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Cited by 63Malaria Research and ControlInsect Resistance and GeneticsDengue and Mosquito Control Research

Underpinning Sustainable Vector Control through Informed Insecticide Resistance Management

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Thomsen, Edward K., Strode, Clare, Hemmings, Kay, Hughes, Angela J., Chanda, Emmanuel, Musapa, Mulenga, Kamuliwo, Mulakwa, Phiri, Faustina N. +9 more·2014·PLoS ONE
DOI 10.1371/journal.pone.0099822PMC PMC4059741
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Abstract

BACKGROUND: There has been rapid scale-up of malaria vector control in the last ten years. Both of the primary control strategies, long-lasting pyrethroid treated nets and indoor residual spraying, rely on the use of a limited number of insecticides. Insecticide resistance, as measured by bioassay, has rapidly increased in prevalence and has come to the forefront as an issue that needs to be addressed to maintain the sustainability of malaria control and the drive to elimination. Zambia's programme reported high levels of resistance to the insecticides it used in 2010, and, as a result, increased its investment in resistance monitoring to support informed resistance management decisions. METHODOLOGY/PRINCIPAL FINDINGS: A country-wide survey on insecticide resistance in Zambian malaria vectors was performed using WHO bioassays to detect resistant phenotypes. Molecular techniques were used to detect target-site mutations and microarray to detect metabolic resistance mechanisms. Anopheles gambiae s.s. was resistant to pyrethroids, DDT and carbamates, with potential organophosphate resistance in one population. The resistant phenotypes were conferred by both target-site and metabolic mechanisms. Anopheles funestus s.s. was largely resistant to pyrethroids and carbamates, with potential resistance to DDT in two locations. The resistant phenotypes were conferred by elevated levels of cytochrome p450s. CONCLUSIONS/SIGNIFICANCE: Currently, the Zambia National Malaria Control Centre is using these results to inform their vector control strategy. The methods employed here can serve as a template to all malaria-endemic countries striving to create a sustainable insecticide resistance management plan.

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  • Updated insecticide resistance data will help to choose relevant areas to implement randomized controlled trials.

    “Updated insecticide resistance data will also help to choose relevant areas to implement such randomized controlled trials [50, 51].”

    From Mapping insecticide resistance in Anopheles gambiae (s.l.) from Côte d'Ivoire (2018) · cites this paper as [50]

    The Discussion (page unavailable) says updated resistance data informed which Zambian provinces received particular insecticides for indoor residual spraying. It does not say the data would help select areas for randomized controlled trials; that specific use is unsupported. (LLM, conf=0.79)

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  1. [1]Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, et al (2012) Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413– 431 10.1016/S0140-6736(12)60034-8 22305225 · DOI · Paper page
  2. [2]Feachem RGA, Phillips AA, Hwang J, Cotter C, Wielgosz B, et al (2010) Shrinking the malaria map: progress and prospects. Lancet 376: 1566– 1578 10.1016/S0140-6736(10)61270-6 21035842 PMC3044848 · DOI · Paper page
  3. [4]Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, et al (2000) Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14: 181– 189. 10872862
  4. [5]Maharaj R, Mthembu DJ, Sharp BL (2005) Impact of DDT re-introduction on malaria transmission in KwaZulu-Natal. South African Med J 95: 871– 874. 16344885
  5. [6]Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, et al (2011) Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 11: 925– 932 10.1016/S1473-3099(11)70194-3 21856232 · DOI
  6. [8]Ranson H, N'guessan R, Lines J, Moiroux N, Nkuni Z, et al (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91– 98 10.1016/j.pt.2010.08.004 20843745 · DOI · Paper page
  7. [9]Kelly-Hope L, Ranson H, Hemingway J (2008) Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis 8: 387– 389 10.1016/S1473-3099(08)70045-8 18374633 · DOI · Paper page
  8. [10]Chizema-Kawesha E, Miller JM, Steketee RW, Mukonka VM, Mukuka C, et al (2010) Scaling up malaria control in Zambia: progress and impact 2005–2008. Am J Trop Med Hyg 83: 480– 488 10.4269/ajtmh.2010.10-0035 20810807 PMC2929038 · DOI
  9. [11]Chanda E, Coleman M, Kleinschmidt I, Hemingway J, Hamainza B, et al (2012) Impact assessment of malaria vector control using routine surveillance data in Zambia: implications for monitoring and evaluation. Malar J 11: 437 10.1186/1475-2875-11-437 23273109 PMC3543298 · DOI
  10. [15]Masaninga F, Chanda E, Chanda-Kapata P, Hamainza B, Masendu HT, et al (2013) Review of the malaria epidemiology and trends in Zambia. Asian Pac J Trop Biomed 3: 89– 94 10.1016/S2221-1691(13)60030-1 23593585 PMC3627166 · DOI
  11. [16]Chanda E, Hemingway J, Kleinschmidt I, Rehman AM, Ramdeen V, et al (2011) Insecticide resistance and the future of malaria control in Zambia. PLoS One 6: e24336 10.1371/journal.pone.0024336 21915314 PMC3167838 · DOI
  12. [17]Chanda E, Mukonka VM, Kamuliwo M, Macdonald MB, Haque U (2013) Operational scale entomological intervention for malaria control: strategies, achievements and challenges in Zambia. Malar J 12: 10 10.1186/1475-2875-12-10 23298401 PMC3585912 · DOI
  13. [19]Sharp B, van Wyk P, Sikasote JB, Banda P, Kleinschmidt I (2002) Malaria control by residual insecticide spraying in Chingola and Chililabombwe, Copperbelt Province, Zambia. Trop Med Int Health 7: 732– 736. 12225502
  14. [23]Scott JA, Brogdon WG, Collins FH (1993) Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520– 529. 8214283
  15. [24]Koekemoer LL, Lochouarn L, Hunt RH, Coetzee M (1999) Single-strand conformation polymorphism analysis for identification of four members of the Anopheles funestus (Diptera: Culicidae) group. J Med Entomol 36: 125– 130. 10083746
  16. [25]Favia G, Torre A, Bagayoko M, Lanfrancotti A, Sagnon NF, et al (1997) Molecular identification of sympatric chromosomal forms of Anopheles gambiae and further evidence of their reproductive isolation. 6: 377– 383. 9359579
  17. [27]Eisen L, Coleman M, Lozano-Fuentes S, McEachen N, Orlans M, et al (2011) Multi-disease data management system platform for vector-borne diseases. PLoS Negl Trop Dis 5: e1016 10.1371/journal.pntd.0001016 21468310 PMC3066141 · DOI
  18. [30]Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, et al (2007) Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malar J 6: 111 10.1186/1475-2875-6-111 17697325 PMC1971715 · DOI · Paper page
  19. [31]Bass C, Nikou D, Vontas J, Williamson MS, Field LM (2010) Development of high-throughput real-time PCR assays for the identification of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae. Pestic Biochem Physiol 96: 80– 85 10.1016/j.pestbp.2009.09.004 · DOI
  20. [32]Mitchell SN, Stevenson BJ, Müller P, Wilding CS, Egyir-Yawson A, et al (2012) Identification and validation of a gene causing cross-resistance between insecticide classes in Anopheles gambiae from Ghana. Proc Natl Acad Sci U S A 109: 6147– 6152 10.1073/pnas.1203452109 22460795 PMC3341073 · DOI
  21. [33]Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. 11328886 PMC55695
  22. [34]Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, et al (2008) PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J 7: 177 10.1186/1475-2875-7-177 18793416 PMC2553798 · DOI · Paper page
  23. [35]Zaim M, Guillet P (2002) Alternative insecticides: an urgent need. Trends Parasitol 18: 2001– 2003. 11998703
  24. [36]Coleman M, Sharp B, Seocharan I, Hemingway J (2006) Developing an evidence-based decision support system for rational insecticide choice in the control of African malaria vectors. J Med Entomol 43: 663– 668. 16892622
  25. [37]Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, et al (2009) Insecticide resistance and its association with target-site mutations in natural populations of Anopheles gambiae from eastern Uganda. Trans R Soc Trop Med Hyg 103: 1121– 1126 doi 10.1016/j.trstmh.2009.02.014. 19303125 · DOI
  26. [39]Abilio AP, Kleinschmidt I, Rehman AM, Cuamba N, Ramdeen V, et al (2011) The emergence of insecticide resistance in central Mozambique and potential threat to the successful indoor residual spraying malaria control programme. Malar J 10: 110 10.1186/1475-2875-10-110 21535872 PMC3096596 · DOI
  27. [40]Casimiro S, Coleman M (2006) Insecticide resistance in Anopheles arabiensis and Anopheles gambiae from Mozambique. J Med … 43: 276– 282. 16619611
  28. [41]Djogbénou L, Pasteur N, Akogbéto M, Weill M, Chandre F (2011) Insecticide resistance in the Anopheles gambiae complex in Benin: a nationwide survey. Med Vet Entomol 25: 256– 267 10.1111/j.1365-2915.2010.00925.x 21155858 · DOI · Paper page
  29. [42]N'Guessan R, Darriet F, Guillet P, Carnevale P, Traore-Lamizana M, et al (2003) Resistance to carbosulfan in Anopheles gambiae from Ivory Coast, based on reduced sensitivity of acetylcholinesterase. Med Vet Entomol 17: 19– 25. 12680920
  30. [43]Oduola AO, Idowu ET, Oyebola MK, Adeogun AO, Olojede JB, et al (2012) Evidence of carbamate resistance in urban populations of Anopheles gambiae s.s. mosquitoes resistant to DDT and deltamethrin insecticides in Lagos, South-Western Nigeria. Parasit Vectors 5: 116 10.1186/1756-3305-5-116 22686575 PMC3409038 · DOI
  31. [44]Aïkpon R, Agossa F, Ossè R, Oussou O, Aïzoun N, et al (2013) Bendiocarb resistance in Anopheles gambiae s.l. populations from Atacora department in Benin, West Africa: a threat for malaria vector control. Parasit Vectors 6: 192 10.1186/1756-3305-6-192 23803527 PMC3698110 · DOI
  32. [45]Casimiro S, Coleman M, Mohloai P, Hemingway J, Sharp B (2006) Insecticide resistance in Anopheles funestus (Diptera: Culicidae) from Mozambique. J Med Entomol 43: 267– 275. 16619610
  33. [46]Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, et al (2012) Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A 109: 19063– 19070 10.1073/pnas.1217229109 23118337 PMC3511128 · DOI
  34. [47]Fornadel CM, Norris DE (2008) Increased Endophily by the Malaria Vector Anopheles arabiensis in Southern Zambia and Identification of Digested Blood Meals. 79: 876– 880. PMC4147109 19052296
  35. [48]Hemingway J, Vontas J, Poupardin R, Raman J, Lines J, et al (2013) Country-level operational implementation of the Global Plan for Insecticide Resistance Management. Proc Natl Acad Sci U S A 110: 9397– 9402 10.1073/pnas.1307656110 23696658 PMC3677419 · DOI
  36. [49]Asidi A, N'Guessan R, Akogbeto M, Curtis C, Rowland M (2012) Loss of household protection from use of insecticide-treated nets against pyrethroid-resistant mosquitoes, benin. Emerg Infect Dis 18: 1101– 1106 10.3201/eid1807.120218 22709930 PMC3376816 · DOI
  37. [50]Kwiatkowska RM, Platt N, Poupardin R, Irving H, Dabire RK, et al (2013) Dissecting the mechanisms responsible for the multiple insecticide resistance phenotype in Anopheles gambiae s.s., M form, from Vallée du Kou, Burkina Faso. Gene 519: 98– 106 10.1016/j.gene.2013.01.036 23380570 PMC3611593 · DOI
  38. [51]Müller P, Donnelly MJ, Ranson H (2007) Transcription profiling of a recently colonised pyrethroid resistant Anopheles gambiae strain from Ghana. BMC Genomics 8: 36 10.1186/1471-2164-8-36 17261191 PMC1797171 · DOI
  39. [52]Müller P, Warr E, Stevenson BJ, Pignatelli PM, Morgan JC, et al (2008) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genet 4: e1000286 10.1371/journal.pgen.1000286 19043575 PMC2583951 · DOI
  40. [53]Ding Y, Ortelli F, Rossiter LC, Hemingway J, Ranson H (2003) The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. BMC Genomics 4: 35 10.1186/1471-2164-4-35 12914673 PMC194574 · DOI
  41. [54]Shang Q, Pan Y, Fang K, Xi J, Wong A, et al.. (2012) Extensive Ace2 Duplication and Multiple Mutations on Ace1 and Ace2 Are Related with High Level of Organophosphates Resistance in Aphis gossypii: 1–8. doi:10.1002/tox. 22489048 · DOI
  42. [55]Brooke BD, Kloke G, Hunt RH, Koekemoer LL, Tem E a, et al (2001) Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bull Entomol Res 91: 265– 272 10.1079/BER2001108 11587622 · DOI
  43. [56]Riveron J, Irving H (2013) Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus. Proc Natl Acad Sci U S A 110: 252– 257 10.1073/pnas.1216705110/-/DCSupplemental www.pnas.org/cgi/doi/10.1073/pnas.1216705110. 23248325 PMC3538203 · DOI
  44. [57]Wondji CS, Irving H, Morgan J, Lobo NF, Collins FH, et al (2009) Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Res 19: 452– 459 10.1101/gr.087916.108 19196725 PMC2661802 · DOI
  45. [58]Christian RN, Strode C, Ranson H, Coetzer N, Coetzee M, et al (2011) Microarray analysis of a pyrethroid resistant African malaria vector, Anopheles funestus, from southern Africa. Pestic Biochem Physiol 99: 140– 147 10.1016/j.pestbp.2010.11.010 · DOI
  46. [59]Amenya DA, Naguran R, Lo T-CM, Ranson H, Spillings BL, et al (2008) Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles Funestus, resistant to pyrethroids. Insect Mol Biol 17: 19– 25 10.1111/j.1365-2583.2008.00776.x 18237281 · DOI
  47. [60]Chanda E, Chanda J, Kandyata A, Phiri FN, Muzia L, et al (2013) Efficacy of ACTELLIC 300 CS, Pirimiphos Methyl, for Indoor Residual Spraying in Areas of High Vector Resistance to Pyrethroids and Carbamates in Zambia. J Med Entomol 50: 1275– 1281. 24843932
  48. [61]Chiu T-L, Wen Z, Rupasinghe SG, Schuler M (2008) Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc Natl Acad Sci U S A 105: 8855– 8860 10.1073/pnas.0709249105 18577597 PMC2449330 · DOI

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Authors
Thomsen, E. K., Strode, C., Hemmings, K., Hughes, A. J., Chanda, E., Musapa, M., Kamuliwo, M., Phiri, F. N., Muzia, L., Chanda, J., Kandyata, A., Chirwa, B., Poer, K., Hemingway, J., Wondji, C. S., Ranson, H., & Coleman, M.
Affiliations
Liverpool School of Tropical Medicine (GB)
Corresponding author
Thomsen, Edward K.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2014-06-16
Volume
9
Issue
6
Pages
e99822
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0099822
PMC
PMC4059741
OpenAlex
W2027334075
Cited by
63
References
2
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FWCI
8.96
Type
journal article
Language
en
Open access
Licence
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)
  • Edge Hill University Research Information Repository (Edge Hill University) (submittedVersion, cc-by)
  • Edge Hill University (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
Wellcome Trust (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
  • Social Sciences › Sociology and Political Science › Dengue and Mosquito Control Research
Keywords
insecticide resistance, malaria vector control, resistance management, Anopheles gambiae, Anopheles funestus, pyrethroid resistance, carbamate resistance, DDT resistance, organophosphate resistance, target-site mutations, metabolic resistance, cytochrome P450, resistance monitoring, Zambia
MeSH terms
Acetylcholinesterase, Animals, Anopheles, DNA, Gene Expression Regulation, Genotype, Geography, Insect Vectors, Insecticide Resistance, Insecticides, Mosquito Control, Mutation, Parasites, Phenotype, World Health Organization, Zambia, Genes, Insect, Molecular Sequence Annotation, Spatio-Temporal Analysis

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