Efficacy of pyriproxyfen-treated nets in sterilizing and shortening the longevity of Anopheles gambiae (Diptera: Culicidae)

Journal of Medical Entomology

Volumn 49, Issue 5, 2012, Pages 1052-1058

  Ohashi, Kazunori ^a   Nakada, Kazuhide ^a   Ishiwatari, Takao ^a   Miyaguchi, Jun'Ichi ^a   Shono, Yoshinori ^a   Lucas, John R ^b   Mito, Nobuaki ^a  

^a SUMITOMO CHEMICAL CO LTD   (Japan)

^b Sumitomo Chemical (UK) Plc Horatio House   (United Kingdom)

Author keywords

insecticide treated bed net; malaria control; pyriproxyfen; resistance management; sterilizing effect

Indexed keywords

JUVENILE HORMONE; PYRIDINE DERIVATIVE; PYRIPROXYFEN;

ANIMAL; ANOPHELES GAMBIAE; ARTICLE; BED NET; DRUG EFFECT; FEMALE; FERTILITY; LONGEVITY; OVIPARITY;

ANIMALS; ANOPHELES GAMBIAE; FEMALE; FERTILITY; INSECTICIDE-TREATED BEDNETS; JUVENILE HORMONES; LONGEVITY; OVIPARITY; PYRIDINES;

ANOPHELES GAMBIAE; CULICIDAE; DIPTERA; HEXAPODA;

EID: 84866370575     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME12006     Document Type: Article

References (50)

1. Aiku, A. O., A. Yates, and M. Rowland. 2006. Laboratory evaluation of pyriproxifen treated bednets on mosquito fertility and fecundity. A preliminary study. West Afr. J. Med. 25: 22-26.
2. Asidi, A. N., R. N'Guessan, A. A. Koffi, C. F. Curtis, J. M. Hougard, F. Chandre, V. Corbel, F. Darriet, M. Zaim, and M. W. Rowland. 2005. Experimental hut evaluation of bednets treated with an organophosphate (chlorpyrifos-methyl) or apyrethroid (lambdacyhalothrin) alone and in combination against insecticide-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes. Malar. J. 4: 25.
3. Bai, H., D. B. Gelman, and S. R. Palli. 2010. Mode of action of methoprene in affecting female reproduction in the African malaria mosquito, Anopheles gambiae. Pest Manag. Sci. 66: 936-943.
4. Bhattarai, A., A. S. Ali, S. P. Kachur, A. Martensson, A. K. Abbas, R Khatib, A. W. Al-Mafazy, M. Ramsan, G. Rotl-lant, J. F. Gerstenmaier, et al. 2007. Impact of artemis-inin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 4: e309.
5. Chandre, F., F. Darrier, L. Manga, M. Akogbeto, O. Faye, J. Mouchet, and P. Guillet. 1999. Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull. W.H.O. 77: 230-234.
6. Charlwood, J. D., T. Smith, F. F. Billingsley, W. Takken, E.O.K. Lyimo, and J.H.E.T. Meuwissen. 1997. Survival and infection probabilities of anthropophagie anophelines from an area of high prevalence of Plasmodium falciparum in humans. Bull. Entomol. Res. 87: 445-453.
7. Corbel, V., F. Darriet, F. Chandre, and J. M. Hougard. 2002. Insecticide mixtures for mosquito net impregnation against malaria vectors. Parasite 9: 255-259.
8. Corbel, V., F. Chandre, C. Brengues, M. Akogbeto, F. Lar-deux, J. M. Hougard, and P. Guillet. 2004. Dosage-dependent effects of permethrin-treated nets on the behaviour of Anopheles gambiae and the selection of pyrethroid resistance. Malar. J. 3: 22.
9. Curtis, C. F. 1985. Theoretical models of the use of insecticide mixtures for the management of resistance. Bull. Entomol. Res. 75: 259-265.
10. Czeher, C, R. Labbo, I. Arzika, and J. B. Duchemin. 2008. Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation. Malar. J. 7: 189.
11. Dabire, K. R., A. Diabate, L. Djogbenou, A. Ouari, R. N'Guessan, J. B. Ouedraogo, J. M. Hougard, F. Chandre, and T. Baldet. 2008. Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar. J. 7: 188.
12. Dabire, R. K., A. Diabate, T. Baldet, L. Pare-Toe, R. T. Guiguemde, J. B. Ouedraogo, and O. Skovmand. 2006. Personal protection of long lasting insecticide-treated nets in areas of Anopheles gambiae s.s. resistance to py-rethroids. Malar. J. 5: 12.
13. Dhadialla, T. S., G R. Carlson, and D. P. Le. 1998. New insecticides with ecdysteroidal and juvenile hormone activity. Annu. Rev. Entomol. 43: 545-569.
14. Dye, C. 1992. The analysis of parasite transmission by bloodsucking insects. Annu. Rev. Entomol. 37: 1-19.
15. [FAO] Food and Agricultural Organization of the United Nations. 1999. Pesticide residues in food-1999. Report of the Joint Meeting of the FAO Panel of Experts on Pesticide Residues in Food and the Environment and the WHO Core Assessment Group. FAO Plant Production and Protection, paper 153. Food and Agricultural Organization of the United Nations, Rome, Italy.
16. Fegan, G. W., A. M. Noor, W. S. Akhwale, S. Cousens, and R. W. Snow. 2007. Effect of expanded insecticide-treated bednet coverage on child survival in rural Kenya: a longitudinal study. Lancet 370: 1035-1059.
17. Garrett-Jones, C. 1964a. Prognosis for interruption of malaria transmission through assessment of the mosquitoÕs vectorial capacity. Nature 204: 1173-1175.
18. Garrett-Jones, C. 1964b. The human blood index of malaria vectors in relation to epidemiological assessment. Bull. W.H.O 30: 241-261.
19. Guillet, P., D. Alnwick, M. K Cham, M. Neira, M. Zaim, D. Heymann, and K. Mukelabai. 2001a. Long-lasting treated mosquito nets: a breakthrough in malaria prevention. Bull. W.H.O. 79: 998.
20. Guillet, P., R. N'Guessan, F. Darriet, M. Traore-Lamizana, F. Chandre, and P. Carnevale. 2001b. Combined pyre-throid and carbamate Ôtwo-in- oneÕ treated mosquito nets: field efficacy against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus. Med. Vet. Entomol. 15: 105-112.
21. Hargreaves, K, L. L. Koekemoer, B. D. Brooke, R. H. Hunt, J. Mthembu, and M. Coetzee. 2000. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med. Vet. Entomol. 14: 181-189.
22. Hatakoshi, M., H. Kawada, S. Nishida, H. Kishida, and I. Nakayama. 1987. Laboratory evaluation of 2-[1-methyl-2-(4-phenoxyphenoxy)-ethoxy] pyridine against larvae of mosquitoes and houseßy. Jpn. J. Sanit. Zool. 38: 271-274.
23. Hawley, W. A., P. A. Phillips-Howard, F. O. ter Kuile, D. J. Terlouw, J. M. Vulule, M. Ombok, B. L. Nahlen, J. E. Gimnig, S. K Kariuki, M. S. Kolczak, et al. 2003. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am. J. Trop. Med. Hyg. 68: 121-127.
24. Henry, M. C, S. B. Assi, C. Rogier, J. Dossou-Yovo, F. Chandre, P. Guillet, and P. Carnevale. 2005. Protective effi-cacy of lambda-cyhalothrin treated nets in Anopheles gambiae pyrethroid resistance areas of Cote dÕIvoire. Am. J. Trop. Med. Hyg. 73: 859-864.
25. Hirano, M., M. Hatakoshi, H. Kawada, and Y. Takimoto. 1998. Pyriproxyfen and other juvenile hormone analogues. Rev. Toxicol. 2: 357-394.
26. Hougard, J. M., V. Corbel, R N'Guessan, F. Darriet, F. Chandre, M. Akogbeto, T. Baldet, P. Guillet, P. Carnevale, and M. Traore-Lamizana. 2003. Efficacy of mosquito nets treated with insecticide mixtures or mosaics against insecticide resistant Anopheles gambiae and Culex quinquefasciatus (Diptera: Culicidae) in Cote dÕIvoire. Bull. Entomol. Res. 93: 491-498.
27. Itoh, T., H. Kawada, A. Abe, Y Eshita, Y. Rongsriyam, and A. Igarashi. 1994. Utilization of bloodfed females of Aedes aegypti as a vehicle for the transfer of the insect growth regulator pyriproxyfen to larval habitats. J. Am. Mosq. Control Assoc. 10: 344-347.
28. Kawada, H, G. O. Dida, K Ohashi, O. Komagata, S. Kasai, T. Tomita, G Sonye, Y Maekawa, C. Mwatele, S. M. Njenga, 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: e22574.
29. Lindblade, K A., T. P. Eisele, J. E. Gimnig, J. A. Alaii, F. Odhiambo, F. O. ter Kuile, W. A. Hawley, K A. Wanne-muehler, P. A. Phillips-Howard, D. H. Rosen, et al. 2004. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets: 4 to 6 years of follow-up. JAMA 291: 2571-2580.
30. Muller, P., M. Chouaibou, P. Pignatelli, J. Etang, E. Walker, M. Donnelly, F. Simard, and H. Ranson. 2008. Pyrethroid tolerance is associated with elevated expression of antioxidants and agricultural practice in Anopheles arabiensis sampled from an area of cotton fields in northern Cameroon. Mol. Ecol. 17: 1145-1155.
31. Malima, R C, R. M. Oxborough, P. K Tungu, C. Maxwell, I. Lyimo, V. Mwingira, F. W. Mosha, J. Matowo, S. M. Magesa, and M. W. Rowland. 2009. Behavioural and in-secticidal effects of organophosphate-, carbamate-and pyrethroid-treated mosquito nets against African malaria vectors. Med. Vet. Entomol. 23: 317-325.
32. Mani, G. S. 1985. Evolution of resistance in the presence of two insecticides. Genetics 109: 761-783.
33. Martinez-Torres, D., F. Chandre, M. S. Williamson, F. Dar-riet, J. B. Berge, A. L. Devonshire, P. Guillet, N. Pasteur, and D. Pauron. 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol. Biol. 7: 179-184.
34. Mathias, D. K, E. Ochomo, F. Atieli, M. Ombok, M. Nabie Bayoh, G. Olang, D. Muhia, L. Kamau, J. M. Vulule, M. J. Hamel, et al. 2011. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and pheno-typic variability in susceptibility to insecticides in western Kenya. Malar. J. 10: 10.
35. Meola, R., S. Pullen, and S. Meola. 1996. Toxicity and his-topathology of the growth regulator pyriproxyfen to adults and eggs of the cat ßea (Siphonaptera: Pulicidae). J. Med. Entomol. 33: 670-679.
36. Miler, J. E. 1994. Can pyriproxyfen (an insect growth regulator) be used to prevent selection of permethrin resistance by impregnated bed nets? Trans. R. Soc. Trop. Med. Hyg. 88: 281.
37. Mosha, F. W., I. N. Lyimo, R. M. Oxborough, R. Malima, F. Tenu, J. Matowo, E. Feston, R. Mndeme, S. M. Magesa, and M. Rowland. 2008. Experimental hut evaluation of the pyrrole insecticide chlorfenapyr on bed nets for the control of Anopheles arabiensis and Culex quinquefasciatus. Trop. Med. Int. Health 13: 644-652.
38. N'Guessan, R., P. Boko, A. Odjo, M. Akogbeto, A. Yates, and M. Rowland. 2007a. Chlorfenapyr: a pyrrole insecticide for the control of pyrethroid or DDT resistant Anopheles gambiae (Diptera: Culicidae) mosquitoes. Acta Trop. 102: 69-78.
39. N'Guessan, R., V. Corbel, J. Bonnet, A. Yates, A. Asidi, P. Boko, A. Odjo, M. Akogbeto, and M. Rowland. 2007b. Evaluation of indoxacarb, an oxadiazine insecticide for the control of pyrethroid-resistant Anopheles gambiae (Diptera: Culicidae). J. Med. Entomol. 44: 270-276.
40. N'Guessan, R, P. Boko, A. Odjo, B. Knols, M. Akogbeto, and M. Rowland. 2009. Control of pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes with chlorfenapyr in Benin. Trop. Med. Int. Health 14: 389-395.
41. Patterson, J. W. 1974. A comparison of the morphogenetic and sterilizing activities of juvenile hormone mimics on Aedes aegypti. J. Insect Physiol. 20: 2095-2106.
42. Ranson, H, R. N'Guessan, J. Lines, N. Moiroux, Z. Nkuni, and V. Corbel. 2011. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 27: 91-98.
43. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http://www.R-project.org).
44. Santolamazza, F., M. Calzetta, J. Etang, E. Barrese, I. Dia, A. Caccone, M. J. Donnelly, V. Petrarca, F. Simard, J. Pinto, et al. 2008. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar. J. 7: 74.
45. SAS Institute. 2009. JMP userÕs guide, release 8. SAS Institute, Cary, NC.
46. Shapiro, A. B., G. D. Wheelock, H. H. Hagedorn, F. C. Baker, L. W. Tsai, and D. A. Schooley. 1986. Juvenile hormone and juvenile hormone esterase in adult females of the mosquito Aedes aegypti. J. Insect Physiol. 32: 867-877.
47. Tabashnik, B. E. 1989. Managing resistance with multiple pesticide tactics: theory, evidence, and recommendations. J. Econ. Entomol. 82: 1263-1269.
48. [WHO] World Health Organization. 2010. World malaria report 2010. (http://www.who.int/malaria/world- malaria-report-2010/en/index.html).
49. Zaim, M., and P. Guillet. 2002. Alternative insecticides: an urgent need. Trends Parasitol. 18: 161-163.
50. Zaim, M., A. Aitio, and N. Nakashima. 2000. Safety of pyre-throid-treated mosquito nets. Med. Vet. Entomol. 14: 1-5.