Long-term trends in Anopheles gambiae insecticide resistance in Côte d’Ivoire

Abstract

BackgroundMalaria control is heavily dependent on the use of insecticides that target adult mosquito vectors via insecticide treated nets (ITNs) or indoor residual spraying (IRS). Four classes of insecticide are approved for IRS but only pyrethroids are available for ITNs. The rapid rise in insecticide resistance in African malaria vectors has raised alarms about the sustainability of existing malaria control activities. This problem might be particularly acute in Côte d’Ivoire where resistance to all four insecticide classes has recently been recorded. Here we investigate temporal trends in insecticide resistance across the ecological zones of Côte d’Ivoire to determine whether apparent pan-African patterns of increasing resistance are detectable and consistent across insecticides and areas.MethodsWe combined data on insecticide resistance from a literature review, and bioassays conducted on field-caught Anopheles gambiae mosquitoes for the four WHO-approved insecticide classes for ITN/IRS. The data were then mapped using Geographical Information Systems (GIS) and the IR mapper tool to provide spatial and temporal distribution data on insecticide resistance in An. gambiae sensu lato from Côte d’Ivoire between 1993 and 2014.ResultsBioassay mortality decreased over time for all insecticide classes, though with significant spatiotemporal variation, such that stronger declines were observed in the southern ecological zone for DDT and pyrethroids than in the central zone, but with an apparently opposite effect for the carbamate and organophosphate. Variation in relative abundance of the molecular forms, coupled with dramatic increase in kdr 1014F frequency in M forms (An. coluzzii) seems likely to be a contributory factor to these patterns. Although records of resistance across insecticide classes have become more common, the number of classes tested in studies has also increased, precluding a conclusion that multiple resistance has also increased.ConclusionOur analyses attempted synthesis of 22 years of bioassay data from Côte d’Ivoire, and despite a number of caveats and potentially confounding variables, suggest significant but spatially-variable temporal trends in insecticide resistance. In the light of such spatio-temporal dynamics, regular, systematic and spatially-expanded monitoring is warranted to provide accurate information on insecticide resistance for control programme management.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-014-0500-z) contains supplementary material, which is available to authorized users.

Mapping trends in insecticide resistance phenotypes in African malaria vectors

“…Although there is evidence that pyrethroid resistance in African malaria vector populations is increasing [6,7], the wide array of field studies that are available do not provide a spatially comprehensive time series of resistance trends [8]. Quantifying these trends will improve our understanding of the historical spread of resistance and assist in designing insecticide resistance management strategies [9].…”

Reduced long-lasting insecticidal net efficacy and pyrethroid insecticide resistance are associated with over-expression ofCYP6P4, CYP6P3andCYP6Z1in populations ofAnopheles coluzziifrom South-East Côte d’Ivoire

“…One notable difference in our dataset, compared to previous work in Agboville [7], was the finding of bendiocarb susceptibility. This may be attributable to small-scale spatial and longitudinal heterogeneity in resistance, which can be highly dynamic [37,44], and/or phenotypic differences between vector species.…”

“…Resistance to pyrethroid and carbamate insecticides in Anopheles mosquitoes was first reported from the central region of Côte d'Ivoire in the early 1990s [4][5][6][7]. Subsequently, local resistance to the major insecticide classes recommended by the World Health Organization (WHO) for adult mosquito control -pyrethroids, carbamates, organophosphates, and organochlorines -evolved rapidly [8][9][10] and has been increasing in intensity, driven largely by selective pressures imposed by contemporaneous scale-up of public health vector control interventions (including those targeting malaria, trypanosomiasis and onchocerciasis vectors) and use of agricultural pesticides [7,[11][12][13][14]. This escalation in resistance has now begun to compromise the insecticidal efficacy and community-wide impact of conventional, pyrethroid LLINs in Côte d'Ivoire [14,15], although some levels of personal protection may still remain [15][16][17].…”

“…Amongst vector populations across Côte d'Ivoire, the L1014F kdr mutation is pervasive and has been implicated in some longitudinal trends in decreasing DDT and pyrethroid susceptibility [7,11]; L1014S kdr and N1575Y resistance mutations have also been detected but at much lower frequencies [18]. Extreme carbamate (bendiocarb) resistance and pyrethroid cross-resistance in local An.…”

Resistance to pirimiphos-methyl in West AfricanAnophelesis spreading via duplication and introgression of theAce1locus

“…The lack of clear signals of pirimiphos-methyl adaptation other than Ace1 in this population may reflect its collection at an early stage of the development of pirimiphos-methyl resistance in West Africa (Edi et al 2014b). Therefore, our genome-wide analyses would only capture pre-existing variants that were enriched in the resistant specimens.…”