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. 2017 Feb 10;6(1):38.
doi: 10.1186/s40249-017-0254-x.

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)

Affiliations

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)

Daniella Goindin et al. Infect Dis Poverty. .

Abstract

Background: In 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.

Results: Resistance 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.

Keywords: Aedes aegypti; Deltamethrin; Guadeloupe; Insecticide resistance; Malathion; Mosquitoes; Saint Martin; Temephos.

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Figures

Fig. 1
Fig. 1
Geographical distribution of Ae. aegypti sampling sites in Guadeloupe and Saint Martin islands. In Guadeloupe, the sampling sites were located in Grande-Terre island (Anse-Bertrand, Saint-François, Les Abymes), and Basse-Terre island (Baie-Mahault and Deshaies)
Fig. 2
Fig. 2
Histogram of genotype proportions for the six populations studied regarding V1016I (a) and F1534C (b) Kdr mutations. V/V: V1016I wild homozygote genotype; I/V: V1016I heterozygote genotype; I/I: V1016I mutant homozygote; F/F: F1534C wild homozygote genotype; F/C: F1534C heterozygote genotype; C/C: F1534C mutant homozygote; ABY Les Abymes, SF Saint-François, BM Baie-Mahault, SXM Saint Martin, AB Anse-Bertrand, DH Deshaies, BORA Bora Bora susceptible strain
Fig. 3
Fig. 3
Adult transcription levels of five cytochrome P450 monooxygenases (014614, CYP6BB2, CYP6M11, CYP9J23, CYP9J28), two carboxyl/cholinesterases (CCEae3a, CCEae6a), and one glutathione S-transferase (GSTe2) for the six Ae. aegypti populations of Guadeloupe and Saint Martin, as compared to the susceptible Bora Bora strain. The transcription ratios obtained from real-time quantitative PCR were normalized with the two housekeeping genes RpL8 and RpS7 and shown as mean value (±SE) for three independent biological replicates. Genes significantly over-transcribed with transcription ratio ≥2 and P-value <0.05) are indicated by asterisks. ABY Les Abymes, SXM Saint Martin, BM Baie-Mahault, SF Saint-François, AB: Anse-Bertrand, DH Deshaies
Fig. 4
Fig. 4
Adult gene amplification levels for three cytochrome P450 monooxygenases (014614, CYP6M11, CYP9J23), one carboxyl/cholinesterase (CCEae3a), and one glutathione S-transferase (GSTe2) for the six Ae. aegypti populations of Guadeloupe and Saint Martin compared to the susceptible Bora Bora strain. The gene amplification levels obtained from real-time quantitative PCR were normalized with both 007808 and 005950 housekeeping genes and shown as mean value (±SE) over 22 to 24 individual DNA. The genes significantly amplified (ratio ≥2) are indicated by asterisks. ABY Les Abymes, SXM Saint Martin, BM Baie-Mahault, SF Saint-François, AB Anse-Bertrand, DH Deshaies
Fig. 5
Fig. 5
PCA for 18 variables including larval resistance levels regarding temephos and malathion, adult resistance levels regarding deltamethrin, adult transcription and amplification ratios of detoxification enzymes, and adult resistant Kdr allele frequencies, for the six mosquito populations tested. Information represented by axis 1-2 (a) and axis 1-3 (b) are shown

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