Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release program

Abstract Background Dengue suppression often relies on control of the mosquito vector, Aedes aegypti, through applications of insecticides of which the pyrethroid group has played a dominant role. Insecticide resistance is prevalent in Ae. aegypti around the world, and the resulting reduction of ins...

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Main Authors: Nancy M. Endersby-Harshman, AboElgasim Ali, Basim Alhumrani, Mohammed Abdullah Alkuriji, Mohammed B. Al-Fageeh, Abdulaziz Al-Malik, Mohammed S. Alsuabeyl, Samia Elfekih, Ary A. Hoffmann
Format: Article
Language:English
Published: BMC 2021-07-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-021-04867-3
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spelling doaj-81e3896cdc004f5fa3a9d66e10afab512021-07-18T11:29:48ZengBMCParasites & Vectors1756-33052021-07-0114111310.1186/s13071-021-04867-3Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release programNancy M. Endersby-Harshman0AboElgasim Ali1Basim Alhumrani2Mohammed Abdullah Alkuriji3Mohammed B. Al-Fageeh4Abdulaziz Al-Malik5Mohammed S. Alsuabeyl6Samia Elfekih7Ary A. Hoffmann8PEARG, School of BioSciences, Bio21 Institute, The University of MelbourneKing Abdul-Aziz City for Science and Technology (KACST)King Abdul-Aziz City for Science and Technology (KACST)King Abdul-Aziz City for Science and Technology (KACST)King Abdul-Aziz City for Science and Technology (KACST)King Abdul-Aziz City for Science and Technology (KACST)King Abdul-Aziz City for Science and Technology (KACST)PEARG, School of BioSciences, Bio21 Institute, The University of MelbournePEARG, School of BioSciences, Bio21 Institute, The University of MelbourneAbstract Background Dengue suppression often relies on control of the mosquito vector, Aedes aegypti, through applications of insecticides of which the pyrethroid group has played a dominant role. Insecticide resistance is prevalent in Ae. aegypti around the world, and the resulting reduction of insecticide efficacy is likely to exacerbate the impact of dengue. Dengue has been a public health problem in Saudi Arabia, particularly in Jeddah, since its discovery there in the 1990s, and insecticide use for vector control is widespread throughout the city. An alternative approach to insecticide use, based on blocking dengue transmission in mosquitoes by the endosymbiont Wolbachia, is being trialed in Jeddah following the success of this approach in Australia and Malaysia. Knowledge of insecticide resistance status of mosquito populations in Jeddah is a prerequisite for establishing a Wolbachia-based dengue control program as releases of Wolbachia mosquitoes succeed when resistance status of the release population is similar to that of the wild population. Methods WHO resistance bioassays of mosquitoes with deltamethrin, permethrin and DDT were used in conjunction with TaqMan® SNP Genotyping Assays to characterize mutation profiles of Ae. aegypti. Results Screening of the voltage-sensitive sodium channel (Vssc), the pyrethroid target site, revealed mutations at codons 989, 1016 and 1534 in Ae. aegypti from two districts of Jeddah. The triple mutant homozygote (1016G/1534C/989P) was confirmed from Al Safa and Al Rawabi. Bioassays with pyrethroids (Type I and II) and DDT showed that mosquitoes were resistant to each of these compounds based on WHO definitions. An association between Vssc mutations and resistance was established for the Type II pyrethroid, deltamethrin, with one genotype (989P/1016G/1534F) conferring a survival advantage over two others (989S/1016V/1534C and the triple heterozygote). An indication of synergism of Type I pyrethroid activity with piperonyl butoxide suggests that detoxification by cytochrome P450s accounts for some of the pyrethroid resistance response in Ae. aegypti populations from Jeddah. Conclusions The results provide a baseline for monitoring and management of resistance as well as knowledge of Vssc genotype frequencies required in Wolbachia release populations to ensure homogeneity with the target field population. Vssc mutation haplotypes observed show some similarity with those from Ae. aegypti in southeast Asia and the Indo-Pacific, but the presence of the triple mutant haplotype in three genotypes indicates that the species in this region may have a unique population history. Graphical Abstracthttps://doi.org/10.1186/s13071-021-04867-3DengueMosquitoTarget-siteKnockdown resistance (kdr)PermethrinDeltamethrin
collection DOAJ
language English
format Article
sources DOAJ
author Nancy M. Endersby-Harshman
AboElgasim Ali
Basim Alhumrani
Mohammed Abdullah Alkuriji
Mohammed B. Al-Fageeh
Abdulaziz Al-Malik
Mohammed S. Alsuabeyl
Samia Elfekih
Ary A. Hoffmann
spellingShingle Nancy M. Endersby-Harshman
AboElgasim Ali
Basim Alhumrani
Mohammed Abdullah Alkuriji
Mohammed B. Al-Fageeh
Abdulaziz Al-Malik
Mohammed S. Alsuabeyl
Samia Elfekih
Ary A. Hoffmann
Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release program
Parasites & Vectors
Dengue
Mosquito
Target-site
Knockdown resistance (kdr)
Permethrin
Deltamethrin
author_facet Nancy M. Endersby-Harshman
AboElgasim Ali
Basim Alhumrani
Mohammed Abdullah Alkuriji
Mohammed B. Al-Fageeh
Abdulaziz Al-Malik
Mohammed S. Alsuabeyl
Samia Elfekih
Ary A. Hoffmann
author_sort Nancy M. Endersby-Harshman
title Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release program
title_short Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release program
title_full Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release program
title_fullStr Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release program
title_full_unstemmed Voltage-sensitive sodium channel (Vssc) mutations associated with pyrethroid insecticide resistance in Aedes aegypti (L.) from two districts of Jeddah, Kingdom of Saudi Arabia: baseline information for a Wolbachia release program
title_sort voltage-sensitive sodium channel (vssc) mutations associated with pyrethroid insecticide resistance in aedes aegypti (l.) from two districts of jeddah, kingdom of saudi arabia: baseline information for a wolbachia release program
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2021-07-01
description Abstract Background Dengue suppression often relies on control of the mosquito vector, Aedes aegypti, through applications of insecticides of which the pyrethroid group has played a dominant role. Insecticide resistance is prevalent in Ae. aegypti around the world, and the resulting reduction of insecticide efficacy is likely to exacerbate the impact of dengue. Dengue has been a public health problem in Saudi Arabia, particularly in Jeddah, since its discovery there in the 1990s, and insecticide use for vector control is widespread throughout the city. An alternative approach to insecticide use, based on blocking dengue transmission in mosquitoes by the endosymbiont Wolbachia, is being trialed in Jeddah following the success of this approach in Australia and Malaysia. Knowledge of insecticide resistance status of mosquito populations in Jeddah is a prerequisite for establishing a Wolbachia-based dengue control program as releases of Wolbachia mosquitoes succeed when resistance status of the release population is similar to that of the wild population. Methods WHO resistance bioassays of mosquitoes with deltamethrin, permethrin and DDT were used in conjunction with TaqMan® SNP Genotyping Assays to characterize mutation profiles of Ae. aegypti. Results Screening of the voltage-sensitive sodium channel (Vssc), the pyrethroid target site, revealed mutations at codons 989, 1016 and 1534 in Ae. aegypti from two districts of Jeddah. The triple mutant homozygote (1016G/1534C/989P) was confirmed from Al Safa and Al Rawabi. Bioassays with pyrethroids (Type I and II) and DDT showed that mosquitoes were resistant to each of these compounds based on WHO definitions. An association between Vssc mutations and resistance was established for the Type II pyrethroid, deltamethrin, with one genotype (989P/1016G/1534F) conferring a survival advantage over two others (989S/1016V/1534C and the triple heterozygote). An indication of synergism of Type I pyrethroid activity with piperonyl butoxide suggests that detoxification by cytochrome P450s accounts for some of the pyrethroid resistance response in Ae. aegypti populations from Jeddah. Conclusions The results provide a baseline for monitoring and management of resistance as well as knowledge of Vssc genotype frequencies required in Wolbachia release populations to ensure homogeneity with the target field population. Vssc mutation haplotypes observed show some similarity with those from Ae. aegypti in southeast Asia and the Indo-Pacific, but the presence of the triple mutant haplotype in three genotypes indicates that the species in this region may have a unique population history. Graphical Abstract
topic Dengue
Mosquito
Target-site
Knockdown resistance (kdr)
Permethrin
Deltamethrin
url https://doi.org/10.1186/s13071-021-04867-3
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