Sympatric Populations of the Anopheles gambiae Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids

Williams, Jessica; Ingham, Victoria A.; Morris, Marion; Toé, Hyacinthe K.; Hien, Aristide Sawdetuo; Morgan, John C.; Dabiré, Roch K.; Guelbeogo, W Moussa; Sagnon, N’Falé; Ranson, Hilary

doi:10.3390/insects13030247

Cited by 21 publications

(22 citation statements)

References 55 publications

(84 reference statements)

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“…coluzzii strains Three insecticide resistant An. coluzzii strains from Burkina Faso: VK7 2014, Banfora M and Tiefora (origin and colonization date shown in Supporting Information, Table S1), that show mortality less than 13% after 1 h exposure to standard WHO bioassays with the pyrethroids deltamethrin, permethrin and alpha cypermethrin and to the organochloride DDT (previously described in 19,20 ), were tested for the presence of VGSC mutations L995F, I1527T, P1874S/L and V402L (Fig. 1).…”

Section: Resultsmentioning

confidence: 99%

In vivo functional validation of the V402L voltage gated sodium channel mutation in the malaria vector An. gambiae

Williams

Cowlishaw

Sanou

et al. 2021

Pest Management Science

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BACKGROUND: Pyrethroids are the most widely used insecticides for the control of malaria transmitting Anopheles gambiae mosquitoes and rapid increase in resistance to this insecticide class is of major concern. Pyrethroids target the Voltage Gated Sodium Channels (VGSCs), that have a key role in the normal function of the mosquitoes' nervous system. VGSC mutations L995F and L995S have long been associated with pyrethroid resistance and screening for their presence is routine in insecticide resistance management programs. Recently, a VGSC haplotype containing two amino acid substitutions associated with resistance in other species, V402L and I1527T, was identified. These two VGSC mutations are found in tight linkage and are mutually exclusive to the classical L995F/S mutations.RESULTS: We identify the presence of the V402L-I1527T haplotype in resistant An. coluzzii colonized strains and in field populations from Burkina Faso, at frequencies higher than previously reported; in some cases almost reaching fixation. Functional validation of V402L in insecticide resistance using a CRISPR/Cas9 genome modified line showed that it confers reduced mortality after exposure to all tested pyrethroids and DDT, but at lower levels compared to L995F. In contrast to L995F however, no fitness costs were identified for mosquitoes carrying V402L under laboratory conditions. CONCLUSION: The V402L substitution confers pyrethroid resistance in An. gambiae in the absence of any other VGSC substitution and/or alternative resistance mechanisms. The lower fitness cost associated with this kdr mutation may provide a selective advantage over the classical kdr in some settings and genotyping at this locus should be added in the list of resistant alleles for routine screening.

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Section: Resultsmentioning

confidence: 99%

In vivo functional validation of the V402L voltage gated sodium channel mutation in the malaria vector An. gambiae

Williams

Cowlishaw

Sanou

et al. 2021

Pest Management Science

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“…Genes implicated in the cuticular hydrocarbon (CHC) synthetic pathway are upregulated in Banfora M, Bakaridjan and Gaoua-ara strains, though downregulated in Tiefora and VK7 2014, and it seems that cuticular resistance may be particularly signi cant in Gaoua-ara. 20 Using a commercially available dust product, sold for the control of household pest insects, this study provides a dramatic demonstration of the potential to overcome pyrethroid resistance mechanisms by manipulating the properties of crystalline insecticides. There is a very limited number of insecticides available for use in public health, and the discovery and development of new compounds is slow and expensive.…”

Section: Discussionmentioning

confidence: 99%

Overcoming Insecticide Resistance in Anopheles Mosquitoes by Using Faster-acting Solid Forms of Deltamethrin

Carson

Erriah

Herodotou

et al. 2023

Preprint

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Background: Controlling malaria-transmitting Anopheles mosquitoes with pyrethroid insecticides is becoming increasingly challenging because of widespread resistance amongst vector populations. The development of new insecticides and insecticidal formulations is time consuming and costly, however. A more active crystalline form of deltamethrin, prepared by heating the commercial crystalline form, previously was reported to be 12-times faster acting against susceptible North American Anopheles quadrimaculatusmosquitoes. Herein we investigate whether heat-activated deltamethrin dispersed on chalk can overcome various resistance mechanisms amongst five West African Anophelesstrains and evaluate its long-term sustained lethality. Methods: The more active deltamethrin form was generated in a commercial dust containing deltamethrin by heating the material as purchased. Tarsal contact bioassays were conducted to investigate its efficacy, potency, and speed of action against resistant Anophelespopulations compared to the commercially available form of deltamethrin dust. Results: In all cases, D-Fense Dust heated to generate the more active form of deltamethrin was substantially more effective than the commercially available formulation. 100% of both Banfora and Kisumu populations were knocked down 10 minutes post-exposure with no recovery afterwards. Gaoua-ara and Tiefora strains exhibited 100% knockdown within 15 minutes, and the VK7 2014 strain exhibited 100% knockdown within 20 minutes. In all cases, 100% mortality was observed 24 hours post-exposure. Conversely, the commercial formulation (unheated) resulted in less than 4% mortality amongst VK7, Banfora, and Gaoua-ara populations by 24 hours, and Tiefora and Kisumu mosquitoes experienced 14 and 47% mortality by 24 hours, respectively. The heat-activated dust maintained comparable efficacy 6 months after heating. Conclusions: The heat-activated form of commercial deltamethrin D-Fense Dust outperformed the material as purchased, dramatically increasing efficacy against all tested pyrethroid-resistant strains. This increase in lethality was retained for six months of storage under ambient conditions in the laboratory. Higher energy forms of commonly used insecticides may be employed to overcome various resistance mechanisms seen in African Anopheles mosquitoes through more rapid uptake of insecticide molecules from their respective solid surfaces. That is, resistant mosquitoes can be killed with an insecticide to which they are resistant without altering the molecular composition of the insecticide.

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“…Pyrethroidresistance is widely spread across all regions in Benin [30][31][32][33][34] . In fact, this situation is associated with the recent massive deployment of LLINs across endemic countries for control of malaria, which led to selection pressure on mosquito vectors [35,36] . In addition, the use of pyrethoids in agriculture in the study area as reported in many other rural settings in Benin [37,38] might have contributed to the high frequency of kdr mutation recorded.…”

Section: Discussionmentioning

confidence: 99%

Seasonal change in species composition and target-site mutations in Anopheles gambiae s.l. in the severe drought area of Kandi, North-eastern Benin

Govoétchan¹,

Sovi²,

Ossè³

et al. 2022

Int. J. Mosq. Res.

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The persistence of malaria transmission in areas with very arid environmental conditions remains enigmatic. The present study investigated seasonal variation of mosquito species composition and Kdr and Ace-1 mutations in Anopheles gambiae s.l. in the very arid district of Kandi in North-eastern Benin. Adult mosquitoes were sampled over 1 year using both human landing catches (HLC) and pyrethrum spray catches in 4 villages belonging to 2 areas of different levels of aridity. The collections were carried out on a bi-monthly basis in the wet season, and once every month in the dry season to better capture the entomological situation in drought period. Females An. gambiae s.l. specimens were kept aside and analysed by PCR for species identification. Presence of kdr and Ace-1 mutations was also assessed in the An. gambiae s.l. collection. A total of 2,211 host-seeking mosquitoes belonging to 15 species were collected in the study area. An. gambiae s.l. was the most abundant species and represented 67% of the collection. Other Anopheles species were found at very low frequency among which An. funestus, An. pharoensis, An. broheri and An. coustani. Molecular species identification showed in dry season a significantly higher frequency of An. coluzzii over An. gambiae s. s. in both less dry (70% vs 29% with p < 0.001) and driest (70% vs 30% and p = 0.034) areas of the district of Kandi. In the rainy season, there was similar frequency of An. coluzzii and An. gambiae s. s. in the less arid area (53% vs 45%; p = 0.153), while An. coluzzii remained significantly predominant (62% vs 38%; p = 0.012) in the driest zone. The frequency of kdr mutation was significantly higher in dry season than in rainy season (93% vs 84%; p < 0.001), while no Ace-1 mutation was detected in the collection. In the current context of climate change marked by increasingly high temperatures and longer droughts, suitable vector control should be designed taking into account characteristics of the vector population maintaining malaria transmission in such arid environmental conditions.

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Sympatric Populations of the Anopheles gambiae Complex in Southwest Burkina Faso Evolve Multiple Diverse Resistance Mechanisms in Response to Intense Selection Pressure with Pyrethroids

Cited by 21 publications

References 55 publications

In vivo functional validation of the V402L voltage gated sodium channel mutation in the malaria vector An. gambiae

In vivo functional validation of the V402L voltage gated sodium channel mutation in the malaria vector An. gambiae

Overcoming Insecticide Resistance in Anopheles Mosquitoes by Using Faster-acting Solid Forms of Deltamethrin

Seasonal change in species composition and target-site mutations in Anopheles gambiae s.l. in the severe drought area of Kandi, North-eastern Benin

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