Insecticide resistance in Culex quinquefasciatus from Zanzibar: implications for vector control programmes

Christopher M Jones,Khalfan Mohammed,Bakari O Khatib,Juma Mcha,Abdullah S Ali,Silas Majambere,Hilary Ranson,Camille Machin,Louise A Kelly-Hope

doi:10.1186/1756-3305-5-78

Abstract

BackgroundZanzibar has a long history of lymphatic filariasis (LF) caused by the filarial parasite Wuchereria bancrofti, and transmitted by the mosquito Culex quinquefasciatus Say. The LF Programme in Zanzibar has successfully implemented mass drug administration (MDA) to interrupt transmission, and is now in the elimination phase. Monitoring infections in mosquitoes, and assessing the potential role of interventions such as vector control, is important in case the disease re-emerges as a public health problem. Here, we examine Culex mosquito species from the two main islands to detect W. bancrofti infection and to determine levels of susceptibility to the insecticides used for vector control.MethodsCulex mosquitoes collected during routine catches in Vitongoji, Pemba Island, and Makadara, Unguja Island were tested for W. bancrofti infection using PCR. Insecticide bioassays on Culex mosquitoes were performed to determine susceptibility to permethrin, deltamethrin, lambda-cyhalothrin, DDT and bendiocarb. Additional synergism assays with piperonyl butoxide (PBO) were used for lambda-cyhalothrin. Pyrosequencing was used to determine the kdr genotype and sequencing of the mitochondrial cytochrome oxidase I (mtCOI) subunit performed to identify ambiguous Culex species.ResultsNone of the wild-caught Culex mosquitoes analysed were found to be positive for W. bancrofti. High frequencies of resistance to all insecticides were found in Wete, Pemba Island, whereas Culex from the nearby site of Tibirinzi (Pemba) and in Kilimani, Unguja Island remained relatively susceptible. Species identification confirmed that mosquitoes from Wete were Culex quinquefasciatus. The majority of the Culex collected from Tibirinzi and all from Kilimani could not be identified to species by molecular assays. Two alternative kdr alleles, both resulting in a L1014F substitution were detected in Cx. quinquefasciatus from Wete with no homozygote susceptible detected. Metabolic resistance to pyrethroids was also implicated by PBO synergism assays.ConclusionsResults from the xenomonitoring are encouraging for the LF programme in Zanzibar. However, the high levels of pyrethroid resistance found in the principle LF vector in Pemba Island will need to be taken into consideration if vector control is to be implemented as part of the elimination programme.

Highlights

Zanzibar has a long history of lymphatic filariasis (LF) caused by the filarial parasite Wuchereria bancrofti, and transmitted by the mosquito Culex quinquefasciatus Say
The Zanzibar archipelago has a long history of lymphatic filariasis (LF), a disabling mosquito-borne disease caused by the filarial parasite Wuchereria bancrofti [1,2,3,4,5,6]
Given the post-mass drug administration (MDA) phase and importance of surveillance in Zanzibar, this study aimed to examine Culex species to detect W. bancrofti infection from routine entomological collections and to determine levels of susceptibility to insecticides used in vector control programmes

Summary

Introduction

Zanzibar has a long history of lymphatic filariasis (LF) caused by the filarial parasite Wuchereria bancrofti, and transmitted by the mosquito Culex quinquefasciatus Say. The Zanzibar archipelago has a long history of lymphatic filariasis (LF), a disabling mosquito-borne disease caused by the filarial parasite Wuchereria bancrofti [1,2,3,4,5,6]. The mosquito species Culex quinquefasciatus Say, is the most important vector of W. bancrofti in the East African coast and the islands of the Indian Ocean, including Zanzibar, Anopheles gambiae s.l and An. funestus play a role in selected areas [7,8,9,10]. Cx. quinquefasciatus is a member of the Culex pipiens complex Linnaeus and one of the main subspecies found in Africa [11,12,13] It is efficient at maintaining low levels of microfilariae (Mf) within a population, highly anthropophilic, and predominately bites at night. In Zanzibar, W. bancrofti Mf rates have ranged from 0.3% to 20.3% in Culex species [1,2,3,6,7,14], unpublished data

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