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Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Insecticide resistance in Anopheles arabiensis populations from Dakar and its suburbs: role of target site and metabolic resistance mechanisms

Authors: A. Kane Dia, O. Kalsom Guèye, E. Amadou Niang, S. Mocote Diédhiou, M. Demba Sy, Abdoulaye Konaté, Badara Samb, Abdoulaye Diop, Lassana Konaté, Ousmane Faye

Published in: Malaria Journal | Issue 1/2018

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Abstract

Background

Urban malaria is an increasing concern in most of the sub-Saharan Africa countries. In Dakar, the capital city of Senegal, the malaria epidemiology has been complicated by recurrent flooding since 2005. The main vector control measure for malaria prevention in Dakar is the community use of long-lasting insecticide-treated nets. However, the increase of insecticide resistance reported in this area needs to be better understood for suitable resistance management. This study reports the situation of insecticide resistance and underlying mechanisms in Anopheles arabiensis populations from Dakar and its suburbs.

Results

All the populations tested showed resistance to almost all insecticides except organophosphates families, which remain the only lethal molecules. Piperonil butoxide (PBO) and ethacrinic acid (EA) the two synergists used, have respectively and significantly restored the susceptibility to DDT and permethrin of Anopheles population. Molecular identification of specimens revealed the presence of An. arabiensis only. Kdr genotyping showed the presence of the L1014F mutation (kdr-West) as well as L1014S (kdr-East). This L1014S mutation was found at very high frequencies (89.53%) in almost all districts surveyed, and in association with the L1014F (10.24%).

Conclusion

Results showed the contribution of both target-site and metabolic mechanisms in conferring pyrethroid resistance to An. arabiensis from the flooded areas of Dakar suburbs. These data, although preliminary, stress the need for close monitoring of the urban An. arabiensis populations for a suitable insecticide resistance management system to preserve core insecticide-based vector control tools in this flooded area.
Literature
1.
go back to reference WHO. Global plan for insecticide management. Geneva: World Health Organization; 2012. WHO. Global plan for insecticide management. Geneva: World Health Organization; 2012.
2.
go back to reference Diedhiou SM, Niang EA, Doucoure S, Samb B, Konate A, Cissokho S, et al. Distribution and characterization of anopheline larval habitats in flooded areas of the Dakar suburbs. J Parasitol Vector Biol. 2016;8:61–73. Diedhiou SM, Niang EA, Doucoure S, Samb B, Konate A, Cissokho S, et al. Distribution and characterization of anopheline larval habitats in flooded areas of the Dakar suburbs. J Parasitol Vector Biol. 2016;8:61–73.
3.
go back to reference Diédhiou SM, Konaté L, Doucouré S, Samb B, Niang EA, Sy O, et al. Efficacité de trois larvicides d’origine biologique et d’un régulateur de croissance contre Anopheles arabiensis au Sénégal. Bull Soc Path Exot. 2017;110:102–15.CrossRef Diédhiou SM, Konaté L, Doucouré S, Samb B, Niang EA, Sy O, et al. Efficacité de trois larvicides d’origine biologique et d’un régulateur de croissance contre Anopheles arabiensis au Sénégal. Bull Soc Path Exot. 2017;110:102–15.CrossRef
4.
go back to reference Machault V, Gadiaga L, Vignolles C, Jarjaval F, Bouzid S, Sokhna C, et al. Highly focused anopheline breeding sites and malaria transmission in Dakar. Malar J. 2009;8:138.CrossRefPubMedPubMedCentral Machault V, Gadiaga L, Vignolles C, Jarjaval F, Bouzid S, Sokhna C, et al. Highly focused anopheline breeding sites and malaria transmission in Dakar. Malar J. 2009;8:138.CrossRefPubMedPubMedCentral
5.
go back to reference Machault V, Vignolles C, Pages F, Gadiaga L, Gaye A, Sokhna C, et al. Spatial heterogeneity and temporal evolution of malaria transmission risk in Dakar, Senegal, according to remotely sensed environmental data. Malar J. 2010;9:252.CrossRefPubMedPubMedCentral Machault V, Vignolles C, Pages F, Gadiaga L, Gaye A, Sokhna C, et al. Spatial heterogeneity and temporal evolution of malaria transmission risk in Dakar, Senegal, according to remotely sensed environmental data. Malar J. 2010;9:252.CrossRefPubMedPubMedCentral
6.
go back to reference Gadiaga L, Machault V, Pagès F, Gaye A, Jarjaval F, Godefroy L, et al. Conditions of malaria transmission in Dakar from 2007 to 2010. Malar J. 2011;10:312.CrossRefPubMedPubMedCentral Gadiaga L, Machault V, Pagès F, Gaye A, Jarjaval F, Godefroy L, et al. Conditions of malaria transmission in Dakar from 2007 to 2010. Malar J. 2011;10:312.CrossRefPubMedPubMedCentral
8.
go back to reference PNLP. Plan stratégique national de lutte contre le paludisme au Sénégal 2016–2020. Programme National de Lutte contre le Paludisme (PNLP) Ministère de la Santé et de Prévention Médicale. 2015. p. 171. PNLP. Plan stratégique national de lutte contre le paludisme au Sénégal 2016–2020. Programme National de Lutte contre le Paludisme (PNLP) Ministère de la Santé et de Prévention Médicale. 2015. p. 171.
10.
go back to reference Faye O, Konate L, Diop A. Profil entomologique du paludisme au Sénégal. Ministére la Santé la Prévention Médicale. 2011. p. 39. Faye O, Konate L, Diop A. Profil entomologique du paludisme au Sénégal. Ministére la Santé la Prévention Médicale. 2011. p. 39.
12.
go back to reference ANSD. Recencement Général de la Population et de l’Habitat, de l’Agriculture et de l’Elevage RGPHAE 2013. Agence Nationale de la Statistique et de la Démographie (ANSD), Ministère de l’Economie et des Finances. 2014. p. 418. ANSD. Recencement Général de la Population et de l’Habitat, de l’Agriculture et de l’Elevage RGPHAE 2013. Agence Nationale de la Statistique et de la Démographie (ANSD), Ministère de l’Economie et des Finances. 2014. p. 418.
13.
go back to reference MR4. Method in Anopheles research. 4th ed. New York: CABI Publishing; 2014. MR4. Method in Anopheles research. 4th ed. New York: CABI Publishing; 2014.
14.
go back to reference WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2013. WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. Geneva: World Health Organization; 2013.
15.
go back to reference Brogdon WG, McAllister JC. Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. J Am Mosq Control Assoc. 1998;14:159–64.PubMed Brogdon WG, McAllister JC. Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. J Am Mosq Control Assoc. 1998;14:159–64.PubMed
16.
go back to reference Wilkins EE, Howell PI, Benedict MQ. IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malar J. 2006;7:1–7. Wilkins EE, Howell PI, Benedict MQ. IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malar J. 2006;7:1–7.
17.
go back to reference Huynh LY, Sandve SR, Hannan LM, Van Ert M, Gimnig JE. Fitness costs of pyrethroidinsecticide resistance in Anopheles gambiae. Annual Meeting of the Society for the Study of Evolution, Christchurch, New Zealand. 2007. Huynh LY, Sandve SR, Hannan LM, Van Ert M, Gimnig JE. Fitness costs of pyrethroidinsecticide resistance in Anopheles gambiae. Annual Meeting of the Society for the Study of Evolution, Christchurch, New Zealand. 2007.
19.
go back to reference Machault V, Vignolles C, Pagès F, Gadiaga L, Tourre YM, Gaye A, et al. Risk mapping of Anopheles gambiae s.l. densities using remotely-rensed environmental and meteorological data in an urban area: Dakar, Senegal. PLoS ONE. 2012;7:e50674.CrossRefPubMedPubMedCentral Machault V, Vignolles C, Pagès F, Gadiaga L, Tourre YM, Gaye A, et al. Risk mapping of Anopheles gambiae s.l. densities using remotely-rensed environmental and meteorological data in an urban area: Dakar, Senegal. PLoS ONE. 2012;7:e50674.CrossRefPubMedPubMedCentral
20.
go back to reference Pagès F, Texier G, Pradines B, Gadiaga L, Machault V, Jarjaval F, Penhoat K, Berger F, Trape JF, Rogier C, Sokhna C. Malaria transmission in Dakar: a two-year survey. Malar J. 2008;7(1):178.CrossRefPubMedPubMedCentral Pagès F, Texier G, Pradines B, Gadiaga L, Machault V, Jarjaval F, Penhoat K, Berger F, Trape JF, Rogier C, Sokhna C. Malaria transmission in Dakar: a two-year survey. Malar J. 2008;7(1):178.CrossRefPubMedPubMedCentral
21.
go back to reference Robert V, Awono-Ambene HP, Thioulouse J. Ecology of larval mosquitoes, with special reference to Anopheles arabiensis (Diptera: Culcidae) in market-garden wells in urban Dakar, Senegal. J Med Entomol. 1998;35:948–55.CrossRefPubMed Robert V, Awono-Ambene HP, Thioulouse J. Ecology of larval mosquitoes, with special reference to Anopheles arabiensis (Diptera: Culcidae) in market-garden wells in urban Dakar, Senegal. J Med Entomol. 1998;35:948–55.CrossRefPubMed
22.
go back to reference Vercruysse J, Jancloes M. Etude entomologique sur la transmission du paludisme humain dans la zone urbaine de Pikine (Sénégal). Cah ORSTOM Série Entomol Méd Parasitol. 1981;19:165–78. Vercruysse J, Jancloes M. Etude entomologique sur la transmission du paludisme humain dans la zone urbaine de Pikine (Sénégal). Cah ORSTOM Série Entomol Méd Parasitol. 1981;19:165–78.
23.
go back to reference Faye O, Gaye O, Diallo S. Evaluation de la sensibilité d’Anopheles gambiae s.l au Fénitrothion au Malathion et au DDT au Sénégal. Dakar Médical. 1991;36:170–7.PubMed Faye O, Gaye O, Diallo S. Evaluation de la sensibilité d’Anopheles gambiae s.l au Fénitrothion au Malathion et au DDT au Sénégal. Dakar Médical. 1991;36:170–7.PubMed
24.
go back to reference Cissé I, Fall ST, Badiane M, Diop Y, Diouf A. Horticulture et usage des pesticides dans la zone des Niayes au Sénégal, document de travail Ecocité n°8. ISRA/LNERV, EISMV, LACT/Faculté de Médecine Pharmacie/UCAD. 2006. p. 14. Cissé I, Fall ST, Badiane M, Diop Y, Diouf A. Horticulture et usage des pesticides dans la zone des Niayes au Sénégal, document de travail Ecocité n°8. ISRA/LNERV, EISMV, LACT/Faculté de Médecine Pharmacie/UCAD. 2006. p. 14.
25.
go back to reference Niang EHA, Konaté L, Diallo M, Faye O, Dia I. Patterns of insecticide resistance and knock down resistance (kdr) in malaria vectors An. arabiensis, An. coluzzii and An. gambiae from sympatric areas in Senegal. Parasit Vectors. 2016;9:71.CrossRefPubMedCentral Niang EHA, Konaté L, Diallo M, Faye O, Dia I. Patterns of insecticide resistance and knock down resistance (kdr) in malaria vectors An. arabiensis, An. coluzzii and An. gambiae from sympatric areas in Senegal. Parasit Vectors. 2016;9:71.CrossRefPubMedCentral
26.
go back to reference Faye O, Gaye O, Fontenille D, Hebrard G, Konate L, Sy N, et al. La sécheresse et la baisse du paludisme dans les Niayes du Sénégal. Cahier Santé. 1995;5:299–305. Faye O, Gaye O, Fontenille D, Hebrard G, Konate L, Sy N, et al. La sécheresse et la baisse du paludisme dans les Niayes du Sénégal. Cahier Santé. 1995;5:299–305.
27.
go back to reference Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, et al. 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;67:617–22.CrossRefPubMed Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, et al. 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;67:617–22.CrossRefPubMed
28.
go back to reference Padonou G, Sezonlin M, Ossé R, Aizoun N, Oké-Agbo F, Oussou O, et al. Impact of three years of large scale indoor residual spraying (IRS) and insecticide treated nets (ITNs) interventions on insecticide resistance in Anopheles gambiae s.l. in Benin. Parasit Vectors. 2012;5:72.CrossRefPubMedPubMedCentral Padonou G, Sezonlin M, Ossé R, Aizoun N, Oké-Agbo F, Oussou O, et al. Impact of three years of large scale indoor residual spraying (IRS) and insecticide treated nets (ITNs) interventions on insecticide resistance in Anopheles gambiae s.l. in Benin. Parasit Vectors. 2012;5:72.CrossRefPubMedPubMedCentral
29.
go back to reference Soderlund DM, Knipple DC. The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochem Mol Biol. 2003;33:563–77.CrossRefPubMed Soderlund DM, Knipple DC. The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochem Mol Biol. 2003;33:563–77.CrossRefPubMed
30.
go back to reference Lynd A, Weetman D, Barbosa S, Yawson AE, Mitchell S, Pinto J, et al. Field, genetic, and modeling approaches show strong positive selection acting upon an insecticide resistance mutation in Anopheles gambiae s.s. Mol Biol Evol. 2010;27:1117–25.CrossRefPubMedPubMedCentral Lynd A, Weetman D, Barbosa S, Yawson AE, Mitchell S, Pinto J, et al. Field, genetic, and modeling approaches show strong positive selection acting upon an insecticide resistance mutation in Anopheles gambiae s.s. Mol Biol Evol. 2010;27:1117–25.CrossRefPubMedPubMedCentral
31.
go back to reference Dabiré RK, Namountougou M, Diabaté A, Soma DD, Bado J, Toé HK, et al. Distribution and frequency of kdr mutations within Anopheles gambiae s.l. populations and first report of the ace.1 G119S mutation in Anopheles arabiensis from Burkina Faso (West Africa). PLoS ONE. 2014;9:e101484.CrossRefPubMedPubMedCentral Dabiré RK, Namountougou M, Diabaté A, Soma DD, Bado J, Toé HK, et al. Distribution and frequency of kdr mutations within Anopheles gambiae s.l. populations and first report of the ace.1 G119S mutation in Anopheles arabiensis from Burkina Faso (West Africa). PLoS ONE. 2014;9:e101484.CrossRefPubMedPubMedCentral
32.
go back to reference Kabula B, Kisinza W, Tungu P, Ndege C, Batengana B, Kollo D, et al. Co-occurrence and distribution of East (L1014S) and West (L1014F) African knock-down resistance in Anopheles gambiae sensu lato population of Tanzania. Trop Med Int Health. 2014;19:331–41.CrossRefPubMed Kabula B, Kisinza W, Tungu P, Ndege C, Batengana B, Kollo D, et al. Co-occurrence and distribution of East (L1014S) and West (L1014F) African knock-down resistance in Anopheles gambiae sensu lato population of Tanzania. Trop Med Int Health. 2014;19:331–41.CrossRefPubMed
33.
go back to reference Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P, et al. First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg. 2006;74:795–7.PubMed Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P, et al. First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg. 2006;74:795–7.PubMed
34.
go back to reference Nwane P, Etang J, Chouaїbou M, Toto JC, Mimpfoundi R, Simard F. Kdr-based insecticide resistance in Anopheles gambiae ss populations in Cameroon: spread of the L1014F and L1014S mutations. BMC Res Notes. 2011;4(1):463.CrossRefPubMedPubMedCentral Nwane P, Etang J, Chouaїbou M, Toto JC, Mimpfoundi R, Simard F. Kdr-based insecticide resistance in Anopheles gambiae ss populations in Cameroon: spread of the L1014F and L1014S mutations. BMC Res Notes. 2011;4(1):463.CrossRefPubMedPubMedCentral
35.
go back to reference Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C. 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;3652600:27–32.CrossRef Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C. 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;3652600:27–32.CrossRef
36.
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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
37.
go back to reference Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, et al. Insecticide resistance in mosquito vectors. Nature. 2003;423:137–8.CrossRef Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, et al. Insecticide resistance in mosquito vectors. Nature. 2003;423:137–8.CrossRef
38.
go back to reference Thiaw O. Evaluation de la sensibilité aux insecticides par la technique des tests de bio-essais en bouteille du CDC et détermination des mécanismes de résistance chez An. gambiae s.l. dans la ville de Dakar, Sénégal. Université Cheikh Anta Diop; 2014. Thiaw O. Evaluation de la sensibilité aux insecticides par la technique des tests de bio-essais en bouteille du CDC et détermination des mécanismes de résistance chez An. gambiae s.l. dans la ville de Dakar, Sénégal. Université Cheikh Anta Diop; 2014.
39.
go back to reference Djègbè I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, et al. Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J. 2011;10:261.CrossRefPubMedPubMedCentral Djègbè I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, et al. Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J. 2011;10:261.CrossRefPubMedPubMedCentral
40.
go back to reference Aïzoun N, Aïkpon R, Padonou GG, Oussou O, Oké-Agbo F, Gnanguenon V, et al. Mixed-function oxidases and esterases associated with permethrin, deltamethrin and bendiocarb resistance in Anopheles gambiae s.l. in the south-north transect Benin, West Africa. Parasit Vectors. 2013;6:223.CrossRefPubMedPubMedCentral Aïzoun N, Aïkpon R, Padonou GG, Oussou O, Oké-Agbo F, Gnanguenon V, et al. Mixed-function oxidases and esterases associated with permethrin, deltamethrin and bendiocarb resistance in Anopheles gambiae s.l. in the south-north transect Benin, West Africa. Parasit Vectors. 2013;6:223.CrossRefPubMedPubMedCentral
41.
go back to reference Nwane P, Etang J, Chouaїbou M, Toto JC, Koffi A, Mimpfoundi R, et al. Multiple insecticide resistance mechanisms in Anopheles gambiae s.l. populations from Cameroon, Central Africa. Parasit Vectors. 2013;6:41.CrossRefPubMedPubMedCentral Nwane P, Etang J, Chouaїbou M, Toto JC, Koffi A, Mimpfoundi R, et al. Multiple insecticide resistance mechanisms in Anopheles gambiae s.l. populations from Cameroon, Central Africa. Parasit Vectors. 2013;6:41.CrossRefPubMedPubMedCentral
Metadata
Title
Insecticide resistance in Anopheles arabiensis populations from Dakar and its suburbs: role of target site and metabolic resistance mechanisms
Authors
A. Kane Dia
O. Kalsom Guèye
E. Amadou Niang
S. Mocote Diédhiou
M. Demba Sy
Abdoulaye Konaté
Badara Samb
Abdoulaye Diop
Lassana Konaté
Ousmane Faye
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2269-6

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