Evidence of a Multiple Insecticide Resistance in the Malaria Vector Anopheles Funestus in South West Nigeria

Overview

Journal Malar J

Publisher Biomed Central

Specialty Tropical Medicine

Date 2016 Nov 24

PMID 27876039

Citations 31

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

Affiliations

Soon will be listed here.

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 F (77%) and F (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 F and F samples shows an association with dieldrin resistance with an odd ratio of 81 (P < 0.0001) (allelic frequency (R) = 76% for F; for F, 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.

Citing Articles

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Low frequency of knockdown resistance mutation (L1014F) and the efficacy of PBO synergist in multiple insecticide-resistant populations of Anopheles gambiae in Ikorodu, Lagos State, Nigeria.

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Multi-centre discriminating concentration determination of broflanilide and potential for cross-resistance to other public health insecticides in Anopheles vector populations.

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References

Antonio-Nkondjio C, Fossog B, Ndo C, Menze Djantio B, Togouet S, Awono-Ambene P . 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. PMC: 3118161. DOI: 10.1186/1475-2875-10-154. View

Sandeu M, Moussiliou A, Moiroux N, Padonou G, Massougbodji A, Corbel V . Optimized Pan-species and speciation duplex real-time PCR assays for Plasmodium parasites detection in malaria vectors. PLoS One. 2013; 7(12):e52719. PMC: 3532469. DOI: 10.1371/journal.pone.0052719. View

Mulamba C, Riveron J, Ibrahim S, Irving H, Barnes K, Mukwaya L . 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(10):e110058. PMC: 4198208. DOI: 10.1371/journal.pone.0110058. View

Djouaka R, Bakare A, Coulibaly O, Akogbeto M, Ranson H, Hemingway J . Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics. 2008; 9:538. PMC: 2588609. DOI: 10.1186/1471-2164-9-538. View

Ibrahim S, Ndula M, Riveron J, Irving H, Wondji C . 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(14):3436-52. PMC: 4950264. DOI: 10.1111/mec.13673. View

Edi C, Djogbenou L, Jenkins A, Regna K, Muskavitch M, Poupardin R . CYP6 P450 enzymes and ACE-1 duplication produce extreme and multiple insecticide resistance in the malaria mosquito Anopheles gambiae. PLoS Genet. 2014; 10(3):e1004236. PMC: 3961184. DOI: 10.1371/journal.pgen.1004236. View

Dabire K, Baldet T, Diabate A, Dia I, Costantini C, Cohuet A . 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(6):990-7. DOI: 10.1603/0022-2585(2007)44[990:afdcia]2.0.co;2. View

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. 2000; 41(4):595-611. View

Riveron J, Yunta C, Ibrahim S, Djouaka R, Irving H, Menze B . A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector. Genome Biol. 2014; 15(2):R27. PMC: 4054843. DOI: 10.1186/gb-2014-15-2-r27. View

10.

Wondji C, Dabire R, Tukur Z, Irving H, Djouaka R, Morgan J . 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(7):484-91. PMC: 3579012. DOI: 10.1016/j.ibmb.2011.03.012. View

11.

Okoye P, Brooke B, Koekemoer L, Hunt R, Coetzee M . Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg. 2008; 102(6):591-8. DOI: 10.1016/j.trstmh.2008.02.022. View

12.

Awolola T, Oyewole I, Koekemoer L, 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(7):525-31. DOI: 10.1016/j.trstmh.2004.12.003. View

13.

Fossog B, Kopya E, Ndo C, Menze-Djantio B, Costantini C, Njiokou F . Water Quality and Anopheles gambiae Larval Tolerance to Pyrethroids in the Cities of Douala and Yaoundé (Cameroon). J Trop Med. 2012; 2012:429817. PMC: 3376768. DOI: 10.1155/2012/429817. View

14.

Casimiro S, Coleman M, Mohloai P, Hemingway J, Sharp B . Insecticide resistance in Anopheles funestus (Diptera: Culicidae) from Mozambique. J Med Entomol. 2006; 43(2):267-75. DOI: 10.1603/0022-2585(2006)043[0267:iriafd]2.0.co;2. View

15.

Menze B, Riveron J, Ibrahim S, Irving H, Antonio-Nkondjio C, Awono-Ambene P . 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(10):e0163261. PMC: 5056689. DOI: 10.1371/journal.pone.0163261. View

16.

Cuamba N, Morgan J, Irving H, Steven A, Wondji C . High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLoS One. 2010; 5(6):e11010. PMC: 2882342. DOI: 10.1371/journal.pone.0011010. View

17.

Vezenegho S, Chiphwanya J, Hunt R, Coetzee M, Bass C, Koekemoer L . Characterization of the Anopheles funestus group, including Anopheles funestus-like, from Northern Malawi. Trans R Soc Trop Med Hyg. 2013; 107(12):753-62. DOI: 10.1093/trstmh/trt089. View

18.

Bass C, Nikou D, Blagborough A, Vontas J, Sinden R, Williamson M . PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J. 2008; 7:177. PMC: 2553798. DOI: 10.1186/1475-2875-7-177. View

19.

Akogbeto M, Djouaka R, Kinde-Gazard D . Screening of pesticide residues in soil and water samples from agricultural settings. Malar J. 2006; 5:22. PMC: 1513586. DOI: 10.1186/1475-2875-5-22. View

20.

Wondji C, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M . Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A. 2012; 109(47):19063-70. PMC: 3511128. DOI: 10.1073/pnas.1217229109. View