Cited by 128Malaria Research and ControlInsect Resistance and GeneticsVector-borne infectious diseases

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Widespread Pyrethroid and DDT Resistance in the Major Malaria Vector Anopheles funestus in East Africa Is Driven by Metabolic Resistance Mechanisms

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Mulamba, Charles, Riveron, Jacob M., Ibrahim, Sulaiman S., Irving, Helen, Barnes, Kayla G., Mukwaya, Louis G., Birungi, Josephine, Wondji, Charles S.·2014·PLoS ONE

DOI 10.1371/journal.pone.0110058PMC PMC4198208

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Abstract

BACKGROUND: Establishing the extent, geographical distribution and mechanisms of insecticide resistance in malaria vectors is a prerequisite for resistance management. Here, we report a widespread distribution of insecticide resistance in the major malaria vector An. funestus across Uganda and western Kenya under the control of metabolic resistance mechanisms. METHODOLOGY/PRINCIPAL FINDINGS: Female An. funestus collected throughout Uganda and western Kenya exhibited a Plasmodium infection rate between 4.2 to 10.4%. Widespread resistance against both type I (permethrin) and II (deltamethrin) pyrethroids and DDT was observed across Uganda and western Kenya. All populations remain highly susceptible to carbamate, organophosphate and dieldrin insecticides. Knockdown resistance plays no role in the pyrethroid and DDT resistance as no kdr mutation associated with resistance was detected despite the presence of a F1021C replacement. Additionally, no signature of selection was observed on the sodium channel gene. Synergist assays and qRT-PCR indicated that metabolic resistance plays a major role notably through elevated expression of cytochrome P450s. DDT resistance mechanisms differ from West Africa as the L119F-GSTe2 mutation only explains a small proportion of the genetic variance to DDT resistance. CONCLUSION: The extensive distribution of pyrethroid and DDT resistance in East African An. funestus populations represents a challenge to the control of this vector. However, the observed carbamate and organophosphate susceptibility offers alternative solutions for resistance management.

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Figure 1 Map of Uganda showing study districts.CC BY · PubMed Central

Figure 2 Resistance profiles for pyrethroids in An. funestus populations Uganda and Kenya (Kisumu). (A) is for permethrin and (B) for deltamethrin.CC BY · PubMed Central

Figure 3 Resistance profiles for DDT (A) and other insecticides (B) in An. funestus populations Uganda and Kenya.CC BY · PubMed Central

Figure 4 Susceptibility profile after synergist assay with PBO.CC BY · PubMed Central

Figure 5 TCS network for the VGSC haplotypes between susceptible and resistant permethrin samples in Bulambuli (A) whereas (B) is for DDT samples in Jinja; Haplotypes are represented as an oval or a rectangle shape, scaled to reflect their frequencies. Lines connecting haplotypes and each node represent a single mutation event (respective polymorphic positions are given above branches). Blue shapes represent haplotypes unique in susceptible mosquitoes; Green shapes represent haplotypes commonly found in resistant mosquitoes and dead mosquitoes; Red shapes represent haplotypes unique to resistant mosquitoes.CC BY · PubMed Central

Figure 6 Investigation of metabolic resistance mechanisms. (A) Differential expression of candidate resistance genes by qRT-PCR between resistant mosquitoes (Lira, Tororo and Kisumu) and the susceptible FANG strain; Error bars represent standard deviation (n = 3). *** P<0.001; ** P<0.01; *P<0.05; ns not significant. (B) Correlation between the L119F alleles and DDT resistance phenotype. (C) Genotype distribution of L119F mutation between DDT resistant and susceptible mosquitoes.CC BY · PubMed Central

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Authors: Mulamba, C., Riveron, J. M., Ibrahim, S. S., Irving, H., Barnes, K. G., Mukwaya, L. G., Birungi, J., & Wondji, C. S.
Affiliations: Liverpool School of Tropical Medicine (GB)
Uganda Virus Research Institute (UG)
Corresponding author: Wondji, Charles S.
ORCID: Riveron, Jacob M.
Ibrahim, Sulaiman S.
Barnes, Kayla G.
Birungi, Josephine
Wondji, Charles S.
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2014-10-15
Volume: 9
Issue: 10
Pages: e110058
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0110058
PMC: PMC4198208
OpenAlex: W2110918782
Cited by: 128
References: 46
Citations by year: 2026: 9 · 2025: 8 · 2024: 13 · 2023: 10 · 2022: 8 · 2021: 9 · 2020: 15 · 2019: 5 · 2018: 11 · 2017: 18 · 2016: 17 · 2015: 5
FWCI: 13.27
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
LSTM Online Archive (Liverpool School of Tropical Medicine) (acceptedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Greater South Information System
Funders: Wellcome Trust (092794/Z/10/Z, 092794, 083515/Z/07/Z, 083515, 101893, 101893/Z/13/Z)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
Keywords: Anopheles funestus, insecticide resistance, pyrethroid resistance, DDT resistance, metabolic resistance, malaria vectors, cytochrome P450, knockdown resistance, kdr mutation, GSTe2, resistance management, East Africa
MeSH terms: Africa, Eastern, Animals, Anopheles, DDT, Female, Insect Vectors, Insecticide Resistance, Insecticides, Malaria, Molecular Sequence Data, Mutation, Pyrethrins, Sodium Channels

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Widespread Pyrethroid and DDT Resistance in the Major Malaria Vector Anopheles funestus in East Africa Is Driven by Metabolic Resistance Mechanisms

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