Widespread pyrethroid and DDT resistance in the major malaria vector anopheles funestus in East Africa is driven by metabolic resistance mechanisms

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Mulamba, Charles ^a,b   Riveron, Jacob M ^a   Ibrahim, Sulaiman S ^a   Irving, Helen ^a   Barnes, Kayla G ^a   Mukwaya, Louis G ^a   Birungi, Josephine ^b   Wondji, Charles S ^b  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^b UGANDA VIRUS RESEARCH INSTITUTE   (Uganda)

Author keywords

[No Author keywords available]

Indexed keywords

BENDIOCARB; CHLORPHENOTANE; CYSTEINE; CYTOCHROME P450; DELTAMETHRIN; DIELDRIN; FENITROTHION; MALATHION; ORGANOPHOSPHATE; PERMETHRIN; PHENYLALANINE; PYRETHROID; VASCULOTROPIN RECEPTOR 2; VOLTAGE GATED SODIUM CHANNEL; INSECTICIDE; SODIUM CHANNEL;

ADULT; AFRICA; AMINO ACID SUBSTITUTION; ANOPHELES FUNESTUS; ARTICLE; CONTROLLED STUDY; CYP6P9A GENE; CYP6P9B GENE; DRUG SENSITIVITY; FEMALE; GENE FREQUENCY; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; GSTE2 GENE; HAPLOTYPE; KDR GENE; MALARIA; MALE; METABOLIC INHIBITION; MICROBIAL GENE; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PESTICIDE RESISTANCE; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; VOLTAGE GATED SODIUM CHANNEL GENE; ANIMAL; ANOPHELES; DISEASE CARRIER; DRUG EFFECTS; GENETICS; INSECTICIDE RESISTANCE; MOLECULAR GENETICS; MUTATION; TRANSMISSION;

ANOPHELES FUNESTUS;

AFRICA, EASTERN; ANIMALS; ANOPHELES; DDT; FEMALE; INSECT VECTORS; INSECTICIDE RESISTANCE; INSECTICIDES; MALARIA; MOLECULAR SEQUENCE DATA; MUTATION; PYRETHRINS; SODIUM CHANNELS;

EID: 84908108248     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110058     Document Type: Article

References (47)

1. WHO (2013) World Malaria Report 2013.
2. WHO (2010) World Malaria Report 2010.
3. Chanda E, Hemingway J, Kleinschmidt I, Rehman AM, Ramdeen V, et al. (2011) Insecticide resistance and the future of malaria control in zambia. PLoS One 6: e24336.
4. Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS (2010) High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLoS ONE 5: e11010.
5. Riveron JM, Irving H, Ndula M, Barnes KG, Ibrahim SS, et al. (2013) Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus. Proc Natl Acad Sci U S A 110: 252-257.
6. Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, et al. (2012) Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A 109: 19063-19070.
7. Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R, et al. (2011) Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochem Mol Biol 41: 484-491.
8. Djouaka R, Irving H, Tukur Z, Wondji CS (2011) Exploring Mechanisms of Multiple Insecticide Resistance in a Population of the Malaria Vector Anopheles funestus in Benin. PLoS One 6: e27760.
9. Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M (2008) Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg 102: 591-598.
10. Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, et al. (2009) Insecticide resistance and its association with target-site mutations in natural populations of Anopheles gambiae from eastern Uganda. Trans R Soc Trop Med Hyg 103: 1121-1126.
11. Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS (2010) Pyrethroid resistance in an Anopheles funestus population from Uganda. PLoS ONE 5: e11872.
12. Coetzee M, Fontenille D (2004) Advances in the study of Anopheles funestus, a major vector of malaria in Africa. Insect Biochem Mol Biol 34: 599-605.
13. Coetzee M, Koekemoer LL (2013) Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu Rev Entomol 58: 393-412.
14. WHO (2012) Global Plan for Insecticide Resistance Management (GPIRM); Programme WGM, editor. Geneva, Switzerland: World Health Organization.
15. Gillies MT, Coetzee M (1987) A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). Publications of the South African Institute for Medical Research 55: 143.
16. Livak KJ (1984) Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics 107: 611-634.
17. Koekemoer LL, Kamau L, Hunt RH, Coetzee M (2002) A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg 66: 804-811.
18. Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, et al. (2008) PCRbased detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malaria Journal 7: 177.
19. Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, et al. (1993) High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. MolBiochemParasitol 61: 315-320.
20. WHO (1998) Test procedure for insecticide resistance monitoring in malaria vectors, bioefficacy and persistence of insecticides on treated surfaces. Geneva: World Health Organization.
21. Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, et al. (1998) Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 7: 179-184.
22. Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, et al. (2000) 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 9: 491-497.
23. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
24. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
25. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583-589.
26. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
27. Riveron JM, Yunta C, Ibrahim SS, Djouaka R, Irving H, et al. (2014) A single mutation in the GSTe2 gene allows tracking of metabolically-based insecticide resistance in a major malaria vector. Genome Biol 15: R27.
28. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
29. Mulamba C, Irving H, Riveron JM, Mukwaya LG, Birungi J, et al. (2014) Contrasting Plasmodium infection rates and insecticide susceptibility profiles between the sympatric sibling species Anopheles parensis and Anopheles funestus s.s: a potential challenge for malaria vector control in Uganda. Parasit Vectors 7: 71.
30. Echodu R, Okello-Onen J, Lutwama J, Enyaru J, Ocan R, et al. (2010) Heterogeneity of Anopheles Mosquitoes in Nyabushozi County, Kiruhura district, Uganda. Journal of Parasitology and Vector Biology 2: 28-34.
31. Okello PE, Van Bortel W, Byaruhanga AM, Correwyn A, Roelants P, et al. (2006) Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg 75: 219-225.
32. Dia I, Guelbeogo MW, Ayala D (2013) Advances and Perspectives in the Study of the Malaria Mosquito Anopheles funestus. In: Manguin S, editor. Anopheles mosquitoes - New insights into malaria vectors: In Tech Publisher. pp.197-220.
33. Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, et al. (2010) Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis 201: 1764-1774.
34. Kawada H, Dida GO, Ohashi K, Komagata O, Kasai S, et al. (2011) Multimodal Pyrethroid Resistance in Malaria Vectors, Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus s.s. in Western Kenya. Plos One 6.
35. Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, et al. (1999) Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ 77: 230-234.
36. Hunt R, Edwardes M, Coetzee M (2010) Pyrethroid resistance in southern African Anopheles funestus extends to Likoma Island in Lake Malawi. Parasit Vectors 3: 122.
37. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, et al. (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91-98.
38. Brooke BD, Kloke G, Hunt RH, Koekemoer LL, Temu EA, et al. (2001) Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bull Entomol Res 91: 265-272.
39. Michel AP, Ingrasci MJ, Schemerhorn BJ, Kern M, Le Goff G, et al. (2005) Rangewide population genetic structure of the African malaria vector Anopheles funestus. Mol Ecol 14: 4235-4248.
40. Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, et al. (2009) Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J 8: 299.
41. Davies TG, Field LM, Usherwood PN, Williamson MS (2007) A comparative study of voltage-gated sodium channels in the Insecta: implications for pyrethroid resistance in Anopheline and other Neopteran species. Insect Mol Biol 16: 361-375.
42. Kwiatkowska RM, Platt N, Poupardin R, Irving H, Dabire RK, et al. (2013) Dissecting the mechanisms responsible for the multiple insecticide resistance phenotype in Anopheles gambiae s.s., M form, from Vallee du Kou, Burkina Faso. Gene 519: 98-106.
43. Harris AF, Rajatileka S, Ranson H (2010) Pyrethroid resistance in Aedes aegypti from Grand Cayman. Am J Trop Med Hyg 83: 277-284.
44. Wondji CS, Priyanka De Silva WA, Hemingway J, Ranson H, Parakrama Karunaratne SH (2008) Characterization of knockdown resistance in DDT- and pyrethroid-resistant Culex quinquefasciatus populations from Sri Lanka. Trop Med Int Health 13: 548-555.
45. Mitchell SN, Stevenson BJ, Muller P, Wilding CS, Egyir-Yawson A, et al. (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci U S A 109: 6147-6152.
46. Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, et al. (2012) Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS One 7: e42857.
47. Okia M, Ndyomugyenyi R, Kirunda J, Byaruhanga A, Adibaku S, et al. (2013) Bioefficacy of long-lasting insecticidal nets against pyrethroid-resistant populations of Anopheles gambiae s.s. from different malaria transmission zones in Uganda. Parasit Vectors 6: 130.