Insecticide Resistance Allele Frequencies in Anopheles gambiae before and after Anti-Vector Interventions in Continental Equatorial Guinea

Michael R. Reddy Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Adrian Godoy Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Kirstin Dion Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Abrahan Matias Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Kevin Callender Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Anthony E. Kiszewski Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Immo Kleinschmidt Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Frances C. Ridl Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Jeffrey R. Powell Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Adalgisa Caccone Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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Michel A. Slotman Department of Epidemiology and Public Health, Department of Ecology and Evolutionary Biology, and Department of Psychology, Yale University, New Haven, Connecticut; Medical Care Development International Inc., Silver Spring, Maryland; Department of Natural and Applied Sciences, Bentley University, Waltham, Massachusetts; London School of Hygiene and Tropical Medicine, London, United Kingdom; Malaria Research Lead Programme, Medical Research Council, Durban, South Africa; Department of Entomology, Texas A&M University, College Station, Texas

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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 (kdr) and acetylcholinesterase-1 (ace-1), which confer resistance to pyrethroids and DDT, and carbamates, respectively. A total of 7,059 Anopheles gambiae 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.

Author Notes

* Address correspondence to Michael R. Reddy, Department of Epidemiology and Public Health, Yale University, 170 Whitney Avenue, ESC 158b, New Haven CT 06511. E-mail: michael.r.reddy@gmail.com

Author contributions: Michael R. Reddy conceived and planned the study, performed a portion of the pre-intervention collections, supervised the molecular analyses of all specimens, and composed the first draft of the manuscript; Adrian Godoy, performed molecular analyses of collected specimens and contributed to manuscript preparation; Kirstin Dion, supervised and performed molecular analyses and contributed to manuscript preparation; Abrahan Matias, coordinated and supervised the 2009–2011 field collections; Kevin Callender contributed statistical analysis assistance; Anthony E. Kiszewski participated in the study design, provided statistical analysis assistance and editorial input, and contributed to manuscript preparation; Immo Kleinschmidt designed the pre-intervention window trap monitoring system and facilitated the use of archived mosquito samples collected before initiation of intervention activities; Frances C. Ridl processed and archived mosquitoes collected during the pre-intervention period and assisted in the transfer of these specimens to the Yale laboratory for further molecular analysis; Jeffrey R. Powell planned and supervised the study and assisted in analysis of results; Adalgisa Caccone planned and supervised the study, assisted in analysis of results, and contributed to manuscript preparation; and Michel A. Slotman planned and supervised the study, assisted in analysis of results, and co-wrote the manuscript.

Financial support: This study was supported by an operational research grant awarded by the Bioko Island Malaria Control Program to Michael A. Slotman and Adalgisa Caccone. The Bioko Island Malaria Control Program is supported by a consortium led by Marathon Oil Corporation (Houston, TX) and the government of Equatorial Guinea. This study was also supported by EGMCI, which was supported through a grant from the Global Fund to Fight AIDS, Tuberculosis and Malaria.

Authors' addresses: Michael R. Reddy, Department of Epidemiology and Public Health, Yale University, New Haven CT, E-mail: michael.r.reddy@gmail.com. Adrian Godoy, Kirstin Dion, Jeffrey R. Powell, and Adalgisa Caccone, Department of Ecology and Evolutionary Biology, Yale University, New Haven CT, E-mails: adrian.godoy2008@gmail.com, kirstin.dion@yale.edu, jeffrey.powell@yale.edu, and adalgisa.caccone@yale.edu. Abrahan Matias, Medical Care Development International Inc., Silver Spring, MD, E-mail: amatias@mcd.org. Kevin Callender, Department of Psychology, Yale University, New Haven, CT, E-mail: kevin.callender@yale.edu. Anthony E. Kiszewski, Department of Natural and Applied Sciences, Bentley University, Waltham, MA, E-mail: akiszewski@bentley.edu. Immo Kleinschmidt, Medical Research Council Topical Epidemiology Group, London School of Hygiene and Tropical Medicine, London, UK, E-mail: immo.kleinschmidt@lshtm.ac.uk. Frances C. Ridl, Malaria Research Lead Programme, Medical Research Council, Durban, South Africa, E-mail: franridl@gmail.com. Michel A. Slotman, Department of Entomology, Texas A&M University, College Station, TX, E-mail: maslotman@tamu.edu.

  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Zlotkin E, 1999. The insect voltage-gated sodium channel as target of insecticides. Annu Rev Entomol 44: 429455.

  • 5.

    Soderlund DM, Knipple DC, 2003. The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochem Mol Biol 33: 563577.

  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Cohnstaedt LW, Gillen JI, Munstermann LE, 2008. Light-emitting diode technology improves insect trapping. J Am Mosq Control Assoc 24: 331334.

  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
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