Fast emerging insecticide resistance in Aedes albopictus in Guangzhou, China: Alarm to the dengue epidemic

Dengue is one of the most serious mosquito-borne infectious diseases in the world. Aedes albopictus is the most invasive mosquito and one of the primary vectors of dengue. Vector control using insecticides is the only viable strategy to prevent dengue virus transmission. In Guangzhou, after the 2014 pandemic, massive insecticides have been implemented. Massive insecticide use may lead to the development of resistance, but few reports are available on the status of insecticide resistance in Guangzhou after 2014. In this study, Ae. albopictus were collected from four districts with varied dengue virus transmission intensity in Guangzhou from 2015 to 2017. Adult Ae. albopictus insecticide susceptibility to deltamethrin (0.03%), permethrin(0.25%), DDT(4%), malathion (0.8%) and bendiocarb (0.1%) was determined by the standard WHO tube test, and larval resistance bioassays were conducted using temephos, Bacillus thuringiensis israelensis (Bti), pyriproxyfen (PPF) and hexaflumuron. Mutations at the voltage-gated sodium channel (VGSC) gene and acetylcholinesterase (AChE) gene were analyzed. The effect of cytochrome P450s on the resistance of Ae. albopictus to deltamethrin was tested using the synergistic agent piperonyl butoxide (PBO). The results showed that Ae. albopictus populations have rapidly developed very high resistances to multiple commonly used insecticides at all study areas except malathion, Bti and hexaflumuron. We found 1534 codon mutations in the VGSC gene that were significantly correlated with the resistance to pyrethroids and DDT, and 11 synonymous mutations were also found in the gene. The resistance to deltamethrin can be significantly reduced by PBO but may generated cross-resistance to PPF. Fast emerging resistance in Ae. albopictus may affect mosquito management and threaten the prevention and control of dengue, similar to the resistance in Anopheles mosquitoes has prevented the elimination of malaria and call for timely and guided insecticide management. Author summary Guangzhou is the most epidemic area of dengue in China. Massive insecticides have been used to control the vector mosquito Ae. albopictus, as no specific vaccines are available for dengue. Regular monitoring of insecticide susceptibility is essential for insecticide resistance management. In this study, the insecticide resistances of Ae. albopictus in Guangzhou were comparatively analyzed from 2015 to 2017. The results displayed that Ae. albopictus had rapidly generated high resistance to the most commonly used adult insecticide pyrethroid (deltamethrin and permethrin) and larvicide organophosphate (temephos). The combination of malathion for adult mosquitoes and Bti or hexaflumuron for larvae might be a better choice for vector control. Resistance to deltamethrin can be significantly reduced by PBO but may generated cross-resistance to PPF. F1534S and F1534L mutations in the VGSC gene were significantly correlated with resistance to pyrethroids. This study indicated that the insecticide resistances had been generated in Ae. albopictus in Guangzhou which was correlated with the dengue epidemic responses.