Levels of insecticide resistance to deltamethrin, malathion, and temephos, and associated mechanisms in Aedes aegypti mosquitoes from the Guadeloupe and Saint Martin islands (French West Indies)

Abstract

BackgroundIn the Guadeloupe and Saint Martin islands, Aedes aegypti mosquitoes are the only recognized vectors of dengue, chikungunya, and Zika viruses. For around 40 years, malathion was used as a mosquito adulticide and temephos as a larvicide. Since the European Union banned the use of these two insecticide molecules in the first decade of the 21st century, deltamethrin and Bacillus thuringiensis var. israelensis are the remaining adulticide and larvicide, respectively, used in Guadeloupe. In order to improve the management of vector control activities in Guadeloupe and Saint Martin, we investigated Ae. aegypti resistance to and mechanisms associated with deltamethrin, malathion, and temephos.Methods Ae. aegypti mosquitoes were collected from six different localities of Guadeloupe and Saint Martin. Larvae were used for malathion and temephos bioassays, and adult mosquitoes for deltamethrin bioassays, following World Health Organization recommendations. Knockdown resistance (Kdr) genotyping for V1016I and F1534C mutations, and expression levels of eight enzymes involved in detoxification mechanisms were examined in comparison with the susceptible reference Bora Bora strain.ResultsResistance ratios (RR50) calculated for Ae. aegypti larvae showed high resistance levels to temephos (from 8.9 to 33.1-fold) and low resistance levels to malathion (from 1.7 to 4.4-fold). Adult females displayed moderate resistance levels to deltamethrin regarding the time necessary to affect 50% of individuals, varying from 8.0 to 28.1-fold. Molecular investigations on adult mosquitoes showed high resistant allele frequencies for V1016I and F1534C (from 85 to 96% and from 90 to 98%, respectively), as well as an overexpression of the glutathione S-transferase gene, GSTe2, the carboxylesterase CCEae3a, and the cytochrome genes 014614, CYP6BB2, CYP6M11, and CYP9J23.Conclusions Ae. aegypti populations from Guadeloupe and Saint Martin exhibit multiple resistance to organophosphates (temephos and malathion), and pyrethroids (deltamethrin). The mechanisms associated with these resistance patterns show strong frequencies of F1534C and V1016I Kdr mutations, and an over-expression of CCEae3a, GSTe2, and four cytochrome P450 genes (014614, CYP9J23, CYP6M11, CYP6BB2). These results will form the baseline for a deeper understanding of the insecticide resistance levels and associated mechanisms of Ae. aegypti populations and will be used to improve vector control strategies in Guadeloupe and Saint Martin.Electronic supplementary materialThe online version of this article (doi:10.1186/s40249-017-0254-x) contains supplementary material, which is available to authorized users.

Insecticide Susceptibility of Aedes Aegypti Larvae to Bacillus Thuringiensis Israelensis and Juvenile Hormone in Dengue Epidemic Areas of Samutsongkhram, Thailand

“…The Public Health Department emphasizes using sand covered by temephos or pesticide spraying to control the mosquito vector. There are reports in many countries including Thailand [7] that Ae. aegypti (mosquito larvae) has started to resist the temephos chemical.…”

The need to harmonize insecticide resistance testing: methodology, intensity concentrations and molecular mechanisms evaluated inAedes aegyptipopulations in Central America and Hispaniola

“…As pirimiphos-methyl is scarcely used in the region, resistance to this product could be a cross-resistance phenomenon stemming from the continuous and wide spread use of temephos (26, 71, 72). Resistance to malathion and pirimiphos methyl have been reported elsewhere (21, 73–75), and in the LAC region (26, 36, 71, 76–81).…”

“…In America, kdr mutations have been reported in Ae. aegypti populations from Ecuador, (22), United States (23, 24), Colombia (25, 26), México (27–29), Brazil (30–35), Lesser Antilles (36–40), French Guiana (37), Venezuela (29, 41), Cuba (29, 39), Panamá (42), Puerto Rico (43). This is the first report of kdr mutations for the countries included in this study, except for Haiti (87).…”

“…Resistance to pyrethroids in mosquitoes have been widely associated with the F1534C (21, 23, 25, 27, 29, 30, 32, 39–41, 83, 88–101) and V1016I mutations (24, 25, 27, 29, 30, 32, 36, 38, 40, 41, 88, 93, 97, 100, 102, 103). The simultaneous presence of both mutations has been associated with enhanced tolerance to deltamethrin in the past (31).…”

A cluster of CYP6 gene family associated with the major quantitative trait locus is responsible for the pyrethroid resistance in Culex pipiens pallen

“…Comparison of CYP6BB4 with other closely related sequences reveals that it is 56% identical to its orthologue A. aegypti CYP6BB2 (GenBank: AAEL014893). Indeed, an overexpression of CYP6BB2 was associated with a DM, malathion, and temephos resistance phenotype (Kasai et al ., ; Dusfour et al ., ; Goindin et al ., ). Faucon et al .…”