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Published in: Malaria Journal 1/2008

Open Access 01-12-2008 | Research

Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation

Authors: Cyrille Czeher, Rabiou Labbo, Ibrahim Arzika, Jean-Bernard Duchemin

Published in: Malaria Journal | Issue 1/2008

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Abstract

Background

At the end of 2005, a nationwide long-lasting insecticide-treated net (LLIN) distribution targeting the most vulnerable populations was implemented throughout Niger. A large number of studies in Africa have reported the existence of anopheline populations resistant to various insecticides, partly due to knockdown resistance (kdr) mutations, but few operational wide-scale control programmes were coupled with the monitoring of such mutations. The distribution of the kdr-west (kdr-w) Leu-Phe mutation was studied in Anopheles gambiae s.l. populations from Niger and temporal variations were monitored following the nationwide LLIN implementation.

Methods

Mosquitoes were collected from 14 localities during the wet seasons of 2005, 2006 and 2007 with additional sampling in the capital city, Niamey. After morphological identification of Anopheles gambiae s.l. specimens, DNA extracts were used for the determination of species and molecular forms of the Anopheles gambiae complex and for the detection of the kdr-w mutation.

Results

Around 1,500 specimens collected in the three consecutive years were analysed. All Anopheles arabiensis specimens analysed were homozygous susceptible, whereas the few Anopheles gambiae S forms exhibited a high overall kdr-w frequency. The M form samples exhibited a low overall kdr-w frequency before the LLIN distribution, that increased significantly in the two wet season collections following the LLIN distribution. Higher kdr frequencies were repeatedly noticed within host-seeking females compared to resting ones in indoor collections. In addition, preliminary results in M form urban populations from Niamey showed far higher kdr frequencies than in all of the rural sites studied.

Discussion

This study describes the first case of kdr mutation in Anopheles gambiae populations from Niger. It is suspected that the LLIN have caused the important temporal increase of kdr-w mutation observed during this study. While the kdr mutation is still found at a low level, this rapid increase could potentially lead to high kdr frequencies within a few years.

Conclusion

These results are of prime importance in the effort to document multiple effects of operational control programmes on mosquito vectors, and to conceive sustainable control strategies for future malaria control programmes.
Appendix
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Literature
1.
go back to reference Labbo R, Fouta A, Jeanne I, Ousmane I, Duchemin JB: Anopheles funestus in Sahel: new evidence from Niger. Lancet. 2004, 363: 660-10.1016/S0140-6736(04)15606-7.CrossRefPubMed Labbo R, Fouta A, Jeanne I, Ousmane I, Duchemin JB: Anopheles funestus in Sahel: new evidence from Niger. Lancet. 2004, 363: 660-10.1016/S0140-6736(04)15606-7.CrossRefPubMed
2.
go back to reference Czeher C, Labbo R, Djibrilla A, Here L, Arzika I, Duchemin JB: ELISA study of oocyst-sporozoite transition in malaria vectors. Parasite. 2006, 13: 257-261.CrossRefPubMed Czeher C, Labbo R, Djibrilla A, Here L, Arzika I, Duchemin JB: ELISA study of oocyst-sporozoite transition in malaria vectors. Parasite. 2006, 13: 257-261.CrossRefPubMed
3.
go back to reference Esnault C, Boulesteix M, Duchemin JB, Koffi AA, Chandre F, Dabiré R, Robert V, Simard F, Tripet F, Donnelly MJ, Fontenille D, Biémont C: High genetic differentiation between the M and S molecular forms of Anopheles gambiae in Africa. PLoS ONE. 2008, 3: e1968-10.1371/journal.pone.0001968.PubMedCentralCrossRefPubMed Esnault C, Boulesteix M, Duchemin JB, Koffi AA, Chandre F, Dabiré R, Robert V, Simard F, Tripet F, Donnelly MJ, Fontenille D, Biémont C: High genetic differentiation between the M and S molecular forms of Anopheles gambiae in Africa. PLoS ONE. 2008, 3: e1968-10.1371/journal.pone.0001968.PubMedCentralCrossRefPubMed
4.
go back to reference Loewenberg S: Niger welcomes largest bednet distribution in history. Lancet. 2006, 367: 1473-10.1016/S0140-6736(06)68630-3.CrossRefPubMed Loewenberg S: Niger welcomes largest bednet distribution in history. Lancet. 2006, 367: 1473-10.1016/S0140-6736(06)68630-3.CrossRefPubMed
5.
go back to reference Eisele TP, Lindblade KA, Wannemuehler KA, Gimnig JE, Odhiambo F, Hawley WA, Ter Kuile FO, Phillips-Howard P, Rosen DH, Nahlen BL, Vulule JM, Slutsker L: Effect of sustained insecticide-treated bed net use on all-cause child mortality in an area of intense perennial transmission in western Kenya. Am J Trop Med Hyg. 2005, 73: 149-156. Eisele TP, Lindblade KA, Wannemuehler KA, Gimnig JE, Odhiambo F, Hawley WA, Ter Kuile FO, Phillips-Howard P, Rosen DH, Nahlen BL, Vulule JM, Slutsker L: Effect of sustained insecticide-treated bed net use on all-cause child mortality in an area of intense perennial transmission in western Kenya. Am J Trop Med Hyg. 2005, 73: 149-156.
6.
go back to reference ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL: Impact of permethrin-treated bed nets on malaria and all-cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: cross-sectional survey. Am J Trop Med Hyg. 2003, 68: 100-107.PubMed ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL: Impact of permethrin-treated bed nets on malaria and all-cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: cross-sectional survey. Am J Trop Med Hyg. 2003, 68: 100-107.PubMed
7.
go back to reference Fegan GW, Noor AM, Akhwale WS, Cousens S, Snow RW: Effect of expanded insecticide-treated bednet coverage on child survival in rural Kenya: a longitudinal study. Lancet. 2007, 370: 1035-1039. 10.1016/S0140-6736(07)61477-9.PubMedCentralCrossRefPubMed Fegan GW, Noor AM, Akhwale WS, Cousens S, Snow RW: Effect of expanded insecticide-treated bednet coverage on child survival in rural Kenya: a longitudinal study. Lancet. 2007, 370: 1035-1039. 10.1016/S0140-6736(07)61477-9.PubMedCentralCrossRefPubMed
8.
go back to reference Schellenberg JR, Abdulla S, Nathan R, Mukasa O, Marchant TJ, Kikumbih N, Mushi AK, Mponda H, Minja H, Mshinda H, Tanner M, Lengeler C: Effect of large-scale social marketing of insecticide-treated nets on child survival in rural Tanzania. Lancet. 2001, 357: 1241-1247. 10.1016/S0140-6736(00)04404-4.CrossRefPubMed Schellenberg JR, Abdulla S, Nathan R, Mukasa O, Marchant TJ, Kikumbih N, Mushi AK, Mponda H, Minja H, Mshinda H, Tanner M, Lengeler C: Effect of large-scale social marketing of insecticide-treated nets on child survival in rural Tanzania. Lancet. 2001, 357: 1241-1247. 10.1016/S0140-6736(00)04404-4.CrossRefPubMed
9.
go back to reference Henry MC, Assi SB, Rogier C, Dossou-Yovo J, Chandre F, Guillet P, Carnevale P: Protective efficacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Côte d'Ivoire. Am J Trop Med Hyg. 2005, 73: 859-864.PubMed Henry MC, Assi SB, Rogier C, Dossou-Yovo J, Chandre F, Guillet P, Carnevale P: Protective efficacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Côte d'Ivoire. Am J Trop Med Hyg. 2005, 73: 859-864.PubMed
10.
go back to reference Thwing J, Hochberg N, Eng Vanden J, Issifi S, Eliades MJ, Minkoulou E, Wolkon A, Gado H, Ibrahim O, Newman RD, Lama M: Insecticide-treated net ownership and usage in Niger after a nationwide integrated campaign. Trop Med Int Health. 2008, 13: 827-834.CrossRefPubMed Thwing J, Hochberg N, Eng Vanden J, Issifi S, Eliades MJ, Minkoulou E, Wolkon A, Gado H, Ibrahim O, Newman RD, Lama M: Insecticide-treated net ownership and usage in Niger after a nationwide integrated campaign. Trop Med Int Health. 2008, 13: 827-834.CrossRefPubMed
11.
go back to reference Maxwell CA, Chambo W, Mwaimu M, Magogo F, Carneiro IA, Curtis CF: Variation of malaria transmission and morbidity with altitude in Tanzania and with introduction of alphacypermethrin treated nets. Malar J. 2003, 2: 28-10.1186/1475-2875-2-28.PubMedCentralCrossRefPubMed Maxwell CA, Chambo W, Mwaimu M, Magogo F, Carneiro IA, Curtis CF: Variation of malaria transmission and morbidity with altitude in Tanzania and with introduction of alphacypermethrin treated nets. Malar J. 2003, 2: 28-10.1186/1475-2875-2-28.PubMedCentralCrossRefPubMed
12.
go back to reference Soremekun S, Maxwell C, Zuwakuu M, Chen C, Michael E, Curtis C: Measuring the efficacy of insecticide treated bednets: the use of DNA fingerprinting to increase the accuracy of personal protection estimates in Tanzania. Trop Med Int Health. 2004, 9: 664-672. 10.1111/j.1365-3156.2004.01250.x.CrossRefPubMed Soremekun S, Maxwell C, Zuwakuu M, Chen C, Michael E, Curtis C: Measuring the efficacy of insecticide treated bednets: the use of DNA fingerprinting to increase the accuracy of personal protection estimates in Tanzania. Trop Med Int Health. 2004, 9: 664-672. 10.1111/j.1365-3156.2004.01250.x.CrossRefPubMed
13.
go back to reference Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, Ter Kuile FO, Vulule JM, Slutsker L: Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol. 2006, 43: 428-432. 10.1603/0022-2585(2006)043[0428:IOSUOI]2.0.CO;2.CrossRefPubMed Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, Ter Kuile FO, Vulule JM, Slutsker L: Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol. 2006, 43: 428-432. 10.1603/0022-2585(2006)043[0428:IOSUOI]2.0.CO;2.CrossRefPubMed
14.
go back to reference Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA: Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg. 2003, 68: 16-22.PubMed Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA: Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg. 2003, 68: 16-22.PubMed
15.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
16.
go back to reference Malima RC, Magesa SM, Tungu PK, Mwingira V, Magogo FS, Sudi W, Mosha FW, Curtis CF, Maxwell C, Rowland M: An experimental hut evaluation of Olyset nets against anopheline mosquitoes after seven years use in Tanzanian villages. Malar J. 2008, 7: 38-10.1186/1475-2875-7-38.PubMedCentralCrossRef Malima RC, Magesa SM, Tungu PK, Mwingira V, Magogo FS, Sudi W, Mosha FW, Curtis CF, Maxwell C, Rowland M: An experimental hut evaluation of Olyset nets against anopheline mosquitoes after seven years use in Tanzanian villages. Malar J. 2008, 7: 38-10.1186/1475-2875-7-38.PubMedCentralCrossRef
17.
go back to reference Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, Guillet P: Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ. 1999, 77: 230-234.PubMedCentralPubMed Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, Guillet P: Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ. 1999, 77: 230-234.PubMedCentralPubMed
18.
go back to reference Kolaczinski JH, Fanello C, Hervé JP, Conway DJ, Carnevale P, Curtis CF: Experimental and molecular genetic analysis of the impact of pyrethroid and non-pyrethroid insecticide impregnated bednets for mosquito control in an area of pyrethroid resistance. Bull Entomol Res. 2000, 90: 125-132.PubMed Kolaczinski JH, Fanello C, Hervé JP, Conway DJ, Carnevale P, Curtis CF: Experimental and molecular genetic analysis of the impact of pyrethroid and non-pyrethroid insecticide impregnated bednets for mosquito control in an area of pyrethroid resistance. Bull Entomol Res. 2000, 90: 125-132.PubMed
19.
go back to reference 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. 10.1016/j.actatropica.2007.01.005.CrossRefPubMed 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. 10.1016/j.actatropica.2007.01.005.CrossRefPubMed
20.
go back to reference 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. FrenchPubMed 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. FrenchPubMed
21.
go back to reference Chouaïbou M, Etang J, Brévault T, Nwane P, Hinzoumbé 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.CrossRefPubMed Chouaïbou M, Etang J, Brévault T, Nwane P, Hinzoumbé 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.CrossRefPubMed
22.
go back to reference Awolola TS, Oduola AO, Oyewole IO, Obansa JB, Amajoh CN, Koekemoer LL, Coetzee M: Dynamics of knockdown pyrethroid insecticide resistance alleles in a field population of Anopheles gambiae s.s. in southwestern Nigeria. J Vector Borne Dis. 2007, 44: 181-188.PubMed Awolola TS, Oduola AO, Oyewole IO, Obansa JB, Amajoh CN, Koekemoer LL, Coetzee M: Dynamics of knockdown pyrethroid insecticide resistance alleles in a field population of Anopheles gambiae s.s. in southwestern Nigeria. J Vector Borne Dis. 2007, 44: 181-188.PubMed
23.
go back to reference Kristan M, Fleischmann H, della Torre A, Stich A, 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. 10.1046/j.1365-2915.2003.00449.x.CrossRefPubMed Kristan M, Fleischmann H, della Torre A, Stich A, 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. 10.1046/j.1365-2915.2003.00449.x.CrossRefPubMed
24.
go back to reference Hemingway J, Hawkes NJ, McCarroll L, Ranson H: The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004, 34: 653-665. 10.1016/j.ibmb.2004.03.018.CrossRefPubMed Hemingway J, Hawkes NJ, McCarroll L, Ranson H: The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004, 34: 653-665. 10.1016/j.ibmb.2004.03.018.CrossRefPubMed
25.
go back to reference 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. 10.1046/j.1365-2583.1998.72062.x.CrossRefPubMed 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. 10.1046/j.1365-2583.1998.72062.x.CrossRefPubMed
26.
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
27.
go back to reference Awolola TS, Oyewole IO, Amajoh CN, Idowu ET, Ajayi MB, Oduola A, Manafa OU, Ibrahim K, Koekemoer LL, Coetzee M: Distribution of the molecular forms of Anopheles gambiae and pyrethroid knock down resistance gene in Nigeria. Acta Trop. 2005, 95: 204-209. 10.1016/j.actatropica.2005.06.002.CrossRef Awolola TS, Oyewole IO, Amajoh CN, Idowu ET, Ajayi MB, Oduola A, Manafa OU, Ibrahim K, Koekemoer LL, Coetzee M: Distribution of the molecular forms of Anopheles gambiae and pyrethroid knock down resistance gene in Nigeria. Acta Trop. 2005, 95: 204-209. 10.1016/j.actatropica.2005.06.002.CrossRef
28.
go back to reference 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.PubMed 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.PubMed
29.
go back to reference Diabate A, Baldet T, Chandre F, Akoobeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM: The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg. 2002, 67: 617-622.PubMed Diabate A, Baldet T, Chandre F, Akoobeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM: The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg. 2002, 67: 617-622.PubMed
30.
go back to reference Diabate A, Baldet T, Chandre F, Guiguemdé RT, Brengues C, Guillet P, Hemingway J, Hougard JM: First report of the kdr mutation in Anopheles gambiae M form from Burkina Faso, west Africa. Parassitologia. 2002, 44: 157-158.PubMed Diabate A, Baldet T, Chandre F, Guiguemdé RT, Brengues C, Guillet P, Hemingway J, Hougard JM: First report of the kdr mutation in Anopheles gambiae M form from Burkina Faso, west Africa. Parassitologia. 2002, 44: 157-158.PubMed
31.
go back to reference Diabate A, Baldet T, Chandre C, Dabire KR, Kengne P, Guiguemde TR, Simard F, Guillet P, Hemingway J, Hougard JM: KDR mutation, a genetic marker to assess events of introgression between the molecular M and S forms of Anopheles gambiae (Diptera: Culicidae) in the tropical savannah area of West Africa. J Med Entomol. 2003, 40: 195-198.CrossRefPubMed Diabate A, Baldet T, Chandre C, Dabire KR, Kengne P, Guiguemde TR, Simard F, Guillet P, Hemingway J, Hougard JM: KDR mutation, a genetic marker to assess events of introgression between the molecular M and S forms of Anopheles gambiae (Diptera: Culicidae) in the tropical savannah area of West Africa. J Med Entomol. 2003, 40: 195-198.CrossRefPubMed
32.
go back to reference 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. 10.1111/j.1365-3156.2004.01336.x.CrossRefPubMed 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. 10.1111/j.1365-3156.2004.01336.x.CrossRefPubMed
33.
go back to reference Fanello C, Petrarca V, della Torre A, Santolamazza F, Dolo G, Coulibaly M, Alloueche A, Curtis CF, Touré YT, Coluzzi M: The pyrethroid knock-down resistance gene in the Anopheles gambiae complex in Mali and further indication of incipient speciation within An. gambiae s.s. Insect Mol Biol. 2003, 12: 241-245. 10.1046/j.1365-2583.2003.00407.x.CrossRefPubMed Fanello C, Petrarca V, della Torre A, Santolamazza F, Dolo G, Coulibaly M, Alloueche A, Curtis CF, Touré YT, Coluzzi M: The pyrethroid knock-down resistance gene in the Anopheles gambiae complex in Mali and further indication of incipient speciation within An. gambiae s.s. Insect Mol Biol. 2003, 12: 241-245. 10.1046/j.1365-2583.2003.00407.x.CrossRefPubMed
34.
go back to reference 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. Am J Trop Med Hyg. 2007, 76: 81-87.PubMed 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. Am J Trop Med Hyg. 2007, 76: 81-87.PubMed
35.
go back to reference Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, Guillet P, Raymond M: The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol. 2000, 9: 451-455. 10.1046/j.1365-2583.2000.00206.x.CrossRefPubMed Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, Guillet P, Raymond M: The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol. 2000, 9: 451-455. 10.1046/j.1365-2583.2000.00206.x.CrossRefPubMed
36.
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
37.
go back to reference 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. Am J Trop Med Hyg. 2006, 74 (5): 795-797.PubMed 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. Am J Trop Med Hyg. 2006, 74 (5): 795-797.PubMed
38.
go back to reference Reimer L, Fondjo E, Patchoké S, Diallo B, Lee Y, Ng A, Ndjemai HM, Atangana J, Traore SF, Lanzaro G, Cornel AJ: Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae. J Med Entomol. 2008, 45: 260-266. 10.1603/0022-2585(2008)45[260:RBKMAR]2.0.CO;2.CrossRefPubMed Reimer L, Fondjo E, Patchoké S, Diallo B, Lee Y, Ng A, Ndjemai HM, Atangana J, Traore SF, Lanzaro G, Cornel AJ: Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae. J Med Entomol. 2008, 45: 260-266. 10.1603/0022-2585(2008)45[260:RBKMAR]2.0.CO;2.CrossRefPubMed
39.
go back to reference Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C, Gentile G, Caccone A, do Rosário VE: 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. 2006, 20: 27-32. 10.1111/j.1365-2915.2006.00611.x.CrossRefPubMed Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C, Gentile G, Caccone A, do Rosário VE: 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. 2006, 20: 27-32. 10.1111/j.1365-2915.2006.00611.x.CrossRefPubMed
40.
go back to reference Pinto J, Lynd A, Vicente JL, Santolamazza F, Randle NP, Gentile G, Moreno M, Simard F, Charlwood JD, do Rosário VE, Caccone A, Della Torre A, Donnelly MJ: Multiple origins of knockdown resistance mutations in the afrotropical mosquito vector Anopheles gambiae. PLoS ONE. 2007, 2: e1243-10.1371/journal.pone.0001243.PubMedCentralCrossRefPubMed Pinto J, Lynd A, Vicente JL, Santolamazza F, Randle NP, Gentile G, Moreno M, Simard F, Charlwood JD, do Rosário VE, Caccone A, Della Torre A, Donnelly MJ: Multiple origins of knockdown resistance mutations in the afrotropical mosquito vector Anopheles gambiae. PLoS ONE. 2007, 2: e1243-10.1371/journal.pone.0001243.PubMedCentralCrossRefPubMed
41.
go back to reference 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. 10.1111/j.1365-2583.2005.00599.x.CrossRefPubMed 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. 10.1111/j.1365-2583.2005.00599.x.CrossRefPubMed
42.
go back to reference Tripet F, Wright J, Lanzaro G: A new high-performance PCR diagnostic for the detection of pyrethroid knockdown resistance kdr in Anopheles gambiae. Am J Trop Med Hyg. 2006, 74: 658-662.PubMed Tripet F, Wright J, Lanzaro G: A new high-performance PCR diagnostic for the detection of pyrethroid knockdown resistance kdr in Anopheles gambiae. Am J Trop Med Hyg. 2006, 74: 658-662.PubMed
43.
go back to reference Girod R, Orlandi-Pradines E, Rogier C, Pages F: Malaria transmission and insecticide resistance of Anopheles gambiae (Diptera: Culicidae) in the French military camp of Port-Bouët, Abidjan (Côte d'Ivoire): implications for vector control. J Med Entomol. 2006, 43: 1082-1087. 10.1603/0022-2585(2006)43[1082:MTAIRO]2.0.CO;2.PubMed Girod R, Orlandi-Pradines E, Rogier C, Pages F: Malaria transmission and insecticide resistance of Anopheles gambiae (Diptera: Culicidae) in the French military camp of Port-Bouët, Abidjan (Côte d'Ivoire): implications for vector control. J Med Entomol. 2006, 43: 1082-1087. 10.1603/0022-2585(2006)43[1082:MTAIRO]2.0.CO;2.PubMed
44.
go back to reference Akogbéto MC, Djouaka RF, Kindé-Gazard DA: Screening of pesticide residues in soil and water samples from agricultural settings. Malar J. 2006, 5: 22-10.1186/1475-2875-5-22.PubMedCentralCrossRefPubMed Akogbéto MC, Djouaka RF, Kindé-Gazard DA: Screening of pesticide residues in soil and water samples from agricultural settings. Malar J. 2006, 5: 22-10.1186/1475-2875-5-22.PubMedCentralCrossRefPubMed
45.
go back to reference Corbel V, Chandre F, Brengues C, Akogbéto M, Lardeux F, Hougard JM, Guillet P: Dosage-dependent effects of permethrin-treated nets on the behaviour of Anopheles gambiae and the selection of pyrethroid resistance. Malar J. 2004, 3: 22-10.1186/1475-2875-3-22.PubMedCentralCrossRefPubMed Corbel V, Chandre F, Brengues C, Akogbéto M, Lardeux F, Hougard JM, Guillet P: Dosage-dependent effects of permethrin-treated nets on the behaviour of Anopheles gambiae and the selection of pyrethroid resistance. Malar J. 2004, 3: 22-10.1186/1475-2875-3-22.PubMedCentralCrossRefPubMed
46.
go back to reference Moreno M, Vicente JL, Cano J, Berzosa PJ, de Lucio A, Nzambo S, Bobuakasi L, Buatiche JN, Ondo M, Micha F, Do Rosario VE, Pinto J, Benito A: Knockdown resistance mutations (kdr) and insecticide susceptibility to DDT and pyrethroids in Anopheles gambiae from Equatorial Guinea. Trop Med Int Health. 2008, 13: 430-433.CrossRefPubMed Moreno M, Vicente JL, Cano J, Berzosa PJ, de Lucio A, Nzambo S, Bobuakasi L, Buatiche JN, Ondo M, Micha F, Do Rosario VE, Pinto J, Benito A: Knockdown resistance mutations (kdr) and insecticide susceptibility to DDT and pyrethroids in Anopheles gambiae from Equatorial Guinea. Trop Med Int Health. 2008, 13: 430-433.CrossRefPubMed
47.
go back to reference Janeira F, Vicente JL, Kanganje Y, Moreno M, Do Rosário VE, Cravo P, Pinto J: A primer-introduced restriction analysis-polymerase chain reaction method to detect knockdown resistance mutations in Anopheles gambiae. J Med Entomol. 2008, 45: 237-241. 10.1603/0022-2585(2008)45[237:APRACR]2.0.CO;2.CrossRefPubMed Janeira F, Vicente JL, Kanganje Y, Moreno M, Do Rosário VE, Cravo P, Pinto J: A primer-introduced restriction analysis-polymerase chain reaction method to detect knockdown resistance mutations in Anopheles gambiae. J Med Entomol. 2008, 45: 237-241. 10.1603/0022-2585(2008)45[237:APRACR]2.0.CO;2.CrossRefPubMed
48.
go back to reference Verhaeghen K, Van Bortel W, Roelants P, Backeljau T, Coosemans M: Detection of the East and West African kdr mutation in Anopheles gambiae and Anopheles arabiensis from Uganda using a new assay based on FRET/Melt Curve analysis. Malar J. 2006, 5: 16-10.1186/1475-2875-5-16.PubMedCentralCrossRefPubMed Verhaeghen K, Van Bortel W, Roelants P, Backeljau T, Coosemans M: Detection of the East and West African kdr mutation in Anopheles gambiae and Anopheles arabiensis from Uganda using a new assay based on FRET/Melt Curve analysis. Malar J. 2006, 5: 16-10.1186/1475-2875-5-16.PubMedCentralCrossRefPubMed
49.
go back to reference Kulkarni MA, Rowland M, Alifrangis M, Mosha FW, Matowo J, Malima R, Peter J, Kweka E, Lyimo I, Magesa S, Salanti A, Rau ME, Drakeley C: Occurrence of the leucine-to-phenylalanine knockdown resistance (kdr) mutation in Anopheles arabiensis populations in Tanzania, detected by a simplified high-throughput SSOP-ELISA method. Malar J. 2006, 5: 56-10.1186/1475-2875-5-56.PubMedCentralCrossRefPubMed Kulkarni MA, Rowland M, Alifrangis M, Mosha FW, Matowo J, Malima R, Peter J, Kweka E, Lyimo I, Magesa S, Salanti A, Rau ME, Drakeley C: Occurrence of the leucine-to-phenylalanine knockdown resistance (kdr) mutation in Anopheles arabiensis populations in Tanzania, detected by a simplified high-throughput SSOP-ELISA method. Malar J. 2006, 5: 56-10.1186/1475-2875-5-56.PubMedCentralCrossRefPubMed
50.
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
51.
go back to reference Kelly-Hope L, Ranson H, Hemingway J: Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis. 2008, 8: 387-389. 10.1016/S1473-3099(08)70045-8.CrossRefPubMed Kelly-Hope L, Ranson H, Hemingway J: Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis. 2008, 8: 387-389. 10.1016/S1473-3099(08)70045-8.CrossRefPubMed
52.
go back to reference WHO: Tests procedures for insecticide resistance monitoring in malaria vectors, bioefficacy and persistence of insecticides on treated surfaces. Report of the WHO Informal Consultation, WHO/MAL/98.12. Geneva. 43- WHO: Tests procedures for insecticide resistance monitoring in malaria vectors, bioefficacy and persistence of insecticides on treated surfaces. Report of the WHO Informal Consultation, WHO/MAL/98.12. Geneva. 43-
53.
go back to reference Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P: Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Med Vet Entomol. 2000, 14: 81-88. 10.1046/j.1365-2915.2000.00212.x.CrossRefPubMed Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P: Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Med Vet Entomol. 2000, 14: 81-88. 10.1046/j.1365-2915.2000.00212.x.CrossRefPubMed
54.
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
55.
go back to reference 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. 10.1111/j.1365-2915.1996.tb00084.x.CrossRefPubMed 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. 10.1111/j.1365-2915.1996.tb00084.x.CrossRefPubMed
56.
go back to reference Kulkarni MA, Malima R, Mosha FW, Msangi S, Mrema E, Kabula B, Lawrence B, Kinung'hi S, Swilla J, Kisinza W, Rau ME, Miller JE, Schellenberg JA, Maxwell C, Rowland M, Magesa S, Drakeley C: 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.CrossRefPubMed Kulkarni MA, Malima R, Mosha FW, Msangi S, Mrema E, Kabula B, Lawrence B, Kinung'hi S, Swilla J, Kisinza W, Rau ME, Miller JE, Schellenberg JA, Maxwell C, Rowland M, Magesa S, Drakeley C: 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.CrossRefPubMed
57.
go back to reference 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. Am J Trop Med Hyg. 2004, 70: 591-596.PubMed 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. Am J Trop Med Hyg. 2004, 70: 591-596.PubMed
58.
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
59.
go back to reference Santolamazza F, Della Torre A, Caccone A: Short report: A new polymerase chain reaction-restriction fragment length polymorphism method to identify Anopheles arabiensis from An. gambiae and its two molecular forms from degraded DNA templates or museum samples. Am J Trop Med Hyg. 2004, 70: 604-606.PubMed Santolamazza F, Della Torre A, Caccone A: Short report: A new polymerase chain reaction-restriction fragment length polymorphism method to identify Anopheles arabiensis from An. gambiae and its two molecular forms from degraded DNA templates or museum samples. Am J Trop Med Hyg. 2004, 70: 604-606.PubMed
60.
go back to reference Guo SW, Thompson EA: Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics. 1992, 48: 361-372. 10.2307/2532296.CrossRefPubMed Guo SW, Thompson EA: Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics. 1992, 48: 361-372. 10.2307/2532296.CrossRefPubMed
61.
go back to reference Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online. 2005, 1: 47-50.PubMedCentral Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online. 2005, 1: 47-50.PubMedCentral
62.
go back to reference Dean AG, Sullivan KM, Soe MM: OpenEpi: Open Source Epidemiologic Statistics for Public Health. via the Internet, updated 2008/04/06, accessed 2008/04/29, [http://www.openepi.com] Dean AG, Sullivan KM, Soe MM: OpenEpi: Open Source Epidemiologic Statistics for Public Health. via the Internet, updated 2008/04/06, accessed 2008/04/29, [http://​www.​openepi.​com]
63.
go back to reference Matambo TS, Abdalla H, Brooke BD, Koekemoer LL, Mnzava A, Hunt RH, Coetzee M: Insecticide resistance in the malarial mosquito Anopheles arabiensis and association with the kdr mutation. Med Vet Entomol. 2007, 21: 97-102. 10.1111/j.1365-2915.2007.00671.x.CrossRefPubMed Matambo TS, Abdalla H, Brooke BD, Koekemoer LL, Mnzava A, Hunt RH, Coetzee M: Insecticide resistance in the malarial mosquito Anopheles arabiensis and association with the kdr mutation. Med Vet Entomol. 2007, 21: 97-102. 10.1111/j.1365-2915.2007.00671.x.CrossRefPubMed
65.
go back to reference Berzosa PJ, Cano J, Roche J, Rubio JM, García L, Moyano E, Guerra A, Mateos JC, Petrarca V, Rosario VD, Benito A: Malaria vectors in Bioko Island (Equatorial Guinea): PCR determination of the members of Anopheles gambiae Giles complex (Diptera: Culicidae) and pyrethroid knockdown resistance (kdr) in An. gambiae sensu stricto. J Vector Ecol. 2002, 27: 102-106.PubMed Berzosa PJ, Cano J, Roche J, Rubio JM, García L, Moyano E, Guerra A, Mateos JC, Petrarca V, Rosario VD, Benito A: Malaria vectors in Bioko Island (Equatorial Guinea): PCR determination of the members of Anopheles gambiae Giles complex (Diptera: Culicidae) and pyrethroid knockdown resistance (kdr) in An. gambiae sensu stricto. J Vector Ecol. 2002, 27: 102-106.PubMed
Metadata
Title
Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation
Authors
Cyrille Czeher
Rabiou Labbo
Ibrahim Arzika
Jean-Bernard Duchemin
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2008
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-7-189

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