1921
Volume 88, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Anti-malaria interventions that rely on insecticides can be compromised by insecticide-resistance alleles among malaria vectors. We examined frequency changes of resistance alleles at two loci, knockdown resistance () and acetylcholinesterase-1 (), which confer resistance to pyrethroids and DDT, and carbamates, respectively. A total of 7,059 sensu stricto mosquitoes were analyzed from multiple sites across continental Equatorial Guinea. A subset of sites included samples collected pre-intervention (2007) and post-intervention (2009–2011). Both L1014S and L1014F resistance alleles were observed in almost all pre-intervention collections. In particular, L1014F was already at substantial frequencies in M form populations (17.6–74.6%), and at high frequencies (> 50%) in all but two S form populations. Comparison before and throughout anti-vector interventions showed drastic increases in L1014F, presumably caused by intensified selection pressure imposed by pyrethroids used in vector control efforts. In light of these findings, inclusion of other insecticide classes in any anti-vector intervention can be considered prudent.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.12-0467
2013-05-01
2017-11-18
Loading full text...

Full text loading...

/deliver/fulltext/14761645/88/5/897.html?itemId=/content/journals/10.4269/ajtmh.12-0467&mimeType=html&fmt=ahah

References

  1. Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Bergé JB, Devonshire AL, Guillet P, Pasteur N, Pauron D, , 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol 7: 179184.[Crossref]
  2. Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH, , 2000. Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol 9: 491497.[Crossref]
  3. Weill M, Malcolm C, Chandre F, Mogensen K, Berthomieu A, Marquine M, Raymond M, , 2004. The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 13: 17.[Crossref]
  4. Zlotkin E, , 1999. The insect voltage-gated sodium channel as target of insecticides. Annu Rev Entomol 44: 429455.[Crossref]
  5. Soderlund DM, Knipple DC, , 2003. The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochem Mol Biol 33: 563577.[Crossref]
  6. Pinto J, Lynd A, Vicente JL, Santolamazza F, Randle NP, Gentile G, Moreno M, Simard F, Charlwood JD, do Rosário VE, Caccone A, Della Torre A, Donnelly MJ, , 2007. Multiple origins of knockdown resistance mutations in the Afrotropical mosquito vector Anopheles gambiae . PLoS ONE 2: e1243.[Crossref]
  7. Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P, Chouaibou M, Ndjemai H, Simard F, , 2006. First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg 74: 795797.
  8. Pinto J, Lynd A, Elissa N, Donnelly MJ, Costa C, Gentile G, Caccone A, do Rosário VE, , 2006. Co-occurrence of east and West African kdr mutations suggests high levels of resistance to pyrethroid insecticides in Anopheles gambiae from Libreville, Gabon. Med Vet Entomol 20: 2732.[Crossref]
  9. Verhaeghen K, Van Bortel W, Roelants P, Backeljau T, Coosemans M, , 2006. Detection of the East and West African kdr mutation in Anopheles gambiae and Anopheles arabiensis from Uganda using a new assay based on FRET/Melt Curve analysis. Malar J 5: 1624.[Crossref]
  10. Yewhalaw D, Bortel WV, Denis L, Coosemans M, Duchateau L, Speybroeck N, , 2010. First evidence of high knockdown resistance frequency in Anopheles arabiensis (Diptera: Culicidae) from Ethiopia. Am J Trop Med Hyg 83: 122125.[Crossref]
  11. Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, Donnelly MJ, Petrarca V, Simard F, Pinto J, della Torre A, , 2008. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 7: 74.[Crossref]
  12. Ridl FC, Bass C, Torrez M, Govender D, Ramdeen V, Yellot L, Edu AE, Schwabe C, Mohloai P, Maharaj R, Kleinschmidt I, , 2008. A pre-intervention study of malaria vector abundance in Rio Muni, Equatorial Guinea: their role in malaria transmission and the incidence of insecticide resistance alleles. Malar J 7: 194203.[Crossref]
  13. Moreno M, Vicente JL, Cano J, Berzosa PJ, de Lucio A, Nzambo S, Bobuakasi L, Buatiche JN, Ondo M, Micha F, Do Rosario VE, Pinto J, Benito A, , 2008. Knockdown resistance mutations (kdr) and insecticide susceptibility to DDT and pyrethroids in Anopheles gambiae from Equatorial Guinea. Trop Med Int Health 13: 430433.[Crossref]
  14. Sharp BL, Ridl FC, Govender D, Kuklinski J, Kleinschmidt I, , 2007. Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malar J 6: 5259.[Crossref]
  15. Djègbè I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, Akogbéto M, Corbel V, , 2011. Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J 10: 261.[Crossref]
  16. Stump AD, Atieli FK, Vulule JM, Besansky NJ, , 2004. Dynamics of the pyrethroid knockdown resistance allele in western Kenyan populations of Anopheles gambiae in response to insecticide-treated bed net trials. Am J Trop Med Hyg 70: 591596.
  17. Mathias DK, Ochomo E, Atieli F, Ombok M, Bayoh MN, Olang G, Muhia D, Kamau L, Vulule JM, Hamel MJ, Hawley WA, Walker ED, Gimnig JE, , 2011. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in western Kenya. Malar J 10: 10.[Crossref]
  18. Padonou GG, Sezonlin M, Ossé R, Aizoun N, Oké-Agbo F, Oussou O, Gbédjissi G, Akogbéto M, , 2012. Impact of three years of large scale indoor residual spraying (IRS) and insecticide treated nets (ITNs) interventions on insecticide resistance in Anopheles gambiae s.l. in Benin. Parasit Vectors. 5: 7282.[Crossref]
  19. Verhaeghen K, Bortel WV, Roelants P, Okello PE, Talisuna A, Coosemans M, , 2010. Spatio-temporal patterns in kdr frequency in permethrin and DDT resistant Anopheles gambiae s.s. from Uganda. Am J Trop Med Hyg 82: 566573.[Crossref]
  20. della Torre A, Fanello C, Akogbeto M, Dossou-Yovo J, Favia G, Petrarca V, Coluzzi M, , 2001. Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol Biol 20: 918.[Crossref]
  21. Yewhalaw D, Wassie F, Steurbaut W, Spanoghe P, Van Bortel W, Denis L, Tessema DA, Getachew Y, Coosemans M, Duchateau L, Speybroeck N, , 2011. Multiple insecticide resistance: an impediment to insecticide-based malaria vector control program. PLoS ONE 6: e16066.[Crossref]
  22. Czeher C, Labbo R, Arzika I, Duchemin JB, , 2008. Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation. Malar J 7: 189196.[Crossref]
  23. Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M, , 2008. Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg 102: 591598.[Crossref]
  24. Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS, , 2010. Pyrethroid resistance in an Anopheles funestus population from Uganda. PLoS ONE 5: e11872.[Crossref]
  25. Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J, , 2003. Molecular evidence for a kdr-like pyrethroid resistance mechanism in the malaria vector mosquito Anopheles stephensi . Med Vet Entomol 17: 138144.[Crossref]
  26. Singh OP, Bali P, Hemingway J, Subbarao SK, Dash AP, Adak T, , 2009. PCR-based methods for the detection of L1014 kdr mutation in Anopheles culicifacies sensu lato. Malar J 8: 154.[Crossref]
  27. Singh OP, Dykes CL, Das MK, Pradhan S, Bhatt RM, Agrawal OP, Adak T, , 2010. Presence of two alternative kdr-like mutations, L1014F and L1014S, and a novel mutation, V1010L, in the voltage gated Na+ channel of Anopheles culicifacies from Orissa, India. Malar J 9: 146.[Crossref]
  28. Djogbénou L, Dabiré R, Diabaté A, Kengne P, Akogbéto M, Hougard JM, Chandre F, , 2008. Identification and geographic distribution of the ACE-1R mutation in the malaria vector Anopheles gambiae in south-western Burkina Faso, West Africa. Am J Trop Med Hyg 78: 298302.
  29. Djogbénou L, Labbé P, Chandre F, Pasteur N, Weill M, , 2009. Ace-1 duplication in Anopheles gambiae: a challenge for malaria control. Malar J 18: 7075.[Crossref]
  30. Nwane P, Etang J, Chouaibou M, Toto JC, Kerah-Hinzoumbé C, Mimpfoundi R, Awono-Ambene HP, Simard F, , 2009. Trends in DDT and pyrethroid resistance in Anopheles gambiae s.s. populations from urban and agro-industrial settings in southern Cameroon. BMC Infect Dis 30: 163171.[Crossref]
  31. Djogbénou L, Chandre F, Berthomieu A, Dabiré R, Koffi A, Alout H, Weill M, , 2008. Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s.s. PLoS ONE 3: e2172.[Crossref]
  32. Chandre F, Darriet F, Doannio JM, Rivière F, Pasteur N, Guillet P, , 1997. Distribution of organophosphate and carbamate resistance in Culex pipiens quinquefasciatus (Diptera: Culicidae) in West Africa. J Med Entomol 34: 664671.[Crossref]
  33. N'Guessan R, Darriet F, Guillet P, Carnevale P, Traore-Lamizana M, Corbel V, Koffi AA, Chandre F, , 2003. Resistance to carbosulfan in Anopheles gambiae from Ivory Coast, based on reduced sensitivity of acetylcholinesterase. Med Vet Entomol 17: 1925.[Crossref]
  34. Ahoua Alou LP, Koffi AA, Adja MA, Tia E, Kouassi PK, Koné M, Chandre F, , 2010. Distribution of ace-1R and resistance to carbamates and organophosphates in Anopheles gambiae s.s. populations from Côte d'Ivoire. Malar J 9: 167173.[Crossref]
  35. Corbel V, N'Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, Akogbéto M, Hougard JM, Rowland M, , 2007. Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 101: 207216.[Crossref]
  36. Dabiré KR, Diabaté A, Namontougou M, Djogbenou L, Kengne P, Simard F, Bass C, Baldet T, , 2009. Distribution of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae s.l. populations from Burkina Faso (West Africa). Trop Med Int Health 14: 396403.[Crossref]
  37. Cohnstaedt LW, Gillen JI, Munstermann LE, , 2008. Light-emitting diode technology improves insect trapping. J Am Mosq Control Assoc 24: 331334.[Crossref]
  38. Scott J, Brogdon W, Collins F, , 1993. Identification of single specimens of the Anopheles gambiae group by polymerase chain reaction. Am J Trop Med Hyg 49: 520529.
  39. Fanello C, Santolamazza F, della Torre A, , 2002. Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol 16: 461464.[Crossref]
  40. Bass C, Nikou D, Donnelly MJ, Williamson MS, Ranson H, Ball A, Vontas J, Field LM, , 2007. Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods. Malar J 6: 111121.[Crossref]
  41. Bass C, Nikou D, Vontas J, Donnelly MJ, Williamson MS, Field LM, , 2010. The vector population monitoring tool (VPMT): high-throughput DNA-based diagnostics for the monitoring of mosquito vector populations. Malar Res Treat 2010: e190434.
  42. Dalet D, , d-maps.com. Available at: http://d-maps.com/m/guineeeq/guineeeq50.pdf/. Accessed July 16, 2012.
  43. Raymond M, Rousset F, , 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86: 248249.[Crossref]
  44. Excoffier L, Lischer HE, , 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 10: 564.[Crossref]
  45. Joosse SA, , 2011. Two-Proportion Z-Test Calculator. Available at: http://in-silico.net/statistics/ztest.
  46. Athrey G, Hodges TK, Reddy MR, Overgaard HJ, Matias A, Ridl FC, Kleinschmidt I, Caccone A, Slotman MA, , 2012. The effective population size of malaria mosquitoes: large impact of vector control. PLoS Genet 8: e1003097.[Crossref]
  47. Pritchard JK, Stephens M, Donnelly P, , 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945959.
  48. Earl DA, von Holdt BM, , 2011. Structure Harvester: A Website and Program for Visualizing Structure Output and Implementing the Evanno Method. Conserv Gene Resource. doi:10.1007/s12686-011-9548-7. Available at: http://taylor0.biology.ucla.edu/struct_harvest/. Accessed March 4, 2012.
  49. Reimer L, Fondjo E, Patchoké S, Diallo B, Lee Y, Ng A, Ndjemai HM, Atangana J, Traore SF, Lanzaro G, Cornel AJ, , 2008. Relationship between kdr mutation and resistance to pyrethroid and DDT insecticides in natural populations of Anopheles gambiae . J Med Entomol 45: 260266.[Crossref]
  50. Lynd A, Weetman D, Barbosa S, Egyir Yawson A, Mitchell S, Pinto J, Hastings I, Donnelly MJ, , 2010. Field, genetic, and modeling approaches show strong positive selection acting upon an insecticide resistance mutation in Anopheles gambiae s.s. Mol Biol Evol 27: 11171125.[Crossref]
  51. CIA World Factbook - Equatorial Guinea. Available at: http://www.cia.gov/library/publications/the-world-factbook/geos/ek.html. Accessed April 2, 2012.
  52. Molina R, Benito A, Roche J, Blanca F, Amela C, Sanchez A, Alvar J, , 1993. Baseline entomological data for a pilot malaria control program in Equatorial Guinea. J Med Entomol 30: 622624.[Crossref]
  53. Donnelly MJ, Corbel V, Weetman D, Wilding CS, Williamson MS, Black WC, IV, 2009. Does kdr genotype predict insecticide-resistance phenotype in mosquitoes? Trends Parasitol 25: 213219.[Crossref]
  54. Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, D'Alessandro U, Coosemans M, , 2008. A significant increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands. Trop Med Int Health 13: 14791487.[Crossref]
  55. Protopopoff N, Van Bortel W, Marcotty T, Van Herp M, Maes P, Baza D, D'Alessandro U, Coosemans M, , 2007. Spatial targeted vector control in the highlands of Burundi and its impact on malaria transmission. Malar J 6: 158.[Crossref]
  56. Ngufor C, N'Guessan R, Boko P, Odjo A, Vigninou E, Asidi A, Akogbeto M, Rowland M, , 2011. Combining indoor residual spraying with chlorfenapyr and long-lasting insecticidal bed nets for improved control of pyrethroid-resistant Anopheles gambiae: an experimental hut trial in Benin. Malar J 10: 343349.[Crossref]
  57. Hardstone MC, Leichter CA, Scott JG, , 2009. Multiplicative interaction between the two major mechanisms of permethrin resistance, kdr and cytochrome P450-monooxygenase detoxification, in mosquitoes. J Evol Biol 22: 416423.[Crossref]
  58. Overgaard HJ, Reddy VP, Abaga S, Matias A, Reddy MR, Kulkarni V, Schwabe C, Segura L, Kleinschmidt I, Slotman MA, , 2012. Malaria transmission after five years of vector control on Bioko Island, Equatorial Guinea. Parasit Vectors 5: 253.[Crossref]
  59. Djogbénou L, Weill M, Hougard JM, Raymond M, Akogbéto M, Chandre F, , 2007. Characterization of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance. J Med Entomol 44: 805810.
  60. Moreno M, Salgueiro P, Vicente JL, Cano J, Berzosa PJ, de Lucio A, Simard F, Caccone A, Do Rosario VE, Pinto J, Benito A, , 2007. Genetic population structure of Anopheles gambiae in Equatorial Guinea. Malar J 6: 137.[Crossref]
  61. Slotman MA, Parmakelis A, Marshall JC, Awono-Ambene PH, Antonio-Nkondjo C, Simard F, Caccone A, Powell JR, , 2007. Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis . PLoS ONE 2: e793.[Crossref]
  62. Ndiath MO, Sarr JB, Gaayeb L, Mazenot C, Sougoufara S, Konate L, Remoue F, Hermann E, Trape JF, Riveau G, Sokhna C, , 2012. Low and seasonal malaria transmission in the middle Senegal River basin: identification and characteristics of Anopheles vectors. Parasit Vectors. 5: 21.[Crossref]
  63. Dery DB, Brown C, Asante KP, Adams M, Dosoo D, Amenga-Etego S, Wilson M, Chandramohan D, Greenwood B, Owusu-Agyei S, , 2010. Patterns and seasonality of malaria transmission in the forest-savannah transitional zones of Ghana. Malar J 9: 314.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.12-0467
Loading
/content/journals/10.4269/ajtmh.12-0467
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

  • Received : 01 Aug 2012
  • Accepted : 21 Jan 2013

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error