Insensitivity to the Spatial Repellent Action of Transfluthrin in Aedes aegypti: A Heritable Trait Associated with Decreased Insecticide Susceptibility

PLoS Neglected Tropical Diseases

Volumn 9, Issue 4, 2015, Pages

  Wagman, Joseph M ^a   Achee, Nicole L ^b   Grieco, John P ^b  

^a Uniformed Services University of the Health Sciences   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPHENOTANE; INSECT REPELLENT; MALATHION; TRANSFLUTHRIN; UNCLASSIFIED DRUG; CYCLOPROPANE DERIVATIVE; FLUOROBENZENE; INSECTICIDE;

ADULT; AEDES AEGYPTI; ALLELE; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BIOASSAY; BREEDING; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; GENE FREQUENCY; HERITABILITY; HIGH THROUGHPUT SCREENING; INSECTICIDE RESISTANCE; MALE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROGENY; QUANTITATIVE TRAIT; SPATIAL REPELLENCY; AEDES; ANIMAL; DRUG EFFECTS; GENETICS; PROCEDURES;

AEDES; ANIMALS; BIOLOGICAL ASSAY; CYCLOPROPANES; FLUOROBENZENES; INSECT REPELLENTS; INSECTICIDE RESISTANCE; INSECTICIDES;

EID: 84929493844     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003726     Document Type: Article

References (58)

1. Tanner M, de Savigny D, Malaria eradication back on the table. Bull World Health Organ. 2008;86(2):82. 18297155
2. Townson H, Nathan MB, Zaim M, Guillet P, Manga L, Bos R, et al. Exploiting the potential of vector control for disease prevention. Bull World Health Organ. 2005;83(12):942–7. 16462987
3. WHO. Innovative vector control interventions—2009 annual report. TDR/BL5.10. Geneva: World Health Organization; 2010.
4. Achee N, Grieco J, Is it time to formally recognize spatial repellency for disease prevention? Outlooks on Pest Management. 2012;23(6):283–6.
5. Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG, et al. Spatial repellents: from discovery and development to evidence-based validation. Malar J. 2012;11:164. 22583679
6. Grieco JP, Achee NL, Chareonviriyaphap T, Suwonkerd W, Chauhan K, Sardelis MR, et al. A new classification system for the actions of IRS chemicals traditionally used for malaria control. PLoS One. 2007;2(1):e716.
7. Ogoma SB, Lorenz LM, Ngonyani H, Sangusangu R, Kitumbukile M, Kilalangongono M, et al. An experimental hut study to quantify the effect of DDT and airborne pyrethroids on entomological parameters of malaria transmission. Malar J. 2014;13:131. doi: 10.1186/1475-2875-13-131 24693934
8. Roberts D, Insecticide Repellency in Malaria Vector Control: A Position Paper. Report No.:81131. Arlington, VA: Medical Service Corporation Internaitonal/USAID; 1993.
9. WHOPES. Guidelines for Efficacy Testing of Spatial Repellents. Geneva: World Health Organization; 2013.
10. Achee N, Masuoka P, Smith P, Martin N, Chareonviryiphap T, Polsomboon S, et al. Identifying the effective concentration for spatial repellency of the dengue vector Aedes aegypti. Parasit Vectors. 2012;5:300. doi: 10.1186/1756-3305-5-300 23273133
11. Paz-Soldan VA, Plasai V, Morrison AC, Rios-Lopez EJ, Guedez-Gonzales S, Grieco JP, et al. Initial assessment of the acceptability of a Push-Pull Aedes aegypti control strategy in Iquitos, Peru and Kanchanaburi, Thailand. Am J Trop Med Hyg. 2011;84(2):208–17. doi: 10.4269/ajtmh.2011.09-0615 21292886
12. Salazar FV, Achee NL, Grieco JP, Prabaripai A, Ojo TA, Eisen L, et al. Effect of Aedes aegypti exposure to spatial repellent chemicals on BG-SentinelTM trap catches. Parasit Vectors. 2013;6(1):145.
13. Syafruddin D, Bangs MJ, Sidik D, Elyazar I, Asih PB, Chan K, et al. Impact of a Spatial Repellent on Malaria Incidence in Two Villages in Sumba, Indonesia. Am J Trop Med Hyg. 2014;91(6):1079–87. doi: 10.4269/ajtmh.13-0735 25311699
14. Ditzen M, Pellegrino M, Vosshall LB, Insect odorant receptors are molecular targets of the insect repellent DEET. Science. 2008;319(5871):1838–42. doi: 10.1126/science.1153121 18339904
15. Kawada H, Ohashi K, Dida GO, Sonye G, Njenga SM, Mwandawiro C, et al. Insecticidal and repellent activities of pyrethroids to the three major pyrethroid-resistant malaria vectors in western Kenya. Parasit Vectors. 2014;7(1):208.
16. Syed Z, Leal WS, Mosquitoes smell and avoid the insect repellent DEET. Proc Natl Acad Sci U S A. 2008;105(36):13598–603. doi: 10.1073/pnas.0805312105 18711137
17. Bohbot JD, Dickens JC, Odorant receptor modulation: ternary paradigm for mode of action of insect repellents. Neuropharmacology. 2012;62(5–6):2086–95.
18. Stanczyk NM, Brookfield JF, Field LM, Logan JG, Aedes aegypti mosquitoes exhibit decreased repellency by DEET following previous exposure. PLoS One. 2013;8(2):e54438. doi: 10.1371/journal.pone.0054438 23437043
19. Stanczyk NM, Brookfield JF, Ignell R, Logan JG, Field LM, Behavioral insensitivity to DEET in Aedes aegypti is a genetically determined trait residing in changes in sensillum function. Proc Natl Acad Sci U S A. 2010;107(19):8575–80. doi: 10.1073/pnas.1001313107 20439757
20. Roberts DR, Alecrim WD, Hshieh P, Grieco JP, Bangs M, Andre RG, et al. A probability model of vector behavior: effects of DDT repellency, irritancy, and toxicity in malaria control. J Vector Ecol. 2000;25(1):48–61. 10925797
21. Bohbot JD, Fu L, Le TC, Chauhan KR, Cantrell CL, Dickens JC, Multiple activities of insect repellents on odorant receptors in mosquitoes. Med Vet Entomol. 2011;25(4):436–44. doi: 10.1111/j.1365-2915.2011.00949.x 21395633
22. Kain P, Boyle SM, Tharadra SK, Guda T, Pham C, Dahanukar A, et al. Odour receptors and neurons for DEET and new insect repellents. Nature. 2013;502(7472):507–12. doi: 10.1038/nature12594 24089210
23. Debboun M, Frances SP, Strickman D, Insect Repellents: Principles, Methods and Uses. Boca Raton, FL: CRC Press; 2007.
24. Moore SJ, Mordue Luntz AJ, Logan JG, Insect bite prevention. Infect Dis Clin North Am. 2012;26(3):655–73. doi: 10.1016/j.idc.2012.07.002 22963776
25. Pickett JA, Birkett MA, Logan JG, DEET repels ORNery mosquitoes. Proc Natl Acad Sci U S A. 2008;105(36):13195–6. doi: 10.1073/pnas.0807167105 18772369
26. DeGennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, Goldman C, et al. orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature. 2013;498(7455):487–91. doi: 10.1038/nature12206 23719379
27. Roberts DR, Andre RG, Insecticide resistance issues in vector-borne disease control. Am J Trop Med Hyg. 1994;50(6 Suppl):21–34. 8024082
28. Achee NL, Sardelis MR, Dusfour I, Chauhan KR, Grieco JP, Characterization of spatial repellent, contact irritant, and toxicant chemical actions of standard vector control compounds. J Am Mosq Control Assoc. 2009;25(2):156–67. 19653497
29. Manda H, Shah P, Polsomboon S, Chareonviriyaphap T, Castro-Llanos F, Morrison A, et al. Contact irritant responses of Aedes aegypti Using sublethal concentration and focal application of pyrethroid chemicals. PLoS Negl Trop Dis. 2013;7(2):e2074. doi: 10.1371/journal.pntd.0002074 23469302
30. Rutledge LC, Gupta RK, Piper GN, Lowe CA, Studies on the inheritance of repellent tolerances in Aedes aegypti. J Am Mosq Control Assoc. 1994;10(1):93–100. 8014634
31. Frances SP, Waterson DG, Beebe NW, Cooper RD, Field evaluation of repellent formulations containing deet and picaridin against mosquitoes in Northern Territory, Australia. J Med Entomol. 2004;41(3):414–7. 15185943
32. Pellegrino M, Steinbach N, Stensmyr MC, Hansson BS, Vosshall LB, A natural polymorphism alters odour and DEET sensitivity in an insect odorant receptor. Nature. 2011;478(7370):511–4. doi: 10.1038/nature10438 21937991
33. Cohnstaedt LW, Allan SA, Effects of sublethal pyrethroid exposure on the host-seeking behavior of female mosquitoes. J Vector Ecol. 2011;36(2):395–403. doi: 10.1111/j.1948-7134.2011.00180.x 22129411
34. Manda H, Arce LM, Foggie T, Shah P, Grieco JP, Achee NL, Effects of irritant chemicals on Aedes aegypti resting behavior: is there a simple shift to untreated "safe sites"? PLoS Negl Trop Dis. 2011;5(7):e1243. doi: 10.1371/journal.pntd.0001243 21814587
35. Siegert PY, Walker E, Miller JR, Differential behavioral responses of Anopheles gambiae (Diptera: Culicidae) modulate mortality caused by pyrethroid-treated bednets. J Econ Entomol. 2009;102(6):2061–71. 20069832
36. Ogoma SB, Ngonyani H, Simfukwe ET, Mseka A, Moore J, Killeen GF, Spatial repellency of transfluthrin-treated hessian strips against laboratory-reared Anopheles arabiensis mosquitoes in a semi-field tunnel cage. Parasit Vectors. 2012;5:54. doi: 10.1186/1756-3305-5-54 22433128
37. Pates HV, Line JD, Keto AJ, Miller JE, Personal protection against mosquitoes in Dar es Salaam, Tanzania, by using a kerosene oil lamp to vaporize transfluthrin. Med Vet Entomol. 2002;16(3):277–84. 12243228
38. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, . Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;27(2):91–8. doi: 10.1016/j.pt.2010.08.004 20843745
39. Hemingway J, The role of vector control in stopping the transmission of malaria: threats and opportunities. Philos Trans R Soc Lond B Biol Sci. 2014;369(1645):20130431. doi: 10.1098/rstb.2013.0431 24821917
40. Ogoma SB, Moore SJ, Maia MF, A systematic review of mosquito coils and passive emanators: defining recommendations for spatial repellency testing methodologies. Parasit Vectors. 2012;5:287. doi: 10.1186/1756-3305-5-287 23216844
41. Grieco JP, Achee NL, Sardelis MR, Chauhan KR, Roberts DR, A novel high-throughput screening system to evaluate the behavioral response of adult mosquitoes to chemicals. J Am Mosq Control Assoc. 2005;21(4):404–11. 16506566
42. Wagman J. Spatial Repellency and the Field Evaluation of a Push-Pull Strategy for the Control of Malaria Vectors in Northern Belize, Central America. Ph.D. Dissertation, Uniformed Services University of the Health Sciences; 2014. Available: dx.doi.org/10.13140/RG.2.1.5148.3682.
43. Brogdon W, Chan A, Guidline for Evaluating Insecticide Resistance in Vectors Using the CDC Bottle Bioassay. Atlanta, GA: US Centers for Disease Control and Prevention; 2013.
44. Linss JG, Brito L, Garcia G, Araki A, Bruno R, Lima JB, et al. Distribution and dissemination of the Val1016Ile and Phe1534Cys Kdr mutations in Aedes aegypti Brazilian natural populations. Parasites & Vectors. 2014;7(1):25.
45. Harris A, Rajatileka S, Ranson H, Pyrethroid resistance in Aedes aegypti from Grand Cayman. Am J Trop Med Hyg. 2010;83:277–84. doi: 10.4269/ajtmh.2010.09-0623 20682868
46. Saavedra-Rodriguez K, Urdaneta-Marquez L, Rajatileka S, Moulton M, Flores A, A mutation in the voltage-gated sodium channel gene associated with pyrethroid resistance in Latin American Aedes aegypti. Insect Mol Biol. 2007;16:785–98. 18093007
47. Pierce B, Population Genetics. Genetics: A Conceptual Approach. 4th ed. New York, NY: W. H. Freeman and Co.; 2012. p. 693–714.
48. Hao H, Wei J, Dai J, Du J, Host-seeking and blood-feeding behavior of Aedes albopictus (Diptera: Culicidae) exposed to vapors of geraniol, citral, citronellal, eugenol, or anisaldehyde. J Med Entomol. 2008;45(3):533–9. 18533449
49. Ndiath MO, Mazenot C, Sokhna C, Trape JF, How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African populations. PLoS One. 2014;9(6):e97700. doi: 10.1371/journal.pone.0097700 24892677
50. Chareonviriyaphap T, Bangs MJ, Suwonkerd W, Kongmee M, Corbel V, Ngoen-Klan R, Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand. Parasit Vectors. 2013;6:280. doi: 10.1186/1756-3305-6-280 24294938
51. Saavedra-Rodriguez K, Beaty M, Lozano-Fuentes S, Denham S, Garcia-Rejon J, Reyes-Solis G, et al. Local Evolution of Pyrethroid Resistance Offsets Gene Flow Among Aedes aegypti Collections in Yucatan State, Mexico. Am J Trop Med Hyg. 2015;92(1):201–9. doi: 10.4269/ajtmh.14-0277 25371186
52. Brito L, Linss J, Lima-Camara T, Belinato T, Peixoto A, Assessing the effects of Aedes aegypti kdr mutations on pyrethroid resistance and its fitness cost. PLoS One. 2013;8:e60878. doi: 10.1371/journal.pone.0060878 23593337
53. Enayati A, Hemingway J, Malaria management: past, present, and future. Annu Rev Entomol. 2010;55:569–91. doi: 10.1146/annurev-ento-112408-085423 19754246
54. Matthews G, Integrated Vector Management: Controlling Vectors of Malaria and Other Insect Vector Borne Diseases. 1 ed. West Sussex, UK: John Wiley & Sons; 2011.
55. WHOPES. WHO recommended insecticides for indoor residual spraying against malaria vectors. Geneva: WHO; 2009.
56. WHOPES. WHO recommended insecticides products for treatment of mosquito nets for malaria vector control. Geneva: WHO; 2007.
57. Nkya TE, Akhouayri I, Kisinza W, David JP, Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects. Insect Biochem Mol Biol. 2013;43(4):407–16. doi: 10.1016/j.ibmb.2012.10.006 23123179
58. malERA. A research agenda for malaria eradication: vector control. PLoS Med. 2011;8(1):e1000401. doi: 10.1371/journal.pmed.1000401 21311587