Multimodal Pyrethroid Resistance in Malaria Vectors, Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus s.s. in Western Kenya

AbstractCDC (Communicable Disease Center) light-traps were compared with human-bait collections as an alternative method for sampling malaria vectors in two villages of western Kenya. The numbers of Anopheles funestus Giles and Anopheles gambiae sensu lato Giles in CDC light-trap collections were significantly correlated to the numbers caught in human-bait collections, but in Anopheles arabiensis Patton the two collections were not significantly correlated. Most of the female vectors collected in the traps were unfed. Parity of A. arabiensis collected in CDC light-traps (44.3%) was significantly lower than the rate obtained from females caught on human-bait (54.5%). Although CDC light-traps provide a cheap and convenient method for collecting vectors, further studies should nevertheless be undertaken to determine the influence of species-specific variation in the sizes and age-structure of collections because such variations can affect the epidemiological interpretation of the data.

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Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania

Malaria Journal ◽

10.1186/s12936-020-03483-3 ◽

2020 ◽

Vol 19 (1) ◽

Author(s):

Polius G. Pinda ◽

Claudia Eichenberger ◽

Halfan S. Ngowo ◽

Dickson S. Msaky ◽

Said Abbasi ◽

...

Keyword(s):

Insecticide Resistance ◽

Malaria Transmission ◽

Anopheles Arabiensis ◽

Pyrethroid Resistance ◽

Anopheles Funestus ◽

Indoor Residual Spraying ◽

Sub Saharan Africa ◽

World Health ◽

Malaria Vectors ◽

South Eastern

Abstract Background Long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) have greatly reduced malaria transmission in sub-Saharan Africa, but are threatened by insecticide resistance. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus are now implicated in > 80% of malaria infections, even in villages where the species occurs at lower densities than the other vector, Anopheles arabiensis. This study compared the insecticide resistance phenotypes between the two malaria vectors in an area where pyrethroid-LLINs are widely used. Methods The study used the World Health Organization (WHO) assays with 1×, 5× and 10× insecticide doses to assess levels of resistance, followed by synergist bioassays to understand possible mechanisms of the observed resistance phenotypes. The tests involved adult mosquitoes collected from three villages across two districts in south-eastern Tanzania and included four insecticide classes. Findings At baseline doses (1×), both species were resistant to the two candidate pyrethroids (permethrin and deltamethrin), but susceptible to the organophosphate (pirimiphos-methyl). Anopheles funestus, but not An. arabiensis was also resistant to the carbamate (bendiocarb). Both species were resistant to DDT in all villages except in one village where An. arabiensis was susceptible. Anopheles funestus showed strong resistance to pyrethroids, surviving the 5× and 10× doses, while An. arabiensis reverted to susceptibility at the 5× dose. Pre-exposure to the synergist, piperonyl butoxide (PBO), enhanced the potency of the pyrethroids against both species and resulted in full susceptibility of An. arabiensis (> 98% mortality). However, for An. funestus from two villages, permethrin-associated mortalities after pre-exposure to PBO only exceeded 90% but not 98%. Conclusions In south-eastern Tanzania, where An. funestus dominates malaria transmission, the species also has much stronger resistance to pyrethroids than its counterpart, An. arabiensis, and can survive more classes of insecticides. The pyrethroid resistance in both species appears to be mostly metabolic and may be partially addressed using synergists, e.g. PBO. These findings may explain the continued persistence and dominance of An. funestus despite widespread use of pyrethroid-treated LLINs, and inform new intervention choices for such settings. In short and medium-term, these may include PBO-based LLINs or improved IRS with compounds to which the vectors are still susceptible.

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Eave tubes for malaria control in Africa: prototyping and evaluation against Anopheles gambiae s.s. and Anopheles arabiensis under semi-field conditions in western Kenya

Malaria Journal ◽

10.1186/s12936-017-1926-5 ◽

2017 ◽

Vol 16 (1) ◽

Cited By ~ 8

Author(s):

Janneke Snetselaar ◽

Basilio N. Njiru ◽

Beatrice Gachie ◽

Phillip Owigo ◽

Rob Andriessen ◽

...

Keyword(s):

Anopheles Gambiae ◽

Malaria Control ◽

Anopheles Arabiensis ◽

Field Conditions ◽

Anopheles Gambiae S.S ◽

Western Kenya

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Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania

10.21203/rs.3.rs-19762/v3 ◽

2020 ◽

Author(s):

Polius Gerazi Pinda ◽

Claudia Eichenberger ◽

Halfan S Ngowo ◽

Dickson S Msaky ◽

Said Abbasi ◽

...

Keyword(s):

Insecticide Resistance ◽

Malaria Transmission ◽

Anopheles Arabiensis ◽

Pyrethroid Resistance ◽

Anopheles Funestus ◽

Indoor Residual Spraying ◽

Sub Saharan Africa ◽

World Health ◽

Malaria Vectors ◽

South Eastern

Abstract BackgroundLong-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) have greatly reduced malaria transmission in sub-Saharan Africa, but are threatened by insecticide resistance. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus are now implicated in > 80% of malaria infections, even in villages where the species occurs at lower densities than the other vector, Anopheles arabiensis. This study compared the insecticide resistance phenotypes between the two malaria vectors in an area where pyrethroid-LLINs are widely used.MethodsThe study used the World Health Organization (WHO) assays with 1×, 5× and 10× insecticide doses to assess levels of resistance, followed by synergist bioassays to understand possible mechanisms of the observed resistance phenotypes. The tests involved adult mosquitoes collected from three villages across two districts in south-eastern Tanzania and included four insecticide classes.FindingsAt baseline doses (1×), both species were resistant to the two candidate pyrethroids (permethrin and deltamethrin), but susceptible to the organophosphate (pirimiphos-methyl). Anopheles funestus, but not An. arabiensis was also resistant to the carbamate (bendiocarb). Both species were resistant to DDT in all villages except in one village where An. arabiensis was susceptible. Anopheles funestus showed strong resistance to pyrethroids, surviving the 5× and 10× doses, while An. arabiensis reverted to susceptibility at the 5× dose. Pre-exposure to the synergist, piperonyl butoxide (PBO), enhanced the potency of the pyrethroids against both species and resulted in full susceptibility of An. arabiensis (>98% mortality). However, for An. funestus from two villages, permethrin-associated mortalities after pre-exposure to PBO only exceeded 90% but not 98%.ConclusionsIn south-eastern Tanzania, where An. funestus dominates malaria transmission, the species also has much stronger resistance to pyrethroids than its counterpart, An. arabiensis, and can survive more classes of insecticides. The pyrethroid resistance in both species appears to be mostly metabolic and may be partially addressed using synergists, e.g. PBO. These findings may explain the continued persistence and dominance of An. funestus despite widespread use of pyrethroid-treated LLINs, and inform new intervention choices for such settings. In short and medium-term, these may include PBO-based LLINs or improved IRS with compounds to which the vectors are still susceptible.

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Anopheles funestus mosquitoes from rural south-eastern Tanzania may have stronger resistance to pyrethroids than the other malaria vector, Anopheles arabiensis

10.21203/rs.3.rs-19762/v2 ◽

2020 ◽

Author(s):

Polius Gerazi Pinda ◽

Claudia Eichenberger ◽

Halfan S Ngowo ◽

Dickson S Msaky ◽

Said Abbasi ◽

...

Keyword(s):

Malaria Transmission ◽

Anopheles Arabiensis ◽

Pyrethroid Resistance ◽

Anopheles Funestus ◽

Indoor Residual Spraying ◽

The Other ◽

Sub Saharan Africa ◽

Malaria Vectors ◽

Insecticide Treated Nets ◽

South Eastern

Abstract Background: Long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) have greatly reduced malaria transmission in sub-Saharan Africa, but are threatened by insecticide resistance. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus are now implicated in > 80% of malaria infections, even in villages where the species occurs at lower densities than the other vector species, Anopheles arabiensis. This study compared the intensities of resistance between the two malaria vectors, so as to improve options for control. Methods: The study used WHO assays with 1×, 5× and 10× insecticide doses to assess levels of resistance, followed by synergist bioassays to understand possible mechanisms of the observed resistance phenotypes. The tests involved adult mosquitoes collected from villages across two districts in south-eastern Tanzania and identified using morphological and molecular approaches.Findings: At baseline doses (1×), both species were resistant to the two pyrethroids (permethrin and deltamethrin) but susceptible to the organophosphate (pirimiphos-methyl). An. funestus, but not An. arabiensis was also resistant to the carbamate (bendiocarb) at baseline doses. Both species were generally resistant to DDT, except An.arabiensis from one village. An. funestus showed strong resistance to pyrethroids, surviving the 5× and 10× doses except in one village. Pre-exposure to the synergist, piperonyl butoxide (PBO), enhanced the potency of pyrethroid in both An. arabiensis and An. funestus achieving mortalities >98%, except for An. funestus from two villages for which permethrin-associated mortalities exceeded 90% but not 98%. Conclusions: In these communities where An. funestus dominates malaria transmission, this study may suggest that the species also have much stronger resistance to pyrethroids than its counterpart, An. arabiensis and can survive more classes of insecticides, including carbamates. The pyrethroid resistance in both species appears to be mostly metabolic and may be temporarily addressed using synergists, e.g. PBO. These findings may explain the continued persistence and dominance of An. funestus despite widespread use of pyrethroid-treated LLINs, and inform new choices of interventions to tackle malaria transmission in such settings. These may include PBO-based LLINs or improved IRS with compounds to which the vectors are susceptible. Additional field validation of these indications will be necessary using age-synchronized mosquitoes.

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African Water Storage Pots for the Delivery of the Entomopathogenic Fungus Metarhizium anisopliae to the Malaria Vectors Anopheles gambiae s.s. and Anopheles funestus

American Journal of Tropical Medicine and Hygiene ◽

10.4269/ajtmh.2008.78.910 ◽

2008 ◽

Vol 78 (6) ◽

pp. 910-916 ◽

Cited By ~ 48

Author(s):

Marit Farenhorst ◽

Richard H. Hunt ◽

Bart G. J. Knols ◽

Willem Takken ◽

Ernst-Jan Scholte ◽

...

Keyword(s):

Anopheles Gambiae ◽

Metarhizium Anisopliae ◽

Entomopathogenic Fungus ◽

Water Storage ◽

Anopheles Funestus ◽

Malaria Vectors ◽

Anopheles Gambiae S.S

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Elevated Plasmodium infection and multiple insecticide resistance in the principal malaria vectors Anopheles funestus and Anopheles gambiae in a forested locality close to the airport of Yaoundé, the Capital city of Cameroon

10.21203/rs.2.23277/v1 ◽

2020 ◽

Author(s):

Nkemngo Francis Nongley ◽

Jean Leon Mugenzi Mbugulize ◽

Ebai Terence ◽

Abdoulaye Niang ◽

Murielle Wondji ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Infection Rate ◽

Transcriptional Profiling ◽

Anopheles Funestus ◽

Capital City ◽

Malaria Vectors ◽

Resistance Allele ◽

Test Procedures ◽

Anopheles Gambiae S.S

Abstract Background Reducing the burden of malaria requires better understanding of vector populations particularly in forested regions where the incidence remains elevated. Here, we characterized malaria vectors in a locality near the international airport of Yaoundé, the capital city of Cameroon, including species composition, abundance, Plasmodium infection rate; insecticide resistance profiles and underlying resistance mechanisms. Methods Blood-fed adult mosquitoes resting indoors were aspirated from houses in April 2019 at Elende, a village located 2km from the Yaoundé-Nsimalen airport. Female mosquitoes were forced to lay eggs to generate F 1 adult progeny. WHO bioassays were performed to assess resistance profile to insecticides. The threshold of insecticide susceptibility was fixed above 98% mortality rate and mortality rates below 90% were considered indicative of confirmed insecticide resistance according to the WHO test procedures for insecticide resistance monitoring. Furthermore, the molecular basis of resistance and Plasmodium infection rates were investigated.Results Anopheles funestus s.s. was most abundant species in Elende (85%) followed by Anopheles gambiae s.s. (15%) with both having a similar sporozoite infection rate. Both species exhibited high levels of resistance to pyrethroids (<40% mortality). An. gambiae s.s. was also resistant to DDT (9.9% mortality) and bendiocarb (54% mortality) while susceptible to organophosphate. An. funestus s.s. was resistant to dieldrin (1% mortality), DDT (86% mortality) but susceptible to carbamates and organophosphates. The DDT/pyrethroid L119F-GSTe2 resistance allele (8%) and G119S ace -1 resistance allele (15%) were detected in An. funestus s.s. and An. gambiae s.s. respectively. Furthermore, the high pyrethroid/DDT resistances in An. gambiae s.s. corresponded with an increase frequency of 1014F kdr allele (95%). The CYP6P9a P450 resistance allele was absent in the An. funestus s.s. population meanwhile transcriptional profiling of candidate cytochrome P450 genes reveals the over-expression of CYP6P5 , CYP6P9a and CYP6P9b. Conclusion The resistance to multiple insecticide classes observed in these vector populations alongside the high Plasmodium infection rate highlights the challenges that public health vector control programs encounter in sustaining the regular effectiveness of contemporary insecticide-based control interventions in forested areas. More particularly, the resistance observed against the carbamates and possible resistance against the organophosphates constitutes a major concern for IRS.

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Insecticide resistance status of Anopheles arabiensis in irrigated and non-irrigated areas in western Kenya

Parasites & Vectors ◽

10.1186/s13071-021-04833-z ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Pauline Winnie Orondo ◽

Steven G. Nyanjom ◽

Harrysone Atieli ◽

John Githure ◽

Benyl M. Ondeto ◽

...

Keyword(s):

Insecticide Resistance ◽

Vector Control ◽

Anopheles Arabiensis ◽

Crop Protection ◽

Indoor Residual Spraying ◽

Malaria Vectors ◽

Western Kenya ◽

Animal Protection ◽

Selection Of ◽

Selection Of Resistance

Abstract Background Malaria control in Kenya is based on case management and vector control using long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS). However, the development of insecticide resistance compromises the effectiveness of insecticide-based vector control programs. The use of pesticides for agricultural purposes has been implicated as one of the sources driving the selection of resistance. The current study was undertaken to assess the status and mechanism of insecticide resistance in malaria vectors in irrigated and non-irrigated areas with varying agrochemical use in western Kenya. Methods The study was carried out in 2018–2019 in Homa Bay County, western Kenya. The bioassay was performed on adults reared from larvae collected from irrigated and non-irrigated fields in order to assess the susceptibility of malaria vectors to different classes of insecticides following the standard WHO guidelines. Characterization of knockdown resistance (kdr) and acetylcholinesterase-inhibiting enzyme/angiotensin-converting enzyme (Ace-1) mutations within Anopheles gambiae s.l. species was performed using the polymerase chain reaction (PCR) method. To determine the agricultural and public health insecticide usage pattern, a questionnaire was administered to farmers, households, and veterinary officers in the study area. Results Anopheles arabiensis was the predominant species in the irrigated (100%, n = 154) area and the dominant species in the non-irrigated areas (97.5%, n = 162), the rest being An. gambiae sensu stricto. In 2018, Anopheles arabiensis in the irrigated region were susceptible to all insecticides tested, while in the non-irrigated region reduced mortality was observed (84%) against deltamethrin. In 2019, phenotypic mortality was decreased (97.8–84% to 83.3–78.2%). In contrast, high mortality from malathion (100%), DDT (98.98%), and piperonyl butoxide (PBO)-deltamethrin (100%) was observed. Molecular analysis of the vectors from the irrigated and non-irrigated areas revealed low levels of leucine-serine/phenylalanine substitution at position 1014 (L1014S/L1014F), with mutation frequencies of 1–16%, and low-frequency mutation in the Ace-1R gene (0.7%). In addition to very high coverage of LLINs impregnated with pyrethroids and IRS with organophosphate insecticides, pyrethroids were the predominant chemical class of pesticides used for crop and animal protection. Conclusion Anopheles arabiensis from irrigated areas showed increased phenotypic resistance, and the intensive use of pesticides for crop protection in this region may have contributed to the selection of resistance genes observed. The susceptibility of these malaria vectors to organophosphates and PBO synergists in pyrethroids offers a promising future for IRS and insecticide-treated net-based vector control interventions. These findings emphasize the need for integrated vector control strategies, with particular attention to agricultural practices to mitigate mosquito resistance to insecticides. Graphic abstract

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Phenotypic Insecticide Resistance in Anopheles gambiae (Diptera: Culicidae): Specific Characterization of Underlying Resistance Mechanisms Still Matters

Journal of Medical Entomology ◽

10.1093/jme/tjaa195 ◽

2020 ◽

Author(s):

Adandé A Medjigbodo ◽

Luc S Djogbenou ◽

Aubin A Koumba ◽

Laurette Djossou ◽

Athanase Badolo ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Resistance Mechanisms ◽

Malaria Vectors ◽

Effective Control ◽

Anopheles Coluzzii ◽

Anopheles Gambiae S.S ◽

Diagnostic Dose ◽

Pirimiphos Methyl ◽

Old Adult

Abstract An effective control of malaria vectors requires an extensive knowledge of mechanisms underlying the resistance-phenotypes developed by these vectors against insecticides. We investigated Anopheles gambiae mosquitoes from Benin and Togo for their intensity of insecticide resistance and we discussed the involvement of genotyped mechanisms in the resistance-phenotypes observed. Three- to five-day-old adult mosquitoes emerged from field and laboratory An. gambiae larvae were assayed using WHO tube intensity tests against various doses of deltamethrin: 1× (0.05%); 2× (0.1%); 5× (0.25%); 7.5× (0.375%) and those of pirimiphos-methyl: 0.5× (0.125%); 1× (0.25%). Members of An. gambiae complex were screened in field populations using polymerase chain reaction (PCR) assays. The presence of kdrR(1014F/1014S) and ace-1R(119S) mutations was also investigated using TaqMan and PCR-RFLP techniques, respectively. Anopheles gambiae from field were very resistant to deltamethrin, whereas KisKdr and AcerKdrKis strains displayed 100% mortality rates at 2× the diagnostic dose. In contrast, the field mosquitoes displayed a low resistance-intensity against 1× the diagnostic dose of pirimiphos-methyl, whereas AcerKis and AcerKdrKis strains showed susceptibility at 0.5× the diagnostic dose. Anopheles gambiae s.s., Anopheles coluzzii, and Anopheles arabiensis were identified. Allelic frequencies of kdrR (1014F) and ace-1R (119S) mutations in the field populations varied from 0.65 to 1 and 0 to 0.84, respectively. The field An. gambiae displayed high-resistance levels against deltamethrin and pirimiphos-methyl when compared with those of the laboratory An. gambiae-resistant strains. These results exhibit the complexity of underlying insecticide resistance mechanisms in these field malaria vectors.

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