1921
Volume 98, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Vector control programs, particularly in the form of insecticide-treated bed nets (ITNs), are essential for achieving malaria elimination goals. Recent reports of increasing knockdown resistance () mutation frequencies for in Western Kenya heightens the concern on the future effectiveness of ITNs in Kenya. We examined resistance in populations across Kenya through mutations and World Health Organization–recommended bioassays. We detected two alleles, L1014F and L1014S. mutations were found in five of the 11 study sites, with mutation frequencies ranging from 3% to 63%. In two Western Kenya populations, the L1014F allele frequency was as high as 10%. The L1014S frequency was highest at Chulaimbo at 55%. Notably, the L1014F mutation was found to be associated with pyrethroid resistance at Port Victoria, but mutations were not significantly associated with resistance at Chulaimbo, which had the highest mutation frequency among all sites. This study demonstrated the emerging pyrethroid resistance in and that pyrethroid resistance may be related to mutations. Resistance monitoring and management are urgently needed for this species in Kenya where resistance is emerging and its abundance is becoming predominant. mutations may serve as a biomarker for pyrethroid resistance in .

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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References

  1. World Health Organization, 2014. World Malaria Report 2014. Geneva, Switzerland: WHO.
  2. Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, Vulule JM, Hawley WA, Hamel MJ, Walker ED, , 2010. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9: 62. [Google Scholar]
  3. Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, , 2011. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 9198. [Google Scholar]
  4. O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, Newton CR, Marsh K, , 2008. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372: 15551562. [Google Scholar]
  5. Mathias DK, 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. [Google Scholar]
  6. Ochomo E, 2015. Presence of the knockdown resistance mutation, Vgsc-1014F in Anopheles gambiae and An. arabiensis in western Kenya. Parasit Vectors 8: 616. [Google Scholar]
  7. Ochomo E, Bayoh MN, Brogdon WG, Gimnig JE, Ouma C, Vulule JM, Walker ED, , 2013. Pyrethroid resistance in Anopheles gambiae s.s. and Anopheles arabiensis in western Kenya: phenotypic, metabolic and target site characterizations of three populations. Med Vet Entomol 27: 156164. [Google Scholar]
  8. Pauron D, Barhanin J, Amichot M, Pralavorio M, Berge JB, Lazdunski M, , 1989. Pyrethroid receptor in the insect Na sup+ channel: alteration of its properties in pyrethroid-resistant flies. Biochemistry 28: 16731677. [Google Scholar]
  9. 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. [Google Scholar]
  10. Ranson H, Jenson 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. [Google Scholar]
  11. Chandre F, Manguin S, Brengues C, Dossou YJ, Darriet F, Diabate A, Carnevale P, Guillet P, , 1999. Current distribution of a pyrethroid resistance gene (kdr) in Anopheles gambiae complex from west Africa and further evidence for reproductive isolation of the Mopti form. Parassitologia 41: 319322. [Google Scholar]
  12. Awolola TS, Brooke BD, Koekemoer LL, Coetzee M, , 2003. Absence of the kdr mutation in the molecular ‘M’form suggests different pyrethroid resistance mechanisms in the malaria vector mosquito Anopheles gambiae s.s. Trop Med Int Health 8: 420422. [Google Scholar]
  13. Fanello C, Petrarca V, Della Torre A, Santolamazza F, Dolo G, Coulibaly M, Alloueche A, Curtis CF, Toure YT, Coluzzi M, , 2003. The pyrethroid knock‐down resistance gene in the Anopheles gambiae complex in Mali and further indication of incipient speciation within An. gambiae s.s. Insect Mol Biol 12: 241245. [Google Scholar]
  14. Yawson AE, McCall PJ, Wilson MD, Donnelly MJ, , 2004. Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol 18: 372377. [Google Scholar]
  15. 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. [Google Scholar]
  16. Santolamazza F, 2008. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 7: 74. [Google Scholar]
  17. 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: 52. [Google Scholar]
  18. Balkew M, Gebre-Michael T, Hailu A, , 2003. Insecticide susceptibility level of Anopheles arabiensis in two agro-development localities in eastern Ethiopia. Parassitologia 45: 13. [Google Scholar]
  19. Ndjemaï HN, Patchoké S, Atangana J, Etang J, Simard F, Bilong CF, Reimer L, Cornel A, Lanzaro GC, Fondjo E, , 2009. The distribution of insecticide resistance in Anopheles gambiae s.l. populations from Cameroon: an update. Trans R Soc Trop Med Hyg 103: 11271138. [Google Scholar]
  20. Himeidan YE, Chen H, Chandre F, Donnelly MJ, Yan G, , 2007. Permethrin and DDT resistance in the malaria vector Anopheles arabiensis from eastern Sudan. Am J Trop Med Hyg 77: 10661068. [Google Scholar]
  21. Alout H, Yameogo B, Djogbénou LS, Chandre F, Dabiré RK, Corbel V, Cohuet A, , 2014. Interplay between Plasmodium infection and resistance to insecticides in vector mosquitoes. J Infect Dis 210: 14641470. [Google Scholar]
  22. Noor AM, Amin AA, Akhwale WS, Snow RW, , 2007. Increasing coverage and decreasing inequity in insecticide-treated bed net use among rural Kenyan children. PLoS Med 4: e255. [Google Scholar]
  23. Wanjala CL, Mbugi JP, Ototo E, Gesuge M, Afrane YA, Atieli HE, Zhou G, Githeko AK, Yan G, , 2015. Pyrethroid and DDT resistance and organophosphate susceptibility among Anopheles spp. mosquitoes, western Kenya. Emerg Infect Dis 21: 2178. [Google Scholar]
  24. Sougoufara S, Harry M, Doucouré S, Sembène PM, Sokhna C, , 2016. Shift in species composition in the Anopheles gambiae complex after implementation of long‐lasting insecticidal nets in Dielmo, Senegal. Med Vet Entomol 30: 365368. [Google Scholar]
  25. Mwangangi JM, Muturi EJ, Muriu SM, Nzovu J, Midega JT, Mbogo C, , 2013. The role of Anopheles arabiensis and Anopheles coustani in indoor and outdoor malaria transmission in Taveta District, Kenya. Parasit Vectors 6: 114. [Google Scholar]
  26. Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G, , 2015. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J 14: 244. [Google Scholar]
  27. Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, Bruce J, Mosha FW, Rowland MW, , 2012. Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLoS One 7: e31481. [Google Scholar]
  28. Kamau L, Agai D, Matoke D, Wachira L, Gikandi G, Vulule JM, , 2008. Status of insecticide susceptibility in Anopheles gambiae sensu lato and Anopheles funestus mosquitoes from western Kenya. J Insect Sci 8: 11. [Google Scholar]
  29. Kawada H, 2011. Multimodal pyrethroid resistance in malaria vectors, Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus s.s. in western Kenya. PLoS One 6: e22574. [Google Scholar]
  30. World Health Organization (WHO), 2013. Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes. Geneva, Switzerland: WHO.
  31. Severson DW, , 1997. RFLP analysis of insect genomes. The Molecular Biology of Insect Disease Vectors. London, United Kingdom: Springer, 309320.
  32. 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: 520529. [Google Scholar]
  33. 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: 111. [Google Scholar]
  34. Kabula B, Kisinza W, Tungu P, Ndege C, Batengana B, Kollo D, Malima R, Kafuko J, Mohamed M, Magesa S, , 2014. Co‐occurrence and distribution of East (L1014S) and West (L1014F) African knock‐down resistance in Anopheles gambiae sensu lato population of Tanzania. Trop Med Int Health 19: 331341. [Google Scholar]
  35. Fettene M, Olana D, Christian RN, Koekemoer LL, Coetzee M, , 2013. Insecticide resistance in Anopheles arabiensis from Ethiopia. Afr Entomol 21: 8994. [Google Scholar]
  36. Yewhalaw D, Van Bortel W, 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. [Google Scholar]
  37. Yewhalaw D, 2011. Multiple insecticide resistance: an impediment to insecticide-based malaria vector control program. PLoS One 6: e16066. [Google Scholar]
  38. Abdalla H, Wilding CS, Nardini L, Pignatelli P, Koekemoer LL, Ranson H, Coetzee M, , 2014. Insecticide resistance in Anopheles arabiensis in Sudan: temporal trends and underlying mechanisms. Parasit Vectors 7: 213. [Google Scholar]
  39. 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. [Google Scholar]
  40. Chen H, Githeko AK, Githure JI, Mutunga J, Zhou G, Yan G, , 2008. Monooxygenase levels and knockdown resistance (kdr) allele frequencies in Anopheles gambiae and Anopheles arabiensis in Kenya. J Med Entomol 45: 242250. [Google Scholar]
  41. Amenya DA, Naguran R, Lo T, Ranson H, Spillings BL, Wood OR, Brooke BD, Coetzee M, Koekemoer LL, , 2008. Over expression of a cytochrome P450 (CYP6P9) in a major African malaria vector, Anopheles funestus, resistant to pyrethroids. Insect Mol Biol 17: 1925. [Google Scholar]
  42. Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS, , 2010. High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLoS One 5: e11010. [Google Scholar]
  43. Mawejje HD, Wilding CS, Rippon EJ, Hughes A, Weetman D, Donnelly MJ, , 2013. Insecticide resistance monitoring of field‐collected Anopheles gambiae s.l. populations from Jinja, eastern Uganda, identifies high levels of pyrethroid resistance. Med Vet Entomol 27: 276283. [Google Scholar]
  44. Weetman D, Steen K, Rippon EJ, Mawejje HD, Donnelly MJ, Wilding CS, , 2014. Contemporary gene flow between wild An. gambiae s.s. and An. arabiensis. Parasit Vectors 7: 345. [Google Scholar]
  45. Asale A, Getachew Y, Hailesilassie W, Speybroeck N, Duchateau L, Yewhalaw D, , 2014. Evaluation of the efficacy of DDT indoor residual spraying and long-lasting insecticidal nets against insecticide resistant populations of Anopheles arabiensis Patton (Diptera: Culicidae) from Ethiopia using experimental huts. Parasit Vectors 7: 131. [Google Scholar]
  46. Mzilahowa T, 2016. Increasing insecticide resistance in Anopheles funestus and Anopheles arabiensis in Malawi, 2011–2015. Malar J 15: 563. [Google Scholar]
  47. Lwetoijera DW, Harris C, Kiware SS, Dongus S, Devine GJ, McCall PJ, Majambere S, , 2014. Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. Malar J 13: 331. [Google Scholar]
  48. Haji KA, Khatib BO, Smith S, Ali AS, Devine GJ, Coetzee M, Majambere S, , 2013. Challenges for malaria elimination in Zanzibar: pyrethroid resistance in malaria vectors and poor performance of long-lasting insecticide nets. Parasit Vectors 6: 82. [Google Scholar]
  49. Jones CM, 2013. The dynamics of pyrethroid resistance in Anopheles arabiensis from Zanzibar and an assessment of the underlying genetic basis. Parasit Vectors 6: 343. [Google Scholar]
  50. Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S, Doumbia S, Schlein Y, , 2010. Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malar J 9: 262. [Google Scholar]
  51. Kroeger A, Horstick O, Riedl C, Kaiser A, Becker N, , 1995. The potential for malaria control with the biological larvicide Bacillus thuringiensis israelensis (Bti) in Peru and Ecuador. Acta Trop 60: 4757. [Google Scholar]
  52. Fillinger U, Lindsay SW, , 2006. Suppression of exposure to malaria vectors by an order of magnitude using microbial larvicides in rural Kenya. Trop Med Int Health 11: 16291642. [Google Scholar]
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  • Received : 07 Jun 2017
  • Accepted : 17 Nov 2017
  • Published online : 22 Jan 2018

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