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Aging partially restores the efficacy of malaria vector control in insecticide-resistant populations of Anopheles gambiae s.l. from Burkina Faso.

ABSTRACT: BACKGROUND: The operational impact of insecticide resistance on the effectiveness of long-lasting insecticide nets (LLINs) and indoor residual spraying (IRS) is poorly understood. One factor which may prolong the effectiveness of these tools in the field is the increase in insecticide susceptibility with mosquito age. In this study, LLINs and IRS were tested against young (three to five days) and old (17-19 days) pyrethroid resistant Anopheles gambiae s.l. from Burkina Faso. METHODS: Blood-fed adult Anopheles gambiae s.l. were collected from south-west Burkina Faso and identified to species/form level. Cohorts of the F1 progeny of An. gambiae s.s. S-forms were exposed to deltamethrin (0.05%) at three to five or 17-19 days post-emergence and tested for the frequency of the resistance allele 1014F. Isofemale lines of the M, S- form of An. gambiae s.s. and Anopheles arabiensis were exposed in WHO cone tests to either a) LLINs deployed in households for two years or (b) bendiocarb sprayed walls. RESULTS: Mortality rates in response to deltamethrin (0.05%) increased from levels indicative of strong resistance in three to five day old F1 mosquitoes, to near full susceptibility in the 17-19 day old cohort. On exposure to LLINs sampled from the field, the mortality rate in isofemale lines was higher in older mosquitoes than young (OR = 5.28, CI 95% = 2.81-9.92), although the mortality estimates were affected by the LLIN tested. In general, the LLINs sampled from the field performed poorly in WHO cone bioassays using either laboratory susceptible or field caught mosquito populations. Finally, there was a clear relationship between mortality and age on exposure to bendiocarb-sprayed walls, with older mosquitoes again proving more susceptible (OR = 3.39, CI 95% = 2.35-4.90). CONCLUSIONS: Age is a key factor determining the susceptibility of mosquitoes to insecticides, not only in laboratory studies, but in response to field-based vector control interventions. This has important implications for understanding the epidemiological impact of resistance. If mosquitoes old enough to transmit malaria are still being suppressed with available insecticides, is resistance potentially having less of an impact than often assumed? However, the poor performance of LLINs used in this study in Burkina Faso, is a cause for concern and requires urgent investigation.

SUBMITTER: Jones CM

PROVIDER: S-EPMC3312828 | biostudies-other | 2012

REPOSITORIES: biostudies-other

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Aging partially restores the efficacy of malaria vector control in insecticide-resistant populations of Anopheles gambiae s.l. from Burkina Faso.

Jones Christopher M CM Sanou Antoine A Guelbeogo Wamdaogo M WM Sagnon N'Fale N Johnson Paul C D PC Ranson Hilary H

Malaria journal 20120123

<h4>Background</h4>The operational impact of insecticide resistance on the effectiveness of long-lasting insecticide nets (LLINs) and indoor residual spraying (IRS) is poorly understood. One factor which may prolong the effectiveness of these tools in the field is the increase in insecticide susceptibility with mosquito age. In this study, LLINs and IRS were tested against young (three to five days) and old (17-19 days) pyrethroid resistant Anopheles gambiae s.l. from Burkina Faso.<h4>Methods</h ...[more]

PMID: 22269002

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Project description:BackgroundThe efficacy of long-lasting insecticidal nets (LLINs) in preventing malaria in Africa is threatened by insecticide resistance. Bioassays assessing 24-hour mortality post-LLIN exposure have established that resistance to the concentration of pyrethroids used in LLINs is widespread. However, although mosquitoes may no longer be rapidly killed by LLIN exposure, a delayed mortality effect has been shown to reduce the transmission potential of mosquitoes exposed to nets. This has been postulated to partially explain the continued efficacy of LLINs against pyrethroid-resistant populations. Burkina Faso is one of a number of countries with very high malaria burdens and pyrethroid-resistant vectors, where progress in controlling this disease has stagnated. We measured the impact of LLIN exposure on mosquito longevity in an area of the country with intense pyrethroid resistance to establish whether pyrethroid exposure was still shortening mosquito lifespan in this setting.MethodsWe quantified the immediate and delayed mortality effects of LLIN exposure using standard laboratory WHO cone tests, tube bioassays and experimental hut trials on Anopheles gambiae populations originating from the Cascades region of Burkina Faso using survival analysis and a Bayesian state-space model.ResultsFollowing single and multiple exposures to a PermaNet 2.0 LLIN only one of the four mosquito populations tested showed evidence of delayed mortality. No delayed mortality was seen in experimental hut studies using LLINs. A delayed mortality effect was only observed in WHO tube bioassays when deltamethrin concentration was increased above the standard diagnostic dose.ConclusionsAs mosquito pyrethroid-resistance increases in intensity, delayed effects from LLIN exposure are substantially reduced or absent. Given the rapid increase in resistance occurring in malaria vectors across Africa it is important to determine whether the failure of LLINs to shorten mosquito lifespan is now a widespread phenomenon as this will have important implications for the future of this pivotal malaria control tool.

Project description:Background and methodsA longitudinal Anopheles gambiae s.l. insecticide-resistance monitoring programme was established in four sentinel sites in Burkina Faso. For three years, between 2008 and 2010, WHO diagnostic dose assays were used to measure the prevalence of resistance to all the major classes of insecticides at the beginning and end of the malaria transmission season. Species identification and genotyping for target site mutations was also performed and the sporozoite rate in adults determined.ResultsAt the onset of the study, resistance to DDT and pyrethroids was already prevalent in An. gambiae s.l. from the south-west of the country but mosquitoes from the two sites in central Burkina Faso were largely susceptible. Within three years, DDT and permethrin resistance was established in all four sites. Carbamate and organophosphate resistance remains relatively rare and largely confined to the south-western areas although a small number of bendiocarb survivors were found in all sites by the final round of monitoring. The ace-1R target site resistance allele was present in all localities and its frequency exceeded 20% in 2010 in two of the sites. The frequency of the 1014F kdr mutation increased throughout the three years and by 2010, the frequency of 1014F in all sites combined was 0.02 in Anopheles arabiensis, 0.56 in An. gambiae M form and 0.96 in An. gambiae S form. This frequency did not differ significantly between the sites. The 1014S kdr allele was only found in An. arabiensis but its frequency increased significantly throughout the study (P = 0.0003) and in 2010 the 1014S allele frequency was 0.08 in An. arabiensis. Maximum sporozoite rates (12%) were observed in Soumousso in 2009 and the difference between sites is significant for each year.ConclusionPyrethroid and DDT resistance is now established in An. gambiae s.l. throughout Burkina Faso. Results from diagnostic dose assays are highly variable within and between rounds of testing, and hence it is important that resistance monitoring is carried out on more than one occasion before decisions on insecticide procurement for vector control are made. The presence of 1014S in An. gambiae s.l., in addition to 1014F, is not unexpected given the recent report of 1014S in Benin but highlights the importance of monitoring for both mutations throughout the continent. Future research must now focus on the impact that this resistance is having on malaria control in Burkina Faso.

Project description:BackgroundVector control activities, namely long-lasting insecticidal nets (LLIN) and indoor residual spraying (IRS), have contributed significantly to the decreasing malaria burden observed in The Gambia since 2008. Nevertheless, insecticide resistance may threaten such success; it is important to regularly assess the susceptibility of local malaria vectors to available insecticides.MethodsIn the transmission seasons of 2016 and 2017, Anopheles gambiae (s.l.) larvae were sampled in or around the nine vector surveillance sentinel sites of the Gambia National Malaria Control Programme (GNMCP) and in a few additional sampling points. Using WHO susceptibility bioassays, female adult mosquitoes were exposed to insecticide-impregnated papers. Molecular identification of sibling species and insecticide resistance molecular markers was done on a subset of 2000 female mosquitoes.ResultsA total of 4666 wild-caught female adult mosquitoes were exposed to either permethrin (n = 665), deltamethrin (n = 744), DDT (n = 1021), bendiocarb (n = 990) or pirimiphos-methyl (n = 630) insecticide-impregnated papers and control papers (n = 616). Among the 2000 anophelines, 1511 (80.7%) were Anopheles arabiensis, 204 (10.9%) Anopheles coluzzii, 75 (4%) Anopheles gambiae (s.s.), and 83 (4.4%) An. gambiae (s.s.) and An. coluzzii hybrids. There was a significant variation in the composition and species distribution by regions and year, P = 0.009. Deltamethrin, permethrin and DDT resistance was found in An. arabiensis, especially in the coastal region, and was mediated by Vgsc-1014F/S mutations (odds ratio = 34, P = 0.014). There was suspected resistance to pirimiphos-methyl (actellic 300CS) in the North Bank Region although only one survivor had the Ace-1-119S mutation.ConclusionsAs no confirmed resistance to bendiocarb and actellic 300CS was detected, the national malaria control programme can continue using these insecticides for IRS. Nevertheless, the detection of Ace-1 119S mutation warrants extensive monitoring. The source of insecticide pressure driving insecticide resistance to pyrethroids and DDT detected at the coastal region should be further investigated in order to properly manage the spread of resistance in The Gambia.

Project description:Many studies have shown the role of agriculture in the selection and spread of resistance of Anopheles gambiae s.l. to insecticides. However, no study has directly demonstrated the presence of insecticides in breeding sources as a source of selection for this resistance. It is in this context that we investigated the presence of pesticide residues in breeding habitats and their formal involvement in vector resistance to insecticides in areas of West Africa with intensive farming. This study was carried out from June to November 2013 in Dano, southwest Burkina Faso in areas of conventional (CC) and biological cotton (BC) growing. Water and sediment samples collected from breeding sites located near BC and CC fields were submitted for chromatographic analysis to research and titrate the residual insecticide content found there. Larvae were also collected in these breeding sites and used in toxicity tests to compare their mortality to those of the susceptible strain, Anopheles gambiae Kisumu. All tested mosquitoes (living and dead) were analyzed by PCR for species identification and characterization of resistance genes. The toxicity analysis of water from breeding sites showed significantly lower mortality rates in breeding site water from biological cotton (WBC) growing sites compared to that from conventional cotton (WCC) sites respective to both An. gambiae Kisumu (WBC: 80.75% vs WCC: 92.75%) and a wild-type strain (49.75% vs 66.5%). The allele frequencies L1014F, L1014S kdr, and G116S ace -1R mutations conferring resistance, respectively, to pyrethroids and carbamates / organophosphates were 0.95, 0.4 and 0.12. Deltamethrin and lambda-cyhalothrin were identified in the water samples taken in October/November from mosquitoes breeding in the CC growing area. The concentrations obtained were respectively 0.0147ug/L and 1.49 ug/L to deltamethrin and lambdacyhalothrin. Our results provided evidence by direct analysis (biological and chromatographic tests) of the role of agriculture as a source of selection pressure on vectors to insecticides used in growing areas.

Project description:BackgroundRelease of gene-drive mutants to suppress Anopheles mosquito reproduction is a promising method of malaria control. However, many scientific, regulatory and ethical questions remain before transgenic mosquitoes can be utilised in the field. At a behavioural level, gene-drive carrying mutants should be at least as sexually attractive as the wildtype populations they compete against, with a key element of Anopheles copulation being acoustic courtship. We analysed sound emissions and acoustic preference in a doublesex mutant previously used to collapse Anopheles gambiae (s.l.) cages.MethodsAnopheles rely on flight tones produced by the beating of their wings for acoustic mating communication. We assessed the impact of disrupting a female-specific isoform of the doublesex gene (dsxF) on the wing beat frequency (WBF; measured as flight tone) of males (XY) and females (XX) in homozygous dsxF- mutants (dsxF-/-), heterozygous dsxF- carriers (dsxF+/-) and G3 dsxF+ controls (dsxF+/+). To exclude non-genetic influences, we controlled for temperature and wing length. We used a phonotaxis assay to test the acoustic preferences of mutant and control mosquitoes.ResultsA previous study showed an altered phenotype only for dsxF-/- females, who appear intersex, suggesting that the female-specific dsxF allele is haplosufficient. We identified significant, dose-dependent increases in the WBF of both dsxF-/- and dsxF+/- females compared to dsxF+/+ females. All female WBFs remained significantly lower than male equivalents, though. Males showed stronger phonotactic responses to the WBFs of control dsxF+/+ females than to those of dsxF+/- and dsxF-/- females. We found no evidence of phonotaxis in any female genotype. No male genotypes displayed any deviations from controls.ConclusionsA prerequisite for anopheline copulation is the phonotactic attraction of males towards female flight tones within mating swarms. Reductions in mutant acoustic attractiveness diminish their mating efficiency and thus the efficacy of population control efforts. Caged population assessments may not successfully reproduce natural mating scenarios. We propose to amend existing testing protocols to better reflect competition between mutants and target populations. Our findings confirm that dsxF disruption has no effect on males; for some phenotypic traits, such as female WBFs, the effects of dsxF appear dose-dependent rather than haplosufficient.

Project description:BackgroundTwenty-seven villages were selected in southwest Burkina Faso to implement new vector control strategies in addition to long lasting insecticidal nets (LLINs) through a Randomized Controlled Trial (RCT). We conducted entomological surveys in the villages during the dry cold season (January 2017), dry hot season (March 2017) and rainy season (June 2017) to describe malaria vectors bionomics, insecticide resistance and transmission prior to this trial.MethodsWe carried out hourly catches (from 17:00 to 09:00) inside and outside 4 houses in each village using the Human Landing Catch technique. Mosquitoes were identified using morphological taxonomic keys. Specimens belonging to the Anopheles gambiae complex and Anopheles funestus group were identified using molecular techniques as well as detection of Plasmodium falciparum infection and insecticide resistance target-site mutations.ResultsEight Anopheles species were detected in the area. Anopheles funestus s.s was the main vector during the dry cold season. It was replaced by Anopheles coluzzii during the dry hot season whereas An. coluzzii and An. gambiae s.s. were the dominant species during the rainy season. Species composition of the Anopheles population varied significantly among seasons. All insecticide resistance mechanisms (kdr-w, kdr-e and ace-1 target site mutations) investigated were found in each members of the An. gambiae complex but at different frequencies. We observed early and late biting phenotypes in the main malaria vector species. Entomological inoculation rates were 2.61, 2.67 and 11.25 infected bites per human per month during dry cold season, dry hot season and rainy season, respectively.ConclusionThe entomological indicators of malaria transmission were high despite the universal coverage with LLINs. We detected early and late biting phenotypes in the main malaria vector species as well as physiological insecticide resistance mechanisms. These data will be used to evaluate the impact of complementary tools to LLINs in an upcoming RCT.

Dataset Information

Aging partially restores the efficacy of malaria vector control in insecticide-resistant populations of Anopheles gambiae s.l. from Burkina Faso.

Publications

Aging partially restores the efficacy of malaria vector control in insecticide-resistant populations of Anopheles gambiae s.l. from Burkina Faso.

Similar Datasets

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