Skip to main content
Top
Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

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

Authors: John Essandoh, Alexander E Yawson, David Weetman

Published in: Malaria Journal | Issue 1/2013

Login to get access

Abstract

Background

With high DDT resistance present throughout much of West Africa, carbamates and organophosphates are increasingly important alternatives to pyrethroids for indoor residual spraying (IRS). Though less widespread, resistance to both of these alternative insecticide classes has also been documented within the Anopheles gambiae species pair (formerly the M and S molecular forms) in West Africa. To manage insecticide efficacy, it is important to predict how and where resistance is likely to occur and spread, which could be aided by using molecular diagnostics with high predictive value.

Methods

Anopheles coluzzii and An. gambiae s.s. were collected from 18 sites throughout southern Ghana and bioassayed with bendiocarb, the most commonly applied carbamate, and an organophosphate, fenitrothion. The Ace-1 target site substitution G119S was genotyped by qPCR.

Results

Fenitrothion induced higher mortality than bendiocarb, though phenotypes correlated strongly across populations. Ace-1 119S was found at much higher frequency in An. gambiae s.s than An. coluzzii, exceeding 90% in a population from Greater Accra, the highest frequency reported to date. Ace-1 G119S was very strongly associated with resistance to both insecticides, providing high predictive power for diagnosis, though with some evidence for a differential effect between molecular forms for bendiocarb. Sequencing of the gene revealed a lack of variation in resistant alleles precluding determination of origin, but Ace-1 copy number variation was detected for the first time in Ghana.

Conclusions

The results validate G119S as a useful diagnostic of organophosphate and carbamate resistance within and among populations, whilst highlighting the potential for an aggregate nature of Ace-1 genotypes, which may comprise both single-copy and duplicated genes. Further work is now required to determine the distribution and resistance-association of Ace-1 duplication.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO: World malaria report. 2012, Geneva, Switzerland: World Health Organization WHO: World malaria report. 2012, Geneva, Switzerland: World Health Organization
2.
go back to reference WHO: Global action plan for insecticide resistance management in malaria vector (GPIRM). 2012, Geneva, Switzerland: World Health Organization WHO: Global action plan for insecticide resistance management in malaria vector (GPIRM). 2012, Geneva, Switzerland: World Health Organization
3.
go back to reference Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky NJ: Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013, 3619: 246-274.CrossRefPubMed Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky NJ: Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013, 3619: 246-274.CrossRefPubMed
4.
go back to reference Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V: Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control?. Trends Parasitol. 2011, 27: 91-98. 10.1016/j.pt.2010.08.004.CrossRefPubMed Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V: Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control?. Trends Parasitol. 2011, 27: 91-98. 10.1016/j.pt.2010.08.004.CrossRefPubMed
5.
go back to reference Martinez‒Torres D, Chandre F, Williamson MS, Darriet F, Berge 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. 10.1046/j.1365-2583.1998.72062.x.CrossRef Martinez‒Torres D, Chandre F, Williamson MS, Darriet F, Berge 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. 10.1046/j.1365-2583.1998.72062.x.CrossRef
6.
go back to reference 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. 10.1046/j.1365-2583.2000.00209.x.CrossRefPubMed 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. 10.1046/j.1365-2583.2000.00209.x.CrossRefPubMed
7.
go back to reference Jones CM, Toé HK, Sanou A, Namountougou M, Hughes A, Diabaté A, Dabiré R, Simard F, Ranson H: Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PloS One. 2012, 7: e45995-10.1371/journal.pone.0045995.PubMedCentralCrossRefPubMed Jones CM, Toé HK, Sanou A, Namountougou M, Hughes A, Diabaté A, Dabiré R, Simard F, Ranson H: Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PloS One. 2012, 7: e45995-10.1371/journal.pone.0045995.PubMedCentralCrossRefPubMed
8.
go back to reference Mitchell SN, Stevenson BJ, Müller P, Wilding CS, Egyir-Yawson A, Field SG, Hemingway J, Paine MJ, Ranson H, Donnelly MJ: Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci USA. 2012, 109: 6147-6152. 10.1073/pnas.1203452109.PubMedCentralCrossRefPubMed Mitchell SN, Stevenson BJ, Müller P, Wilding CS, Egyir-Yawson A, Field SG, Hemingway J, Paine MJ, Ranson H, Donnelly MJ: Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci USA. 2012, 109: 6147-6152. 10.1073/pnas.1203452109.PubMedCentralCrossRefPubMed
9.
go back to reference Akogbéto MC, Padonou GG, Gbénou D, Irish S, Yadouleton A: Bendiocarb, a potential alternative against pyrethroid resistant Anopheles gambiae in Benin, West Africa. Malar J. 2010, 9: 204-10.1186/1475-2875-9-204.PubMedCentralCrossRefPubMed Akogbéto MC, Padonou GG, Gbénou D, Irish S, Yadouleton A: Bendiocarb, a potential alternative against pyrethroid resistant Anopheles gambiae in Benin, West Africa. Malar J. 2010, 9: 204-10.1186/1475-2875-9-204.PubMedCentralCrossRefPubMed
10.
go back to reference 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: 52-10.1186/1475-2875-6-52.PubMedCentralCrossRefPubMed 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: 52-10.1186/1475-2875-6-52.PubMedCentralCrossRefPubMed
11.
go back to reference Akogbéto M, Padonou G, Bankolé H, Kindé Gazard D, Gbédjissi G: Dramatic decline of malaria transmission after implementation of large-scale Indoor Residual Spraying using bendiocarb in Bénin, West Africa, an area of high Anopheles gambiae resistance to pyrethroids. Am J Trop Med Hyg. 2011, 85: 586-593. 10.4269/ajtmh.2011.10-0668.PubMedCentralCrossRefPubMed Akogbéto M, Padonou G, Bankolé H, Kindé Gazard D, Gbédjissi G: Dramatic decline of malaria transmission after implementation of large-scale Indoor Residual Spraying using bendiocarb in Bénin, West Africa, an area of high Anopheles gambiae resistance to pyrethroids. Am J Trop Med Hyg. 2011, 85: 586-593. 10.4269/ajtmh.2011.10-0668.PubMedCentralCrossRefPubMed
12.
go back to reference Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, Rubahika D, Dissanayake G, Kamya MR, Scott F, Dorsey G: Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS ONE. 2012, 7: e42857-10.1371/journal.pone.0042857.PubMedCentralCrossRefPubMed Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, Rubahika D, Dissanayake G, Kamya MR, Scott F, Dorsey G: Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS ONE. 2012, 7: e42857-10.1371/journal.pone.0042857.PubMedCentralCrossRefPubMed
13.
go back to reference Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M: Comparative genomics: insecticide resistance in mosquito vectors. Nature. 2003, 423: 136-137.CrossRefPubMed Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M: Comparative genomics: insecticide resistance in mosquito vectors. Nature. 2003, 423: 136-137.CrossRefPubMed
14.
go back to reference Djogbénou L, Weill M, Hougard JM, Raymond M, Akogbeto M, Chandre F: Characterization of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance. J Med Entomol. 2007, 44: 805-810. 10.1603/0022-2585(2007)44[805:COIAAI]2.0.CO;2.PubMed Djogbénou L, Weill M, Hougard JM, Raymond M, Akogbeto M, Chandre F: Characterization of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance. J Med Entomol. 2007, 44: 805-810. 10.1603/0022-2585(2007)44[805:COIAAI]2.0.CO;2.PubMed
15.
go back to reference Ahoua Alou LP, Koffi AA, Adja MA, Tia E, Kouassi PK, Kone M, Chandre F: Distribution of ace-1R and resistance to carbamates and organophosphates in Anopheles gambiae s.s: populations from Côte d’Ivoire. Malar J. 2010, 9: 167-10.1186/1475-2875-9-167.PubMedCentralCrossRefPubMed Ahoua Alou LP, Koffi AA, Adja MA, Tia E, Kouassi PK, Kone M, Chandre F: Distribution of ace-1R and resistance to carbamates and organophosphates in Anopheles gambiae s.s: populations from Côte d’Ivoire. Malar J. 2010, 9: 167-10.1186/1475-2875-9-167.PubMedCentralCrossRefPubMed
16.
go back to reference Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H: Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis. 2012, 18: 1508-1511. 10.3201/eid1809.120262.PubMedCentralCrossRefPubMed Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H: Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d’Ivoire. Emerg Infect Dis. 2012, 18: 1508-1511. 10.3201/eid1809.120262.PubMedCentralCrossRefPubMed
17.
go back to reference Coetzee M, Van Wyk P, Booman M, Koekemoer LL, Hunt RH: Insecticide resistance in malaria vector mosquitoes in a gold mining town in Ghana and implications for malaria control. Bull Soc Path Exot. 2006, 99: 400-403. Coetzee M, Van Wyk P, Booman M, Koekemoer LL, Hunt RH: Insecticide resistance in malaria vector mosquitoes in a gold mining town in Ghana and implications for malaria control. Bull Soc Path Exot. 2006, 99: 400-403.
18.
go back to reference Adasi K, Hemingway J: Susceptibility to three pyrethroids and detection of knockdown resistance mutation in Ghanaian Anopheles gambiae sensu stricto. J Vector Ecol. 2008, 33: 255-262. 10.3376/1081-1710-33.2.255.CrossRefPubMed Adasi K, Hemingway J: Susceptibility to three pyrethroids and detection of knockdown resistance mutation in Ghanaian Anopheles gambiae sensu stricto. J Vector Ecol. 2008, 33: 255-262. 10.3376/1081-1710-33.2.255.CrossRefPubMed
19.
go back to reference Weetman D, Wilding CS, Steen K, Morgan JC, Simard F, Donnelly MJ: Association mapping of insecticide resistance in wild Anopheles gambiae populations: major variants identified in a low-linkage disequilbrium genome. PLoS One. 2010, 5: e13140-10.1371/journal.pone.0013140.PubMedCentralCrossRefPubMed Weetman D, Wilding CS, Steen K, Morgan JC, Simard F, Donnelly MJ: Association mapping of insecticide resistance in wild Anopheles gambiae populations: major variants identified in a low-linkage disequilbrium genome. PLoS One. 2010, 5: e13140-10.1371/journal.pone.0013140.PubMedCentralCrossRefPubMed
20.
go back to reference Hunt RH, Fuseini G, Knowles S, Stiles-Ocran J, Verster R, Kaiser ML, Choi KS, Koekemoer LL, Coetzee M: Insecticide resistance in malaria vector mosquitoes at four localities in Ghana, West Africa. Parasit Vectors. 2011, 4: 107-10.1186/1756-3305-4-107.PubMedCentralCrossRefPubMed Hunt RH, Fuseini G, Knowles S, Stiles-Ocran J, Verster R, Kaiser ML, Choi KS, Koekemoer LL, Coetzee M: Insecticide resistance in malaria vector mosquitoes at four localities in Ghana, West Africa. Parasit Vectors. 2011, 4: 107-10.1186/1756-3305-4-107.PubMedCentralCrossRefPubMed
21.
go back to reference Yawson AE, Weetman D, Wilson MD, Donnelly MJ: Ecological zones rather than molecular forms predict genetic differentiation in the malaria vector Anopheles gambiae s.s: in Ghana. Genetics. 2007, 175: 751-761. 10.1534/genetics.106.065888.PubMedCentralCrossRefPubMed Yawson AE, Weetman D, Wilson MD, Donnelly MJ: Ecological zones rather than molecular forms predict genetic differentiation in the malaria vector Anopheles gambiae s.s: in Ghana. Genetics. 2007, 175: 751-761. 10.1534/genetics.106.065888.PubMedCentralCrossRefPubMed
22.
go back to reference Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ: Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol. 2012, 29: 279-291. 10.1093/molbev/msr199.PubMedCentralCrossRefPubMed Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ: Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol. 2012, 29: 279-291. 10.1093/molbev/msr199.PubMedCentralCrossRefPubMed
23.
go back to reference Lynd A, Ranson H, McCall P, Randle N, Black W, Walker E, Donnelly M: A simplified high-throughput method for pyrethroid knock-down resistance (kdr) detection in Anopheles gambiae. Malar J. 2005, 4: 16-10.1186/1475-2875-4-16.PubMedCentralCrossRefPubMed Lynd A, Ranson H, McCall P, Randle N, Black W, Walker E, Donnelly M: A simplified high-throughput method for pyrethroid knock-down resistance (kdr) detection in Anopheles gambiae. Malar J. 2005, 4: 16-10.1186/1475-2875-4-16.PubMedCentralCrossRefPubMed
24.
go back to reference Yawson AE, McCall PJ, Wilson MD, Donnelly MJ: Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol. 2004, 18: 372-377. 10.1111/j.0269-283X.2004.00519.x.CrossRefPubMed Yawson AE, McCall PJ, Wilson MD, Donnelly MJ: Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol. 2004, 18: 372-377. 10.1111/j.0269-283X.2004.00519.x.CrossRefPubMed
25.
go back to reference WHO: Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. 2012, Geneva, Switzerland: World Health Organization WHO: Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. 2012, Geneva, Switzerland: World Health Organization
26.
go back to reference Abbott W: A method of computing the effectiveness of an insecticide. J Am Mosquito Contr Assoc. 1987, 3: 302-303. Abbott W: A method of computing the effectiveness of an insecticide. J Am Mosquito Contr Assoc. 1987, 3: 302-303.
27.
go back to reference Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993, 49: 520-529.PubMed Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993, 49: 520-529.PubMed
28.
go back to reference 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: 74-10.1186/1475-2875-7-74.PubMedCentralCrossRefPubMed 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: 74-10.1186/1475-2875-7-74.PubMedCentralCrossRefPubMed
29.
go back to reference Bass C, Nikou D, Vontas J, Williamson MS, Field LM: Development of high-throughput real-time PCR assays for the identification of insensitive acetylcholinesterase in Anopheles gambiae. Pest Biochem Physiol. 2010, 96: 80-85. 10.1016/j.pestbp.2009.09.004.CrossRef Bass C, Nikou D, Vontas J, Williamson MS, Field LM: Development of high-throughput real-time PCR assays for the identification of insensitive acetylcholinesterase in Anopheles gambiae. Pest Biochem Physiol. 2010, 96: 80-85. 10.1016/j.pestbp.2009.09.004.CrossRef
30.
go back to reference Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121.PubMedCentralCrossRefPubMed Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121.PubMedCentralCrossRefPubMed
32.
go back to reference Van de Peer Y: ZT: a software tool for simple and partial Mantel tests. J Stat Soft. 2002, 7: 1-12. Van de Peer Y: ZT: a software tool for simple and partial Mantel tests. J Stat Soft. 2002, 7: 1-12.
33.
go back to reference Ranson H, Abdallah H, Badlo A, Guelbeogo WM, Kerh-Hinzoumbé C, Yangalbé-Kalnoné E, Sagnon N, Simard F, Coetzee M: Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J. 2009, 8: 299-10.1186/1475-2875-8-299.PubMedCentralCrossRefPubMed Ranson H, Abdallah H, Badlo A, Guelbeogo WM, Kerh-Hinzoumbé C, Yangalbé-Kalnoné E, Sagnon N, Simard F, Coetzee M: Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J. 2009, 8: 299-10.1186/1475-2875-8-299.PubMedCentralCrossRefPubMed
34.
go back to reference Tallaki K: The pest control systems in the market gardens of Lomé, Togo. AGROPOLIS: the social, political and environmental dimensions of urban agriculture. Edited by: Mougeot LJA. 2005, London: IDRC, Earthscan, 51-67. Tallaki K: The pest control systems in the market gardens of Lomé, Togo. AGROPOLIS: the social, political and environmental dimensions of urban agriculture. Edited by: Mougeot LJA. 2005, London: IDRC, Earthscan, 51-67.
35.
go back to reference Klinkenberg E, McCall P, Wilson MD, Amerasinghe FP, Donnelly MJ: Impact of urban agriculture on malaria vectors in Accra, Ghana. Malar J. 2008, 7: 151-10.1186/1475-2875-7-151.PubMedCentralCrossRefPubMed Klinkenberg E, McCall P, Wilson MD, Amerasinghe FP, Donnelly MJ: Impact of urban agriculture on malaria vectors in Accra, Ghana. Malar J. 2008, 7: 151-10.1186/1475-2875-7-151.PubMedCentralCrossRefPubMed
36.
go back to reference Keiser J, Utzinger J, Castro MC, Smith TA, Tanner M, Singer BH: Urbanization in sub-Saharan Africa and implication for malaria control. Am J Trop Med Hyg. 2004, 71: 118-127.PubMed Keiser J, Utzinger J, Castro MC, Smith TA, Tanner M, Singer BH: Urbanization in sub-Saharan Africa and implication for malaria control. Am J Trop Med Hyg. 2004, 71: 118-127.PubMed
37.
go back to reference Asidi AN, N’Guessan R, Koffi AA, Curtis CF, Hougard JM, Chandre F, Corbel V, Darriet F, Zaim M, Rowland MW: 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: 25-10.1186/1475-2875-4-25.PubMedCentralCrossRefPubMed Asidi AN, N’Guessan R, Koffi AA, Curtis CF, Hougard JM, Chandre F, Corbel V, Darriet F, Zaim M, Rowland MW: 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: 25-10.1186/1475-2875-4-25.PubMedCentralCrossRefPubMed
38.
go back to reference Dabiré KR, Diabate A, Namontougou M, Djogbénou L, Kengne P, Simard F, Bass C, Baldet T: Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa). Trop Med Int Health. 2009, 14: 396-403. 10.1111/j.1365-3156.2009.02243.x.CrossRefPubMed Dabiré KR, Diabate A, Namontougou M, Djogbénou L, Kengne P, Simard F, Bass C, Baldet T: Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa). Trop Med Int Health. 2009, 14: 396-403. 10.1111/j.1365-3156.2009.02243.x.CrossRefPubMed
39.
go back to reference Lehmann T, Diabaté A: The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect Genet Evol. 2008, 8: 737-746. 10.1016/j.meegid.2008.06.003.PubMedCentralCrossRefPubMed Lehmann T, Diabaté A: The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect Genet Evol. 2008, 8: 737-746. 10.1016/j.meegid.2008.06.003.PubMedCentralCrossRefPubMed
40.
go back to reference Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing J, Fontenille D, Besansky NJ, Costantini C: Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecology. 2009, 9: 17-10.1186/1472-6785-9-17.PubMedCentralCrossRefPubMed Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing J, Fontenille D, Besansky NJ, Costantini C: Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecology. 2009, 9: 17-10.1186/1472-6785-9-17.PubMedCentralCrossRefPubMed
41.
go back to reference Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, Bassole IHN, Ose K, Fotsing J, Sagnon N, Fontenille D, Besansky NJ, Simard F: Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecology. 2009, 9: 16-10.1186/1472-6785-9-16.PubMedCentralCrossRefPubMed Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, Bassole IHN, Ose K, Fotsing J, Sagnon N, Fontenille D, Besansky NJ, Simard F: Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecology. 2009, 9: 16-10.1186/1472-6785-9-16.PubMedCentralCrossRefPubMed
42.
go back to reference Kamdem C, Fossog BT, Simard F, Etouna J, Ndo C, Kengne P, Boussès P, Etoa FX, Awono-Ambene P, Fontenille D, Antonio-Nkondjio C, Besansky NJ, Costantini C: Anthropogenic habitat disturbance and ecological divergence between incipient species of the malaria mosquito Anopheles gambiae. PLoS ONE. 2012, 7: e39453-10.1371/journal.pone.0039453.PubMedCentralCrossRefPubMed Kamdem C, Fossog BT, Simard F, Etouna J, Ndo C, Kengne P, Boussès P, Etoa FX, Awono-Ambene P, Fontenille D, Antonio-Nkondjio C, Besansky NJ, Costantini C: Anthropogenic habitat disturbance and ecological divergence between incipient species of the malaria mosquito Anopheles gambiae. PLoS ONE. 2012, 7: e39453-10.1371/journal.pone.0039453.PubMedCentralCrossRefPubMed
43.
go back to reference Djogbénou L, Chandre F, Berthomieu A, Dabiré R, Koffi A, Alout H, Weill M: Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s. s. PLoS ONE. 2008, 3: e2172-10.1371/journal.pone.0002172.PubMedCentralCrossRefPubMed Djogbénou L, Chandre F, Berthomieu A, Dabiré R, Koffi A, Alout H, Weill M: Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s. s. PLoS ONE. 2008, 3: e2172-10.1371/journal.pone.0002172.PubMedCentralCrossRefPubMed
44.
go back to reference Labbé P, Berthomieu A, Berticat C, Alout H, Raymond M, Lenormand T, Meill M: Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Mol Biol Evol. 2007, 24: 1056-1067. 10.1093/molbev/msm025.CrossRefPubMed Labbé P, Berthomieu A, Berticat C, Alout H, Raymond M, Lenormand T, Meill M: Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Mol Biol Evol. 2007, 24: 1056-1067. 10.1093/molbev/msm025.CrossRefPubMed
45.
go back to reference 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, 112/113: 287-296.CrossRef 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, 112/113: 287-296.CrossRef
46.
go back to reference Alout H, Djogbénou L, Berticat C, Chandre F, Weill M: Comparison of Anopheles gambiae and Culex pipiens acetycholinesterase 1 biochemical properties. Comp Biochem Physiol B. 2008, 150: 271-277. 10.1016/j.cbpb.2008.03.008.CrossRefPubMed Alout H, Djogbénou L, Berticat C, Chandre F, Weill M: Comparison of Anopheles gambiae and Culex pipiens acetycholinesterase 1 biochemical properties. Comp Biochem Physiol B. 2008, 150: 271-277. 10.1016/j.cbpb.2008.03.008.CrossRefPubMed
47.
go back to reference Weill M, Labbe’ P, Duron O, Pasteur N, Fort M, Raymond M: Insecticide resistance in the mosquito Culex pipiens: towards an understanding of the evolution of ace genes. Insect evolutionary ecology. Edited by: Fellowes MDE, Holloway GJ, Rolff J. 2005, Wallingford: CABI Publishing, 397-408. Weill M, Labbe’ P, Duron O, Pasteur N, Fort M, Raymond M: Insecticide resistance in the mosquito Culex pipiens: towards an understanding of the evolution of ace genes. Insect evolutionary ecology. Edited by: Fellowes MDE, Holloway GJ, Rolff J. 2005, Wallingford: CABI Publishing, 397-408.
48.
go back to reference Djogbénou 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: 12-10.1186/1475-2875-9-12.PubMedCentralCrossRefPubMed Djogbénou 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: 12-10.1186/1475-2875-9-12.PubMedCentralCrossRefPubMed
Metadata
Title
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
Authors
John Essandoh
Alexander E Yawson
David Weetman
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-404

Other articles of this Issue 1/2013

Malaria Journal 1/2013 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.