Diabate A, Namountougou M, Djogbenou L, Kengne P, et al. (2009b) Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa). Trop Med Int Health 14: 396–403.
[32]
Scott JG (1996) Cytochrome P450 monooxygenase-mediated resistance to insecticides. J Pest Sci 21: 241–245.
[33]
Hemingway J, Karunaratne SH (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Med Vet Entomol 12: 1–12.
[34]
Prapanthadara LA, Ketterman AJ (1993) Qualitative and quantitative changes in glutathione S-transferases in the mosquito Anopheles gambiae confer DDT-resistance. Biochem Soc trans 21: 304S.
[35]
Prapanthadara LA, Koottathep S, Promtet N, Hemingway J, Ketterman AJ (1996) Purification and characterization of a major glutathione S-transferase from the mosquito Anopheles dirus (species B). Insect Biochem Mol Biol 26: 277–285.
[36]
Hemingway J, Callaghan A, Amin AM (1990) Mechanisms of organophosphate and carbamate resistance in Culex quinquefasciatus from Saudi Arabia. Med Vet Entomol 4: 275–282.
[37]
Hemingway J, Davidson G (1983) Resistance to organophosphate and carbamate insecticides in Anopheles atroparvus. Parassitologia 25: 1–8.
[38]
Hemingway J (1984) The joint action of malathion and IBP against malathion-resistant and -susceptible strains of Anopheles stephensi. Bull World Health Organ 62: 445–449.
[39]
Ranson H, Nikou D, Hutchinson M, Wang X, Roth CW, et al. (2002) Molecular analysis of multiple cytochrome P450 genes from the malaria vector, Anopheles gambiae. Insect Mol Biol 11: 409–418.
[40]
Etang J, Manga L, Toto JC, Guillet P, Fondjo E, et al. (2007) Spectrum of metabolic-based resistance to DDT and pyrethroids in Anopheles gambiae s.l. populations from Cameroon. J Vector Ecol 32: 123–133.
[41]
Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, et al. (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics 9: 538.
[42]
Muller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, et al. (2008a) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 4: e1000286.
[43]
Muller P, Chouaibou M, Pignatelli P, Etang J, Walker ED, et al. (2008b) 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.
[44]
Dabire KR, Diabate A, Djogbenou L, Ouari A, N'Guessan R, et al. (2008) Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar J 7: 188.
[45]
Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, et al. (2009) Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol 9: 16.
[46]
Ouédraogo M, Toé AM, Ouédraogo TZ, Guissou PI (2011) Pesticides in Burkina Faso: Overview of the Situation in a Sahelian African Country. In: Stoytchevan M, editors. Pesticides in the Modern World - Pesticides Use and Management. ISBN. InTech: pp. 35–48.
[47]
Gillies M, De Meillon B (1968) The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region). Inst Med Res 54: 343.
[48]
World Health Organization (1998) Report of the WHO informal consultation on test procedures for insecticides on treated surfaces. WHO/CDS/CPC/MAL/98.
[49]
Fanello C, Santolamazza F, della Torre A (2002) Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol 16: 461–464.
[50]
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.
[51]
Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, et al. (1998) Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 7: 179–184.
[52]
Raymond M, Rousset F (1995) GENEPOP Version 1.2 A population genetics software for exact tests and ecumenicism. J Hered 248–249.
[53]
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254.
Gimonneau G, Pombi M, Choisy M, Morand S, Dabiré RK, et al. (2012) Larval habitat segregation between the molecular forms of the mosquito Anopheles gambiae in a rice field area of Burkina Faso, West Africa. Med Vet Entomol 26: 9–17.
[56]
Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, et al. (1999) Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ 77: 230–234.
[57]
Dabiré KR, Diabaté A, Namountougou M, Djogbenou L, Wondji C, et al.. (2012) Trends in Insecticide Resistance in Natural Populations of Malaria Vectors in Burkina Faso, West Africa: 10 Years' Surveys. In: Perveen F, editors. Insecticides - Pest Engineering. ISBN. InTech: pp. 479–502.
[58]
Akogbeto MC, Djouaka RF, Kinde-Gazard DA (2006) Screening of pesticide residues in soil and water samples from agricultural settings. Malar J 5: 22.
[59]
Akogbeto M, Padonou GG, Bankole HS, Gazard DK, Gbedjissi GL (2011) 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. Am J Trop Med Hyg 85: 586–593.
[60]
Labbe P, Berthomieu A, Berticat C, Alout H, Raymond M, et al. (2007) Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Mol Biol Evol 24: 1056–1067.
[61]
Djogbenou L, Chandre F, Berthomieu A, Dabire R, Koffi A, et al. (2008) Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s.s. PLoS ONE 3: e2172.
[62]
Djogbenou L, Noel V, Agnew P (2010) Costs of insensitive acetylcholinesterase insecticide resistance for the malaria vector Anopheles gambiae homozygous for the G119S mutation. Malar J 9: 12.
[63]
Djogbenou L, Labbé P, Chandre F, Pasteur N, Weill M (2009) Ace-1 duplication in Anopheles gambiae: a challenge for malaria control. Malar J 8: 70.
[64]
Vontas JG, Small GJ, Hemingway J (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 357: 65–72.
[65]
Mitchell SN, Stevenson BJ, Müller P, Wilding CS, Yawson AE, et al. (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. PNAS 109: 6147–6152.
[66]
Willoughby L, Batterham P, Daborn PJ (2007) Piperonyl butoxide induces the expression of cytochrome P450 and glutathione S-transferase genes in Drosophila melanogaster. Pest Manag Sci 63: 803–808.
