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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
Open accessAbstract
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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“Vector control relies on a handful of insecticides used for indoor residual spraying (IRS) and treatment of long-lasting insecticidal nets (LLINs) and insecticide resistance has been widely detected in malaria vectors across the continent [5–8].”
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Cites
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr121 · Cited by 40,207
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data
Librado, P., & Rozas, J. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp187 · Cited by 16,147
Weltgesundheitsorganisation (2005) · Cited by 3,799
Estimation of levels of gene flow from DNA sequence data.
Hudson, R. R., Slatkin, M., & Maddison, W. P. (1992) · Genetics · doi:10.1093/genetics/132.2.583 · Cited by 1,789
Snounou, G., Viriyakosol, S., Zhu, X. P., Jarra, W., Pinheiro, L., do Rosario, V. E., Thaithong, S., & Brown, K. N. (1993) · Molecular and Biochemical Parasitology · doi:10.1016/0166-6851(93)90077-b · Cited by 1,591
Ranson, H., N’Guessan, R., Lines, J., Moiroux, N., Nkuni, Z., & Corbel, V. (2011) · Trends in Parasitology · doi:10.1016/j.pt.2010.08.004 · Cited by 1,142
Martinez‐Torres, D., Chandre, F., Williamson, M. S., Darriet, F., Bergé, J. B., Devonshire, A. L., Guillet, P., Pasteur, N., & Pauron, D. (1998) · Insect Molecular Biology · doi:10.1046/j.1365-2583.1998.72062.x · Cited by 1,040
A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region).
Gillies, M. T., & Coetzee, M. (1987) · IHI Repository · Cited by 812
Ranson, H., Jensen, B., Vulule, J. M., Wang, X., Hemingway, J., & Collins, F. H. (2000) · Insect Molecular Biology · doi:10.1046/j.1365-2583.2000.00209.x · Cited by 645
Koekemoer, L. L., Kamau, L., Hunt, R. H., & Coetzee, M. (2002) · The American journal of tropical medicine and hygiene · doi:10.4269/ajtmh.2002.66.804 · Cited by 641
Andrews, K. G., Fergus, C. A., Aregawi, M. W., Cibulskis, R. E., & Zamani, G. (2014) · Cited by 552
Chan, M. (2010) · Cited by 513
Livak, K. J. (1984) · Genetics · doi:10.1093/genetics/107.4.611 · Cited by 411
Riveron, J. M., Yunta, C., Ibrahim, S. S., Djouaka, R., Irving, H., Menze, B. D., Ismail, H. M., Hemingway, J., Ranson, H., Albert, A., et al. (2014) · Genome biology · doi:10.1186/gb-2014-15-2-r27 · Cited by 368
Self-citationStatus of pyrethroid resistance in Anopheles gambiae sensu lato.
Chandre, F., Darrier, F., Manga, L., Akogbeto, M. C., Faye, O., Mouchet, J., & Guillet, P. (1999) · Europe PMC (PubMed Central) · Cited by 322
VARIATION IN MALARIA TRANSMISSION INTENSITY IN SEVEN SITES THROUGHOUT UGANDA
Okello, P. E., Bortel, W. V., Byaruhanga, A. M., CORREWYN, A., Roelants, P., Talisuna, A. O., D’ALESSANDRO, U., & Coosemans, M. (2006) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2006.75.219 · Cited by 287
Ranson, H., Abdallah, H., Badolo, A., Guelbeogo, M. W., Kerah-Hinzoumbé, C., Yangalbé-Kalnoné, E., Sagnon, N., Simard, F., & Coetzee, M. (2009) · Malaria Journal · doi:10.1186/1475-2875-8-299 · Cited by 283
Identification of Hot Spots of Malaria Transmission for Targeted Malaria Control
Bousema, T., Drakeley, C., Gesase, S., Hashim, R., Magesa, S., Mosha, F., Otieno, S., Carneiro, I., Cox, J., Msuya, E., et al. (2010) · The Journal of Infectious Diseases · doi:10.1086/652456 · Cited by 279
Pyrethroid Resistance in Aedes aegypti from Grand Cayman
Harris, A. F., Rajatileka, S., & Ranson, H. (2010) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2010.09-0623 · Cited by 277
Riveron, J. M., Irving, H., Ndula, M., Barnes, K. G., Ibrahim, S. S., Paine, M. J. I., & Wondji, C. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216705110 · Cited by 242
Self-citationMitchell, S. N., Stevenson, B. J., Müller, P., Wilding, C. S., Egyir-Yawson, A., Field, S. G., Hemingway, J., Paine, M. J. I., Ranson, H., & Donnelly, M. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203452109 · Cited by 239
Brooke, B. D., Kloke, G., Hunt, R. H., Koekemoer, L. L., Tem, E. A., Taylor, M. E., Small, G., Hemingway, J., & Coetzee, M. (2001) · Bulletin of Entomological Research · doi:10.1079/ber2001108 · Cited by 216
Pyrethroid Resistance in an Anopheles funestus Population from Uganda
Morgan, J. C., Irving, H., Okedi, L. M., Steven, A., & Wondji, C. S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011872 · Cited by 214
Self-citationCoetzee, M., & Koekemoer, L. L. (2013) · Annual Review of Entomology · doi:10.1146/annurev-ento-120811-153628 · Cited by 180
Bass, C., Nikou, D., Blagborough, A. M., Vontas, J., Sinden, R. E., Williamson, M. S., & Field, L. M. (2008) · Malaria Journal · doi:10.1186/1475-2875-7-177 · Cited by 177
Wondji, C. S., Dabiré, R. K., Tukur, Z., Irving, H., Djouaka, R., & Morgan, J. C. (2011) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2011.03.012 · Cited by 163
Self-citationImpact of pyrethroid resistance on operational malaria control in Malawi
Wondji, C. S., Coleman, M. M., Kleinschmidt, I., Mzilahowa, T., Irving, H., Ndula, M., Rehman, A. M., Morgan, J. C., Barnes, K. G., & Hemingway, J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217229109 · Cited by 149
Self-citationDavies, T. G. E., Field, L. M., Usherwood, P. N. R., & Williamson, M. S. (2007) · Insect Molecular Biology · doi:10.1111/j.1365-2583.2007.00733.x · Cited by 145
Cuamba, N., Morgan, J. C., Irving, H., Steven, A., & Wondji, C. S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011010 · Cited by 142
Self-citationInsecticide Resistance and the Future of Malaria Control in Zambia
Chanda, E., Hemingway, J., Kleinschmidt, I., Rehman, A. M., Ramdeen, V., Phiri, F. N., Coetzer, S., Mthembu, D. J., Shinondo, C. J., Chizema-Kawesha, E., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024336 · Cited by 132
Advances in the study of Anopheles funestus, a major vector of malaria in Africa
Coetzee, M., & Fontenille, D. (2004) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2004.03.012 · Cited by 127
Kwiatkowska, R. M., Platt, N., Poupardin, R., Irving, H., Dabiré, R. K., Mitchell, S. N., Jones, C. M., Diabaté, A., Ranson, H., & Wondji, C. S. (2013) · Gene · doi:10.1016/j.gene.2013.01.036 · Cited by 122
Self-citationKawada, H., Dida, G. O., Ohashi, K., Komagata, O., Kasai, S., Tomita, T., Sonye, G. O., Maekawa, Y., Mwatele, C., Njenga, S. M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022574 · Cited by 114
Ramphul, U. N., Boase, T., Bass, C., Okedi, L. M., Donnelly, M. J., & Müller, P. (2009) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2009.02.014 · Cited by 107
Kigozi, R. N., Baxi, S. M., Gasasira, A. F., Sserwanga, A., Kakeeto, S., Nasr, S., Rubahika, D., Dissanayake, G., Kamya, M. R., Filler, S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042857 · Cited by 94
Djouaka, R., Irving, H., Tukur, Z., & Wondji, C. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027760 · Cited by 85
Self-citationRangewide population genetic structure of the African malaria vector Anopheles funestus
Michel, A. P., Ingrasci, M. J., Schemerhorn, B. J., Kern, M. K., Goff, G. L., Coetzee, M., Élissa, N., Fontenille, D., VULULE, J. M., Lehmann, T., et al. (2005) · Molecular Ecology · doi:10.1111/j.1365-294x.2005.02754.x · Cited by 80
Okoye, P. N., Brooke, B. D., Koekemoer, L. L., Hunt, R. H., & Coetzee, M. (2008) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2008.02.022 · Cited by 77
Okia, M., Ndyomugyenyi, R., Kirunda, J., Byaruhanga, A. M., Adibaku, S., Lwamafa, D. K., & Kironde, F. (2013) · Parasites & Vectors · doi:10.1186/1756-3305-6-130 · Cited by 64
Pyrethroid resistance in southern African Anopheles funestus extends to Likoma Island in Lake Malawi
Hunt, R., Edwardes, M., & Coetzee, M. (2010) · Parasites & Vectors · doi:10.1186/1756-3305-3-122 · Cited by 60
Advances and Perspectives in the Study of the Malaria Mosquito Anopheles funestus
Dia, I., Guelbeogo, M. W., & Ayala, D. (2013) · InTech eBooks · doi:10.5772/55389 · Cited by 58
Wondji, C. S., de Silva, W. A. P. P., Hemingway, J., Ranson, H., & Karunaratne, S. H. P. P. (2008) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2008.02033.x · Cited by 53
Self-citationMulamba, C., Irving, H., Riveron, J. M., Mukwaya, L. G., Birungi, J., & Wondji, C. S. (2014) · Parasites & Vectors · doi:10.1186/1756-3305-7-71 · Cited by 45
Self-citationHeterogeneity of Anopheles Mosquitoes in Nyabushozi County, Kiruhura district, Uganda
Echodu, R., Okello-Onen, J., Lutwama, J. J., Enyaru, J., Ocan, R., Asaba, R. B., Ajuga, F., Rubaire-Akiiki, C., Bradley, D. J., Mutero, C. M., et al. (2010) · Journal of Stored Products and Postharvest Research · doi:10.5897/jpvb.9000010 · Cited by 12
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Ranson, H., & Lissenden, N. (2016) · Trends in Parasitology · doi:10.1016/j.pt.2015.11.010 · Cited by 989
Churcher, T. S., Lissenden, N., Griffin, J. T., Worrall, E., & Ranson, H. (2016) · eLife · doi:10.7554/elife.16090 · Cited by 312
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Zhu, F., Lavine, L. C., O'Neal, S. D., Lavine, M., Foss, C. R., & Walsh, D. B. (2016) · Insects · doi:10.3390/insects7010002 · Cited by 230
Mnzava, A. P., Knox, T. B., Temu, E. A., Trett, A., Fornadel, C. M., Hemingway, J., & Renshaw, M. (2015) · Malaria Journal · doi:10.1186/s12936-015-0693-4 · Cited by 215
Kaindoa, E. W., Matowo, N. S., Ngowo, H. S., Mkandawile, G., Mmbando, A. S., Finda, M., & Okumu, F. O. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177807 · Cited by 176
Metadata
- 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.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2014-10-15
- Volume
- 9
- Issue
- 10
- Pages
- e110058
- ISSN
- 1932-6203 (ISSN-L)
- 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
- 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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