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

2020 ◽  
Vol 19 (1) ◽  
Author(s):  
Polius G. Pinda ◽  
Claudia Eichenberger ◽  
Halfan S. Ngowo ◽  
Dickson S. Msaky ◽  
Said Abbasi ◽  
...  

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.

2020 ◽  
Author(s):  
Polius Gerazi Pinda ◽  
Claudia Eichenberger ◽  
Halfan S Ngowo ◽  
Dickson S Msaky ◽  
Said Abbasi ◽  
...  

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.


2020 ◽  
Author(s):  
Polius Gerazi Pinda ◽  
Claudia Eichenberger ◽  
Halfan S Ngowo ◽  
Dickson S Msaky ◽  
Said Abbasi ◽  
...  

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.


Author(s):  
Polius Gerazi Pinda ◽  
Claudia Eichenberger ◽  
Halfan S Ngowo ◽  
Dickson S Msaky ◽  
Said Abbasi ◽  
...  

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 dominant malaria vectors. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus now transmit more than 80% of malaria infections even in villages where the species occurs at far lower densities than other vectors such as Anopheles arabiensis.Methods: To better understand the dominance of An. funestus in these settings and improve options for its control, this study compared intensities of resistance between females of this species and those of An. arabiensis , using WHO assays with 1×, 5× and 10× insecticide doses. Additional tests were done to assess the reversibility of such resistance using synergists. The mosquitoes were collected from villages across two districts in south-eastern Tanzania.Findings: Both species were resistant to the two pyrethroids (permethrin and deltamethrin) and the organochloride (DDT) but susceptible to the organophosphate (pirimiphos-methyl) at standard baseline doses (1×). However, An. funestus as opposed to An. arabiensis was also resistant to the carbamate (bendiocarb) at standard doses (1×). An. funestus showed strong resistance to pyrethroids, surviving the 5× doses and 10× doses except in one village. Pre-exposure to the synergist, piperonyl butoxide (PBO), reversed the pyrethroid-resistance 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 now dominates malaria transmission, the species also displays much stronger resistance to pyrethroids than its counterpart, An. arabiensis, and can readily survive more classes of insecticides, including carbamates. The resistance to pyrethroids in both mosquito species appears to be mostly metabolic and can be reversed significantly using synergists such as PBO. These findings may explain the continued persistence and dominance of An. funestus despite widespread use of pyrethroid-treated LLINs, and will also inform future choices of interventions to tackle malaria transmission in this area and other similar settings. Such interventions may include PBO-based LLINs or improved IRS with compounds such as organophosphates against which the vectors are still susceptible.


2017 ◽  
Vol 114 (52) ◽  
pp. E11267-E11275 ◽  
Author(s):  
Hmooda Toto Kafy ◽  
Bashir Adam Ismail ◽  
Abraham Peter Mnzava ◽  
Jonathan Lines ◽  
Mogahid Shiekh Eldin Abdin ◽  
...  

Insecticide-based interventions have contributed to ∼78% of the reduction in the malaria burden in sub-Saharan Africa since 2000. Insecticide resistance in malaria vectors could presage a catastrophic rebound in disease incidence and mortality. A major impediment to the implementation of insecticide resistance management strategies is that evidence of the impact of resistance on malaria disease burden is limited. A cluster randomized trial was conducted in Sudan with pyrethroid-resistant and carbamate-susceptible malaria vectors. Clusters were randomly allocated to receive either long-lasting insecticidal nets (LLINs) alone or LLINs in combination with indoor residual spraying (IRS) with a pyrethroid (deltamethrin) insecticide in the first year and a carbamate (bendiocarb) insecticide in the two subsequent years. Malaria incidence was monitored for 3 y through active case detection in cohorts of children aged 1 to <10 y. When deltamethrin was used for IRS, incidence rates in the LLIN + IRS arm and the LLIN-only arm were similar, with the IRS providing no additional protection [incidence rate ratio (IRR) = 1.0 (95% confidence interval [CI]: 0.36–3.0; P = 0.96)]. When bendiocarb was used for IRS, there was some evidence of additional protection [interaction IRR = 0.55 (95% CI: 0.40–0.76; P < 0.001)]. In conclusion, pyrethroid resistance may have had an impact on pyrethroid-based IRS. The study was not designed to assess whether resistance had an impact on LLINs. These data alone should not be used as the basis for any policy change in vector control interventions.


2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Dominique Mieguim Ngninpogni ◽  
Cyrille Ndo ◽  
Patrick Ntonga Akono ◽  
Anicet Nguemo ◽  
Amine Nguepi ◽  
...  

Abstract Background In Mvoua, a village situated in a forested area of Cameroon, recent studies have reported high prevalence of Plasmodium falciparum infection among the population. In order to understand factors that can sustain such a high malaria transmission, we investigated the biology of Anopheles vectors and its susceptibility to insecticides, as well as long-lasting insecticidal net (LLIN) coverage, use and bio-efficacy. Methods A longitudinal entomological survey was conducted from July 2018 to April 2019. Adult mosquitoes were collected using the human landing catch (HLC) method and identified using morphological and molecular techniques. Anopheles gambiae (s.l.) larvae were sampled from several stagnant water pools throughout the village and reared to generate F1 adults. The presence of P. falciparum circumsporozoite antigen was detected in the heads and thoraces of mosquitoes collected as adults using an enzyme-linked immunosorbent assay. The insecticide susceptibility status of the local An. gambiae (s.l.) F1 population to the pyrethroid insecticides deltamethrin 0.5% and permethrin 0.75% was determined using World Health Organization-tube bioassays, while the frequency of the knockdown resistance (kdr) mutation was determined by PCR. Coverage, use and physical integrity of LLINs were assessed in households, then cone assays were used to test for their bio-efficacy on both the reference insecticide-susceptible Kisumu strain and on field F1 An. gambiae (s.l.) Results In total, 110 Anopheles mosquitoes were collected, of which 59.1% were identified as Anopheles funestus (s.l.), 38.18% as An. gambiae (s.l.) and 2.72% as An. ziemanii. Anopheles funestus was the most abundant species except in the long rainy season, when An. gambiae (s.l.) predominated (65.8%). In the dry seasons, vectors were principally endophagous (76% of those collected indoors) while they tended to be exophagous (66% of those collected outdoors) in rainy seasons. High Plasmodium infection was observed in An. gambiae (s.l.) and An. funestus, with a circumsporozoitic rate of 14.29 and 10.77%, respectively. Anopheles gambiae (s.l.) was highly resistant to pyrethroid insecticides (mortality rates: 32% for permethrin and 5% for deltamethrin) and harbored the kdr-L1014F mutation at a high frequency (89.74%). Of the 80 households surveyed, only 47.69% had achieved universal coverage with LLNs. Around 70% of the LLINs sampled were in poor physical condition, with a proportionate hole index > 300. Of the ten LLNs tested, eight were effective against the An. gambiae reference insecticide-susceptible Kisumu strain, showing mortality rate of > 80%, while none of these LLINs were efficient against local An. gamabie (s.l.) populations (mortality rates < 11.5%). Conclusion A combination of elevated P. falciparum infection in Anopheles vector populations, insufficient coverage and loss of effectiveness of LLINs due to physical degradation, as well as high resistance to pyrethroid insecticides is responsible for the persistence of high malaria transmission in forested rural area of Mvoua, Cameroon.


2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Pauline Winnie Orondo ◽  
Steven G. Nyanjom ◽  
Harrysone Atieli ◽  
John Githure ◽  
Benyl M. Ondeto ◽  
...  

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


2021 ◽  
Author(s):  
Johnson Matowo ◽  
David Weetman ◽  
Patricia Pignatell ◽  
Alexandra Wright ◽  
Jacques Charlwood ◽  
...  

Long lasting insecticidal nets (LLINs) are a proven tool to reduce malaria transmission, but in Africa efficacy is being reduced by pyrethroid resistance in the major vectors. A cluster randomized trial in Muleba district, Tanzania demonstrated that permethrin LLINs co-treated with piperonyl butoxide (PBO), a synergist that can block pyrethroid-metabolizing enzymes in the mosquito, had much greater efficacy than pyrethroid-only nets. Insecticide resistance profiles and underlying mechanisms were investigated in Anopheles gambiae and An. funestus from Muleba during the trial. Diagnostic dose bioassays using permethrin, together with intensity assays, suggest pyrethroid resistance that is both strong and very common, but not extreme. Transcriptomic analysis found multiple P450 genes over expressed including CYP6M2, CYP6Z3, CYP6P3, CYP6P4, CYP6AA1 and CYP9K1 in An. gambiae and CYP6N1, CYP6M7, CYP6M1 and CYP6Z3 in An. funestus. Indeed, very similar suites of P450 enzymes commonly associated with resistant populations elsewhere in Africa were detected as over expressed suggesting a convergence of mechanisms across Sub-Saharan African malaria vectors. The findings give insight into factors that may correlate with pyrethroid PBO LLIN success, broadly supporting model predictions, but revision to guidelines previously issued by the World Health Organization is warranted.


2020 ◽  
Vol 2020 ◽  
pp. 1-5
Author(s):  
Zalalham Al-Koleeby ◽  
Ahmed El Aboudi ◽  
Mithaq Assada ◽  
Mohamed Al-Hadi ◽  
Mohammed Abdalr Ahman ◽  
...  

Control of malaria vectors in Yemen relies on both indoor residual spraying using carbamate (bendiocarb) and long-lasting pyrethroids-treated nets. This paper reports the results of studies conducted to monitor the insecticide resistance of the main malaria vector, Anopheles arabiensis, to the insecticides currently used in the vector control in four different locations. Susceptibility tests were performed following the WHO test procedures. Two pyrethroids (lambda-cyhalothrin 0.05% and deltamethrin 0.05%) and one carbamate (bendiocarb 0.1%) were tested at diagnostic doses (DD). The five-fold DD of lambda-cyhalothrin and deltamethrin (0.25%) were also used to yield information on the intensity of resistance. Besides, tests with synergists were performed to assess the involvement of detoxifying enzyme in the phenotypic resistance of the populations of An. arabiensis to pyrethroids. The results of the performed susceptibility bioassay showed that the vector is susceptible to bendiocarb and resistant to lambda-cyhalothrin and deltamethrin in the four studied areas. The pyrethroids resistance is solely metabolic. This information could help policy-makers to plan insecticide resistance management. Bendiocarb is still an effective insecticide in the form of IRS. Concerning LLINS, it would be interesting to assess their effectiveness, combining a pyrethroid with PBO for the control of the pyrethroid-resistant malaria vector.


Author(s):  
M. Y. Korti ◽  
T. B. Ageep ◽  
A. I. Adam ◽  
K. B. Shitta ◽  
A. A. Hassan ◽  
...  

Abstract Background Chemical control has been the most efficient method in mosquito control, the development of insecticide resistance in target populations has a significant impact on vector control. The use of agricultural pesticides may have a profound impact on the development of resistance in the field populations of malaria vectors. Our study focused on insecticide resistance and knockdown resistance (kdr) of Anopheles arabiensis populations from Northern Sudan, related to agricultural pesticide usage. Results Anopheles arabiensis from urban and rural localities (Merowe and Al-hamadab) were fully susceptible to bendiocarb 0.1% and permethrin 0.75% insecticides while resistant to DDT 4% and malathion 5%. The population of laboratory reference colony F189 from Dongola showed a mortality of 91% to DDT (4%) and fully susceptible to others. GLM analysis indicated that insecticides, sites, site type, and their interaction were determinant factors on mortality rates (P < 0.01). Except for malathion, mortality rates of all insecticides were not significant (P > 0.05) according to sites. Mortality rates of malathion and DDT were varied significantly (P < 0.0001 and P < 0.05 respectively) by site types, while mortality rates of bendiocarb and permethrin were not significant (P >0.05). The West African kdr mutation (L1014F) was found in urban and rural sites. Even though, the low-moderate frequency of kdr (L1014F) mutation was observed. The findings presented here for An. arabiensis showed no correlation between the resistant phenotype as ascertained by bioassay and the presence of the kdr mutation, with all individuals tested except the Merowe site which showed a moderate association with DDT (OR= 6 in allelic test), suggesting that kdr genotype would be a poor indicator of phenotypic resistance. Conclusion The results provide critical pieces of information regarding the insecticide susceptibility status of An. arabiensis in northern Sudan. The usage of the same pesticides in agricultural areas seemed to affect the Anopheles susceptibility when they are exposed to those insecticides in the field. The kdr mutation might have a less role than normally expected in pyrethroids resistance; however, other resistance genes should be in focus. These pieces of information will help to improve the surveillance system and The implication of different vector control programs employing any of these insecticides either in the treatment of bed nets or for indoor residual spraying would achieve satisfactory success rates.


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