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Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Evidence of a multiple insecticide resistance in the malaria vector Anopheles funestus in South West Nigeria

Authors: Rousseau J. Djouaka, Seun M. Atoyebi, Genevieve M. Tchigossou, Jacob M. Riveron, Helen Irving, Romaric Akoton, Michael O. Kusimo, Adekunle A. Bakare, Charles S. Wondji

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

Knowing the extent and spread of insecticide resistance in malaria vectors is vital to successfully manage insecticide resistance in Africa. This information in the main malaria vector, Anopheles funestus sensu stricto, is completely lacking in the most populous country in Africa, Nigeria. This study reports the insecticide susceptibility status and the molecular basis of resistance of An. funestus as well as its involvement in malaria transmission in Akaka-Remo, a farm settlement village in southwest Nigeria.

Results

Plasmodium infection analysis using TaqMan protocol coupled with a nested PCR revealed an infection rate of 8% in An. funestus s.s. from Akaka-Remo. WHO susceptibility tests showed this species has developed multiple resistance to insecticides in the study area. Anopheles funestus s.s. population in Akaka-Remo is highly resistant to organochlorines: dieldrin (8%) and DDT (10%). Resistance was also observed against pyrethroids: permethrin (68%) and deltamethrin (87%), and the carbamate bendiocarb (84%). Mortality rate with DDT slightly increased (from 10 to 30%, n = 45) after PBO pre-exposure indicating that cytochrome P450s play little role in DDT resistance while high mortalities were recorded after PBO pre-exposure with permethrin (from 68 to 100%, n = 70) and dieldrin (from 8 to 100%, n = 48) suggesting the implication of P450s in the observed permethrin and dieldrin resistance. High frequencies of resistant allele, 119F in F0 (77%) and F1 (80% in resistant and 72% in susceptible) populations with an odd ratio of 1.56 (P = 0.1859) show that L119F-GSTe2 mutation is almost fixed in the population. Genotyping of the A296S-RDL mutation in both F0 and F1 samples shows an association with dieldrin resistance with an odd ratio of 81 (P < 0.0001) (allelic frequency (R) = 76% for F0; for F1, 90 and 10% were observed in resistant and susceptible populations, respectively) as this mutation is not yet fixed in the population.

Conclusion

The study reports multiple insecticide resistance in An. funestus from Akaka Remo. It is, therefore, necessary to pay more attention to this major malaria vector for effective malaria control in Nigeria.
Literature
1.
go back to reference CDC. Malaria Operational Plan FY. President’s Initiative in Nigeria. 2015. CDC. Malaria Operational Plan FY. President’s Initiative in Nigeria. 2015.
2.
go back to reference World Health Organization. World malaria report. Geneva: World Health Organization; 2016. World Health Organization. World malaria report. Geneva: World Health Organization; 2016.
3.
go back to reference CDC. Malaria Operational Plan FY. President’s Initiative in Nigeria. 2016. CDC. Malaria Operational Plan FY. President’s Initiative in Nigeria. 2016.
4.
go back to reference Oyewole IO, Ibidapo CA, Oduola AO, Obansa JB, Awolola TS. Anthropophilic mosquitoes and malaria transmission in a tropical rain forest area of Nigeria. J Life Phys Sci. 2005;2:6–10. Oyewole IO, Ibidapo CA, Oduola AO, Obansa JB, Awolola TS. Anthropophilic mosquitoes and malaria transmission in a tropical rain forest area of Nigeria. J Life Phys Sci. 2005;2:6–10.
5.
go back to reference Awolola TS, Oyewole IO, Koekemoer LL, Coetzee M. Identification of three members of the Anopheles funestus (Diptera: Culicidae) group and their role in malaria transmission in two ecological zones in Nigeria. Trans R Soc Trop Med Hyg. 2005;99:525–31.CrossRefPubMed Awolola TS, Oyewole IO, Koekemoer LL, Coetzee M. Identification of three members of the Anopheles funestus (Diptera: Culicidae) group and their role in malaria transmission in two ecological zones in Nigeria. Trans R Soc Trop Med Hyg. 2005;99:525–31.CrossRefPubMed
6.
go back to reference Oyewole IO, Awolola TS. Impact of urbanisation on bionomics and distribution of malaria vectors in Lagos, southwestern Nigeria. J Vector Borne Dis. 2006;43:173–8.PubMed Oyewole IO, Awolola TS. Impact of urbanisation on bionomics and distribution of malaria vectors in Lagos, southwestern Nigeria. J Vector Borne Dis. 2006;43:173–8.PubMed
7.
go back to reference Okwa O, Rasheed A, Adeyemi A, Omoyeni M, Oni L, Fayemi A, et al. Anopheles species abundances, composition and vectoral competence in six areas of Lagos: Nigeria. J Cell Anim Biol. 2007;1:19–23. Okwa O, Rasheed A, Adeyemi A, Omoyeni M, Oni L, Fayemi A, et al. Anopheles species abundances, composition and vectoral competence in six areas of Lagos: Nigeria. J Cell Anim Biol. 2007;1:19–23.
8.
go back to reference Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J, et al. 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 Genom. 2008;9:538.CrossRef Djouaka RF, Bakare AA, Coulibaly ON, Akogbeto MC, Ranson H, Hemingway J, et al. 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 Genom. 2008;9:538.CrossRef
9.
go back to reference Oduola AO, Olojede JB, Ashiegbu CO, Olufemi A, Otubanjo OA, Awolola TS. High level of DDT resistance in the malaria mosquito: Anopheles gambiae s.l. from rural, semi urban and urban communities in Nigeria. J Rural Trop Public Health. 2010;9:114–20. Oduola AO, Olojede JB, Ashiegbu CO, Olufemi A, Otubanjo OA, Awolola TS. High level of DDT resistance in the malaria mosquito: Anopheles gambiae s.l. from rural, semi urban and urban communities in Nigeria. J Rural Trop Public Health. 2010;9:114–20.
10.
go back to reference Oduola AO, Idowu ET, Oyebola MK, Adeogun AA, Olojede JB, Otubanjo OA, et al. Evidence of carbamate resistance in urban populations of Anopheles gambiae s.s. mosquitoes resistant to DDT and deltamethrin insecticides in Lagos. Int Pest Control. 2012;54:206. Oduola AO, Idowu ET, Oyebola MK, Adeogun AA, Olojede JB, Otubanjo OA, et al. Evidence of carbamate resistance in urban populations of Anopheles gambiae s.s. mosquitoes resistant to DDT and deltamethrin insecticides in Lagos. Int Pest Control. 2012;54:206.
11.
go back to reference Ibrahim KT, Popoola KO, Adewuyi OR. Susceptibility of Anopheles gambiae sensu lato (Diptera:Culicidae) to permethrin, deltamethrin and bendiocarb in Ibadan City, Southwest Nigeria. Curr Res J Biol Sci. 2013;5:42–8. Ibrahim KT, Popoola KO, Adewuyi OR. Susceptibility of Anopheles gambiae sensu lato (Diptera:Culicidae) to permethrin, deltamethrin and bendiocarb in Ibadan City, Southwest Nigeria. Curr Res J Biol Sci. 2013;5:42–8.
12.
go back to reference Mulamba C, Riveron JM, Ibrahim SS, Irving H, Barnes KG, Mukwaya LG, et al. Widespread pyrethroid and DDT resistance in the major malaria vector Anopheles funestus in East Africa is driven by metabolic resistance mechanisms. PLoS ONE. 2014;9:e110058.CrossRefPubMedPubMedCentral Mulamba C, Riveron JM, Ibrahim SS, Irving H, Barnes KG, Mukwaya LG, et al. Widespread pyrethroid and DDT resistance in the major malaria vector Anopheles funestus in East Africa is driven by metabolic resistance mechanisms. PLoS ONE. 2014;9:e110058.CrossRefPubMedPubMedCentral
13.
go back to reference Amenya DA, Naguran R, Lo T-CM, Ranson H, Spillings BL, Wood OR, et al. Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles funestus, resistant to pyrethroids. Insect Mol Biol. 2008;17:19–25.CrossRefPubMed Amenya DA, Naguran R, Lo T-CM, Ranson H, Spillings BL, Wood OR, et al. Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles funestus, resistant to pyrethroids. Insect Mol Biol. 2008;17:19–25.CrossRefPubMed
14.
go back to reference Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, et al. Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci USA. 2012;109:19063–70.CrossRefPubMedPubMedCentral Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, et al. Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci USA. 2012;109:19063–70.CrossRefPubMedPubMedCentral
15.
go back to reference Vezenegho SB, Chiphwanya J, Hunt RH, Coetzee M, Bass C, Koekemoer LL. Characterization of the Anopheles funestus group, including Anopheles funestus-like, from Northern Malawi. Trans R Soc Trop Med Hyg. 2013;107:753–62.CrossRefPubMed Vezenegho SB, Chiphwanya J, Hunt RH, Coetzee M, Bass C, Koekemoer LL. Characterization of the Anopheles funestus group, including Anopheles funestus-like, from Northern Malawi. Trans R Soc Trop Med Hyg. 2013;107:753–62.CrossRefPubMed
16.
go back to reference Choi KS, Christian R, Nardini L, Wood OR, Agubuzo E, Muleba M, et al. Insecticide resistance and role in malaria transmission of Anopheles funestus populations from Zambia and Zimbabwe. Parasit Vectors. 2014;7:464.CrossRefPubMedPubMedCentral Choi KS, Christian R, Nardini L, Wood OR, Agubuzo E, Muleba M, et al. Insecticide resistance and role in malaria transmission of Anopheles funestus populations from Zambia and Zimbabwe. Parasit Vectors. 2014;7:464.CrossRefPubMedPubMedCentral
17.
go back to reference Riveron JM, Chiumia M, Menze BD, Barnes KG, Irving H, Ibrahim SS, et al. Rise of multiple insecticide resistance in Anopheles funestus in Malawi: a major concern for malaria vector control. Malar J. 2015;14:344.CrossRefPubMedPubMedCentral Riveron JM, Chiumia M, Menze BD, Barnes KG, Irving H, Ibrahim SS, et al. Rise of multiple insecticide resistance in Anopheles funestus in Malawi: a major concern for malaria vector control. Malar J. 2015;14:344.CrossRefPubMedPubMedCentral
18.
go back to reference Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol. 2000;14:181–9.CrossRefPubMed Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol. 2000;14:181–9.CrossRefPubMed
19.
go back to reference Casimiro S, Coleman M, Mohloai P, Hemingway J, Sharp B. Insecticide resistance in Anopheles funestus (Diptera: Culicidae) from Mozambique. J Med Entomol. 2006;43:267–75.CrossRefPubMed Casimiro S, Coleman M, Mohloai P, Hemingway J, Sharp B. Insecticide resistance in Anopheles funestus (Diptera: Culicidae) from Mozambique. J Med Entomol. 2006;43:267–75.CrossRefPubMed
20.
go back to reference Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R, Morgan JC. Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochem Mol Biol. 2011;41:484–91.CrossRefPubMedPubMedCentral Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R, Morgan JC. Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochem Mol Biol. 2011;41:484–91.CrossRefPubMedPubMedCentral
21.
go back to reference Menze BD, Riveron JM, Ibrahim SS, Irving H, Antonio-Nkondjio C, Awono-Ambene PH, et al. Multiple insecticide resistance in the malaria vector Anopheles funestus from Northern Cameroon is mediated by metabolic resistance alongside potential target site insensitivity mutations. PLoS ONE. 2016;11:e163261.CrossRef Menze BD, Riveron JM, Ibrahim SS, Irving H, Antonio-Nkondjio C, Awono-Ambene PH, et al. Multiple insecticide resistance in the malaria vector Anopheles funestus from Northern Cameroon is mediated by metabolic resistance alongside potential target site insensitivity mutations. PLoS ONE. 2016;11:e163261.CrossRef
22.
go back to reference Djouaka R, Irving H, Tukur Z, Wondji CS. Exploring mechanisms of multiple insecticide resistance in a population of the malaria vector Anopheles funestus in Benin. PLoS ONE. 2011;6:e27760.CrossRefPubMedPubMedCentral Djouaka R, Irving H, Tukur Z, Wondji CS. Exploring mechanisms of multiple insecticide resistance in a population of the malaria vector Anopheles funestus in Benin. PLoS ONE. 2011;6:e27760.CrossRefPubMedPubMedCentral
23.
go back to reference Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M. Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg. 2008;102:591–8.CrossRefPubMed Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M. Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg. 2008;102:591–8.CrossRefPubMed
24.
go back to reference Dabiré KR, Baldet T, Diabaté A, Dia I, Costantini C, Cohuet A, et al. Anopheles funestus (Diptera: Culicidae) in a humid savannah area of western Burkina Faso: bionomics, insecticide resistance status, and role in malaria transmission. J Med Entomol. 2007;44:990–7.CrossRefPubMed Dabiré KR, Baldet T, Diabaté A, Dia I, Costantini C, Cohuet A, et al. Anopheles funestus (Diptera: Culicidae) in a humid savannah area of western Burkina Faso: bionomics, insecticide resistance status, and role in malaria transmission. J Med Entomol. 2007;44:990–7.CrossRefPubMed
25.
go back to reference Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS. High level of pyrethroid resistance in an Anopheles funestus population of the chokwe district in Mozambique. PLoS ONE. 2010;5:e11010.CrossRefPubMedPubMedCentral Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS. High level of pyrethroid resistance in an Anopheles funestus population of the chokwe district in Mozambique. PLoS ONE. 2010;5:e11010.CrossRefPubMedPubMedCentral
26.
go back to reference Djouaka R, Riveron JM, Yessoufou A, Tchigossou G, Akoton R, Irving H, et al. Multiple insecticide resistance in an infected population of the malaria vector Anopheles funestus in Benin. Parasit Vectors. 2016;9:453.CrossRefPubMedPubMedCentral Djouaka R, Riveron JM, Yessoufou A, Tchigossou G, Akoton R, Irving H, et al. Multiple insecticide resistance in an infected population of the malaria vector Anopheles funestus in Benin. Parasit Vectors. 2016;9:453.CrossRefPubMedPubMedCentral
27.
go back to reference Riveron JM, Yunta C, Ibrahim SS, Djouaka R, Irving H, Menze BD, et al. A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector. Genome Biol. 2014;15:27.CrossRef Riveron JM, Yunta C, Ibrahim SS, Djouaka R, Irving H, Menze BD, et al. A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector. Genome Biol. 2014;15:27.CrossRef
28.
go back to reference Ibrahim SS, Ndula M, Riveron JM, Irving H, Wondji CS. The P450 CYP6Z1 confers carbamate/pyrethroid cross- resistance in a major African malaria vector beside a novel carbamate-insensitive N485I acetylcholinesterase-1 mutation. Mol Ecol. 2016;25:3436–52.CrossRefPubMedPubMedCentral Ibrahim SS, Ndula M, Riveron JM, Irving H, Wondji CS. The P450 CYP6Z1 confers carbamate/pyrethroid cross- resistance in a major African malaria vector beside a novel carbamate-insensitive N485I acetylcholinesterase-1 mutation. Mol Ecol. 2016;25:3436–52.CrossRefPubMedPubMedCentral
29.
go back to reference Edi CV, Djogbénou L, Jenkins AM, Regna K, Muskavitch MAT, Poupardin R, et al. CYP6 P450 enzymes and ACE-1 duplication produce extreme and multiple insecticide resistance in the malaria mosquito Anopheles gambiae. PLoS Genet. 2014;10:e1004236.CrossRefPubMedPubMedCentral Edi CV, Djogbénou L, Jenkins AM, Regna K, Muskavitch MAT, Poupardin R, et al. CYP6 P450 enzymes and ACE-1 duplication produce extreme and multiple insecticide resistance in the malaria mosquito Anopheles gambiae. PLoS Genet. 2014;10:e1004236.CrossRefPubMedPubMedCentral
30.
31.
go back to reference Gillies MT, Coetzee M. A Supplement to the Anophelinae of Africa South of the Sahara. Publ South African Inst Med Res. 1987;55:63. Gillies MT, Coetzee M. A Supplement to the Anophelinae of Africa South of the Sahara. Publ South African Inst Med Res. 1987;55:63.
32.
go back to reference Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.PubMed Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.PubMed
33.
go back to reference Livak KJ. Organization and mapping of a sequence on the Drosopila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics. 1984;107:611–34.PubMedPubMedCentral Livak KJ. Organization and mapping of a sequence on the Drosopila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics. 1984;107:611–34.PubMedPubMedCentral
34.
go back to reference Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, Williamson MS, et al. PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J. 2008;7:177.CrossRefPubMedPubMedCentral Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, Williamson MS, et al. PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J. 2008;7:177.CrossRefPubMedPubMedCentral
35.
go back to reference Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong SBK. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20.CrossRefPubMed Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong SBK. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20.CrossRefPubMed
36.
go back to reference WHO. Informal consultation report. Geneva: World Health Organization; 1998. WHO. Informal consultation report. Geneva: World Health Organization; 1998.
37.
go back to reference WHO. World malaria report. Geneva: World Health Organization; 2013. WHO. World malaria report. Geneva: World Health Organization; 2013.
40.
go back to reference Costantini C, Sagnon N, Ilboudo-Sanogo E, Coluzzi M, Boccolini D. Chromosomal and bionomic heterogeneities suggest incipient speciation in Anopheles funestus from Burkina Faso. Parassitologia. 1999;41:595–611.PubMed Costantini C, Sagnon N, Ilboudo-Sanogo E, Coluzzi M, Boccolini D. Chromosomal and bionomic heterogeneities suggest incipient speciation in Anopheles funestus from Burkina Faso. Parassitologia. 1999;41:595–611.PubMed
41.
go back to reference Sandeu MM, Moussiliou A, Moiroux N, Padonou GG, Massougbodji A, Corbel V, et al. Optimized Pan-species and speciation duplex real-time PCR assays for Plasmodium parasites detection in malaria vectors. PLoS ONE. 2012;7:e52719.CrossRefPubMedPubMedCentral Sandeu MM, Moussiliou A, Moiroux N, Padonou GG, Massougbodji A, Corbel V, et al. Optimized Pan-species and speciation duplex real-time PCR assays for Plasmodium parasites detection in malaria vectors. PLoS ONE. 2012;7:e52719.CrossRefPubMedPubMedCentral
42.
go back to reference Riveron JM, Osae M, Egyir-Yawson A, Irving H, Ibrahim SS, Wondji CS. Multiple insecticide resistance in the major malaria vector Anopheles funestus in southern Ghana: implications for malaria control. Parasit Vectors. 2016;9:504.CrossRefPubMedPubMedCentral Riveron JM, Osae M, Egyir-Yawson A, Irving H, Ibrahim SS, Wondji CS. Multiple insecticide resistance in the major malaria vector Anopheles funestus in southern Ghana: implications for malaria control. Parasit Vectors. 2016;9:504.CrossRefPubMedPubMedCentral
43.
go back to reference Oyewole IO, Ibidapo CA, Okwa OO, Oduola AO, Adeoye GO, Okoh HI, et al. Species composition and role of Anopheles mosquitoes in malaria transmission along Badagry Axis of Lagos Lagoon, Lagos, Nigeria. Int J Insect Sci. 2010;2:51–7.CrossRef Oyewole IO, Ibidapo CA, Okwa OO, Oduola AO, Adeoye GO, Okoh HI, et al. Species composition and role of Anopheles mosquitoes in malaria transmission along Badagry Axis of Lagos Lagoon, Lagos, Nigeria. Int J Insect Sci. 2010;2:51–7.CrossRef
44.
go back to reference Ogen O. The agricultural sector and Nigeria’s development: comparative perspectives from the Brazilian Agro-Industrial Economy, 1960–1995; 2007. p. 184–94. Ogen O. The agricultural sector and Nigeria’s development: comparative perspectives from the Brazilian Agro-Industrial Economy, 1960–1995; 2007. p. 184–94.
45.
go back to reference Oil Boom Era (1971–1977). 2003. Accessed 18 Nov 2016. Oil Boom Era (1971–1977). 2003. Accessed 18 Nov 2016.
46.
go back to reference Farm irrigation system and system Design fundamentals. p. 61–109. Farm irrigation system and system Design fundamentals. p. 61–109.
47.
go back to reference Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.CrossRefPubMedPubMedCentral Reid MC, McKenzie FE. The contribution of agricultural insecticide use to increasing insecticide resistance in African malaria vectors. Malar J. 2016;15:107.CrossRefPubMedPubMedCentral
48.
go back to reference NAFDAC. Guidelines for Registration of Imported Drug Products in Nigeria, National Agency for Food and Drug Administration and Control; 2004. p 1–7. NAFDAC. Guidelines for Registration of Imported Drug Products in Nigeria, National Agency for Food and Drug Administration and Control; 2004. p 1–7.
49.
50.
go back to reference Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, Awono-Ambene P, et al. Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaoundé (Cameroon): influence of urban agriculture and pollution. Malar J. 2011;10:154.CrossRefPubMedPubMedCentral Antonio-Nkondjio C, Fossog BT, Ndo C, Djantio BM, Togouet SZ, Awono-Ambene P, et al. Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaoundé (Cameroon): influence of urban agriculture and pollution. Malar J. 2011;10:154.CrossRefPubMedPubMedCentral
51.
go back to reference Tene Fossog B, Kopya E, Ndo C, Menze-Djantio B, Costantini C, Njiokou F, et al. Water quality and Anopheles gambiae larval tolerance to pyrethroids in the cities of Douala and Yaounde (Cameroon). J Trop Med. 2012;2012. Tene Fossog B, Kopya E, Ndo C, Menze-Djantio B, Costantini C, Njiokou F, et al. Water quality and Anopheles gambiae larval tolerance to pyrethroids in the cities of Douala and Yaounde (Cameroon). J Trop Med. 2012;2012.
52.
go back to reference Philbert A, Lyantagaye SL, Nkwengulila G. A review of agricultural pesticides use and the selection for resistance to insecticides in malaria vectors. Adv Entomol. 2014;120–8. Philbert A, Lyantagaye SL, Nkwengulila G. A review of agricultural pesticides use and the selection for resistance to insecticides in malaria vectors. Adv Entomol. 2014;120–8.
53.
go back to reference Djouaka RF, Bakare AA, Bankole HS, Doannio JM, Coulibaly ON, Kossou H, et al. Does the spillage of petroleum products in Anopheles breeding sites have an impact on the pyrethroid resistance? Malar J. 2007;6:159.CrossRefPubMedPubMedCentral Djouaka RF, Bakare AA, Bankole HS, Doannio JM, Coulibaly ON, Kossou H, et al. Does the spillage of petroleum products in Anopheles breeding sites have an impact on the pyrethroid resistance? Malar J. 2007;6:159.CrossRefPubMedPubMedCentral
54.
go back to reference Chanda E, Hemingway J, Kleinschmidt I, Rehman AM, Ramdeen V, Phiri FN, et al. Insecticide resistance and the future of malaria control in Zambia. PLoS ONE. 2011;6:e24336.CrossRefPubMedPubMedCentral Chanda E, Hemingway J, Kleinschmidt I, Rehman AM, Ramdeen V, Phiri FN, et al. Insecticide resistance and the future of malaria control in Zambia. PLoS ONE. 2011;6:e24336.CrossRefPubMedPubMedCentral
55.
go back to reference Okorie PN, Ademowo GO, Irving H, Kelly-Hope LA, Wondji CS. Insecticide susceptibility of Anopheles coluzzii and Anopheles gambiae mosquitoes in Ibadan South–West Nigeria. Med Vet Entomol. 2015;29:44–50.CrossRefPubMed Okorie PN, Ademowo GO, Irving H, Kelly-Hope LA, Wondji CS. Insecticide susceptibility of Anopheles coluzzii and Anopheles gambiae mosquitoes in Ibadan South–West Nigeria. Med Vet Entomol. 2015;29:44–50.CrossRefPubMed
Metadata
Title
Evidence of a multiple insecticide resistance in the malaria vector Anopheles funestus in South West Nigeria
Authors
Rousseau J. Djouaka
Seun M. Atoyebi
Genevieve M. Tchigossou
Jacob M. Riveron
Helen Irving
Romaric Akoton
Michael O. Kusimo
Adekunle A. Bakare
Charles S. Wondji
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1615-9

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