Contrasting Plasmodium infection rates and insecticide susceptibility profiles between the sympatric sibling species Anopheles parensis and Anopheles funestus s.s: a potential challenge for malaria vector control in Uganda

Mulamba, Charles; Irving, Helen; Riveron, Jacob M.; Mukwaya, L. G.; Birungi, Josephine; Wondji, Charles S.

doi:10.1186/1756-3305-7-71

Cited by 49 publications

(52 citation statements)

References 29 publications

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“…The finding of An. funestus populations being resistant to both pyrethroids and carbamates (bendiocarb and propoxur) in all the study areas is consistent with results reported from several other studies [17, 19, 24, 26–28] except for Uganda [25, 29] where this species was susceptible to carbamates (bendiocarb). Furthermore, the results from Malawi confirm a regional decline in the susceptibility of malaria vectors to pyrethroid and carbamate insecticides [14].…”

Section: Discussionsupporting

confidence: 91%

Increasing insecticide resistance in Anopheles funestus and Anopheles arabiensis in Malawi, 2011–2015

Mzilahowa

Chiumia

Mbewe

et al. 2016

Malar J

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BackgroundSusceptibility of principal Anopheles malaria vectors to common insecticides was monitored over a 5-year period across Malawi to inform and guide the national malaria control programme.MethodsAdult blood-fed Anopheles spp. and larvae were collected from multiple sites in sixteen districts across the country between 2011 and 2015. First generation (F1) progeny aged 2–5 days old were tested for susceptibility, using standard WHO procedures, against pyrethroids (permethrin and deltamethrin), carbamates (bendiocarb and propoxur), organophosphates (malathion and pirimiphos-methyl) and an organochlorine (DDT).ResultsMortality of Anopheles funestus to deltamethrin, permethrin, bendiocarb and propoxur declined significantly over the 5-year (2011–2015) monitoring period. There was wide variation in susceptibility to DDT but it was not associated with time. In contrast, An. funestus exhibited 100% mortality to the organophosphates (malathion and pirimiphos-methyl) at all sites tested. There was reduced mortality of Anopheles arabiensis to deltamethrin over time though this was not statistically significant. However, mortality of An. arabiensis exposed to permethrin declined significantly over time. Anopheles arabiensis exposed to DDT were more likely to be killed if there was high ITN coverage in the mosquito collection area the previous year. There were no other associations between mosquito mortality in a bioassay and ITN coverage or IRS implementation. Mortality of An. funestus from four sites exposed to deltamethrin alone ranged from 2 to 31% and from 41 to 94% when pre-exposed to the synergist piperonyl butoxide followed by deltamethrin. For permethrin alone, mortality ranged from 2 to 13% while mortality ranged from 63 to 100% when pre-exposed to PBO.ConclusionPyrethroid resistance was detected in An. funestus and An. arabiensis populations across Malawi and has worsened over the last 5 years. New insecticides and control strategies are urgently needed to reduce the burden of malaria in Malawi.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-016-1610-1) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 91%

Increasing insecticide resistance in Anopheles funestus and Anopheles arabiensis in Malawi, 2011–2015

Mzilahowa

Chiumia

Mbewe

et al. 2016

Malar J

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“…; Mulamba et al . ), (ii) the dramatic increase in the cyp‐l haplotype was coincident with the increase in ITN usage in 2006, and (iii) bioassay results confirm that kdr alone cannot account for the level of resistance observed for kdr:cyp‐l A. coluzzii genotype. That said, the nonsynonymous mutation in AGAP013173 and regulatory variation at Tailless or CPR125 should also be considered good candidates for selection.…”

Section: Discussionmentioning

confidence: 70%

“…Continued population sampling is needed to assess whether the cyp-l A. gambiae genotype detected in 2014 will be selected for in the population and warrant further study. We hypothesize that selection has acted upon cis-regulatory variation at CYP9K1 because (i) CYP9K1 has been shown to be upregulated in resistant anopheline mosquitoes (Tene et al 2013;Mulamba et al 2014), (ii) the dramatic increase in the cyp-l haplotype was coincident with the increase in ITN usage in 2006, and (iii) bioassay results confirm that kdr alone cannot account for the level of resistance observed for kdr:cyp-l A. coluzzii genotype. That said, the nonsynonymous mutation in AGAP013173 and regulatory variation at Tailless or CPR125 should also be considered good candidates for selection.…”

Section: Introgression Vs Selection On Standing Variationmentioning

confidence: 92%

“…But, most of the identified insecticide resistance genes in A. gambiae (119 in all) are P450 genes (64%; Srivastava et al 2010). Gene expression studies in anopheline mosquitoes have reported associations between over expression of several P450 genes and insecticide resistance, including CYP9K1 (Tene et al 2013;Mulamba et al 2014), CYP6P3 (M€ uller et al 2008, CYP6M2 (Stevenson et al 2011), CYP6Z1 (Nikou et al 2003, CYP325A3 (David et al 2005;Awolola et al 2009) and others (Djouaka et al 2008;McLaughlin et al 2008). The molecular basis of DDT resistance in Drosophila has been attributed to increased copy number and cis-regulatory variants at the P450 Cyp6g1 (Schmidt et al 2010).…”

Section: Introductionmentioning

confidence: 99%

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Complex genome evolution in Anopheles coluzzii associated with increased insecticide usage in Mali

Main

Collier

et al. 2015

Molecular Ecology

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In certain cases, a species may have access to important genetic variation present in a related species via adaptive introgression. These novel alleles may interact with their new genetic background, resulting in unexpected phenotypes. In this study, we describe a selective sweep on standing variation on the X chromosome in the mosquito Anopheles coluzzii, a principal malaria vector in West Africa. This event may have been influenced by the recent adaptive introgression of the insecticide resistance gene known as kdr from the sister species Anopheles gambiae. Individuals carrying both kdr and a nearly fixed X‐linked haplotype, encompassing at least four genes including the P450 gene CYP9K1 and the cuticular protein CPR125, have rapidly increased in relative frequency. In parallel, a reproductively isolated insecticide‐susceptible A. gambiae population (Bamako form) has been driven to local extinction, likely due to strong selection from increased insecticide‐treated bed net usage.

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“…However, this population was completely susceptible to bendiocarb (carbamate), malathion (organophosphate) and dieldrin. Recently, widespread resistance against pyrethroids and DDT was observed across Uganda [53,61]. Mutations which confer resistance to DDT and pyrethroids, West African (L1014F) and East African (L1014S) mutations, have been reported from the Ugandan An.…”

Section: Ugandamentioning

confidence: 99%

Insecticide Resistance in East Africa — History, Distribution and Drawbacks on Malaria Vectors and Disease Control

Yewhalaw¹,

Kweka²

2016

Insecticides Resistance

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Malaria is a major contributor to the global disease burden and a significant impediment to socio-economic development in resource-poor countries. In contrast to improved trends of malaria morbidity and mortality in some parts of the world, malaria has remained a life threatening disease in many other regions including East Africa because of factors such as weak health systems, growing drug and insecticide resistance, ecological change, climate anomalies, socio-economic factors and changes in land use patterns. Ongoing malaria vector control strategies rely mainly on the use of indoor residual spraying IRS and insecticide treated nets ITNs which are the primary intervention strategies to reduce malaria burden. The current success in reducing malaria related morbidity and mortality has led to the optimism that elimination of the disease as a public health problem may be a realistic objective. Efforts during the last decades enabled access to ITNs in sub-Saharan Africa protecting millions of people at risk of malaria. The number of countries that employed IRS as a vector control strategy increased almost by two fold and the percentage of households owing at least one ITN in sub-Saharan Africa is estimated to increase from time to time. Currently, all ITNs are treated with pyrethroids while IRS depends on pyrethroids, DDT and recently on carbamates. Despite IRS and ITNs are known in reducing malaria incidence, insecticide resistance in malaria vectors threatens the success of malaria control program. Resistance to insecticides has occurred in most arthropod vectors with different mechanisms. If the current trends of increased insecticide resistance continue, it may jeopardise the efficacy of current vector control tools. Given the limited choice of available insecticides, i.e., only insecticides belonging to classes of insecticides organochlorines, organophosphates, pyrethroids and carbamates , resistance to these insecticides has become a limiting factor for current efforts to sustain control. Currently, no other insecticide class with similar efficacy has been approved by WHOPES. The development of insecticide resistance in malaria vectors has been attributed to the prolonged use of insecticides for IRS and high coverage of ITNs/LLINs. The recent use of pyrethroids for indoor residual spraying is likely to have enhanced the selection pressure for insecticide resistance alleles among East African vector populations. Moreover, mosquitoes breeding in agricultural habitats are exposed to sub lethal doses of pesticides used in agriculture. Since currently recommended insecticides for IRS or ITNs were developed with similar active ingredients of pesticides used for agricultural pest control, their extensive and widespread use to boost agricultural productivity is believed to foster insecticide resistance in mosquito populations. There is strong evidence on the emergence of resistance to DDT and pyrethroids in the major malaria vectors in East Africa however, current information on resistance status of the malar...

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Contrasting Plasmodium infection rates and insecticide susceptibility profiles between the sympatric sibling species Anopheles parensis and Anopheles funestus s.s: a potential challenge for malaria vector control in Uganda

Cited by 49 publications

References 29 publications

Increasing insecticide resistance in Anopheles funestus and Anopheles arabiensis in Malawi, 2011–2015

Increasing insecticide resistance in Anopheles funestus and Anopheles arabiensis in Malawi, 2011–2015

Complex genome evolution in Anopheles coluzzii associated with increased insecticide usage in Mali

Insecticide Resistance in East Africa — History, Distribution and Drawbacks on Malaria Vectors and Disease Control

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