Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Monitoring Insecticide Resistance and Target Site Mutations of L1014 Kdr And G119 Ace Alleles in Five Mosquito Populations in Korea

  • Park, Seo Hye (Department of Parasitology and Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine) ;
  • Jun, Hojong (Department of Parasitology and Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine) ;
  • Ahn, Seong Kyu (Department of Parasitology and Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine) ;
  • Lee, Jinyoung (Department of Parasitology and Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine) ;
  • Yu, Sung-Lim (Inha Research Institute for Medical Sciences, Inha University School of Medicine) ;
  • Lee, Sung Keun (Department of Pharmacology, Inha University School of Medicine) ;
  • Kang, Jung-Mi (Department of Parasitology and Tropical Medicine, and Institute of Health Sciences, Gyeongsang National University College of Medicine) ;
  • Kim, Hyunwoo (Division of Vectors and Parasitic Diseases, Korea Centers for Disease Control and Prevention) ;
  • Lee, Hee-Il (Division of Vectors and Parasitic Diseases, Korea Centers for Disease Control and Prevention) ;
  • Hong, Sung-Jong (Department of Medical Environmental Biology, Chung-Ang University College of Medicine) ;
  • Na, Byoung-Kuk (Department of Parasitology and Tropical Medicine, and Institute of Health Sciences, Gyeongsang National University College of Medicine) ;
  • Bahk, Young Yil (Department of Biotechnology, College of Biomedical and Health Science, Konkuk University) ;
  • Kim, Tong-Soo (Department of Parasitology and Tropical Medicine & Global Resource Bank of Parasitic Protozoa Pathogens, Inha University School of Medicine)
  • Received : 2020.05.30
  • Accepted : 2020.09.01
  • Published : 2020.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

Mosquitoes are globally distributed and important vectors for the transmission of many human diseases. Mosquito control is a difficult task and the cost of preventing mosquito-borne diseases is much lower than that for curing the associated diseases. Thus, chemical control remains the most effective tool for mosquito. Due to the long-term intensive use of insecticides to control mosquito vectors, resistance to most chemical insecticides has been reported. This study aimed to investigate the relationship between insecticide resistance and target site mutation of L1014 kdr and G119 ace alleles in 5 species/species group of mosquitoes (Aedes vexans, Ae. albopictus, Anopheles spp., Culex pipiens complex, and Cx. tritaeniorhynchus) obtained from 6 collection sites. For Anopheles spp., the proportion of mosquitoes with mutated alleles in L1014 was 88.4%, homozygous resistant genotypes were observed in 46.7%, and heterozygous resistant genotypes were observed in 41.8%. For the Cx. pipiens complex and Cx. tritaeniorhynchus species, homozygous resistant genotypes were found in 25.9% and 9.8%, respectively. However, target site mutation of L1014 in the Ae. vexans nipponii and Ae. albopictus species was not observed. Anopheles spp., Cx. pipiens complex, and Cx. tritaeniorhynchus mosquitoes were resistant to deltamethrin and chlorpyriphos, whereas Ae. vexans nipponii and Ae. albopictus were clearly susceptible. We also found a correlation between the resistance phenotype and the presence of the L1014 kdr and G119 ace mutations only in the Anopheles spp. population. In this study, we suggest that insecticide resistance poses a growing threat and resistance management must be integrated into all mosquito control programs.

Keywords

References

  1. Korea Meteorological Administration (KMA). 2019 Abnormal Weather Report [Internet]; [cited 2020 Feb 20]. Available from: http://www.climate.go.kr/home/bbs/view.php?code=93&bname=abnormal&vcode=6385&cpage=1&vNum=Notice&skind=&sword=&category1=&category2.
  2. Yeom JS. Current status and outlook of mosquito-borne diseases in Korea. J Korean Med Assoc 2017; 60: 468-474 (Korean). https://doi.org/10.5124/jkma.2017.60.6.468
  3. Bahk YY, Lee HW, Na BK, Kim J, Jin K, Hong YS, Kim TS. Epidemiological characteristics of re-emerging vivax malaria in the Republic of Korea (1993-2017). Korean J Parasitol 2018; 56: 531-543. https://doi.org/10.3347/kjp.2018.56.6.531
  4. Korea Centers for Disease Control and Prevention. Epidemiology and Management of Vaccine Preventable Diseases. 5th eds. Cheongju, Korea. Korea Centers for Disease Control and Prevention. 2017.
  5. Kharkongor M, Hooroo RNK, Dey S. Effects of the insecticide chlorpyrifos, on hatching, mortality and morphology of Duttaphrynus melanostictus embryos. Chemosphere 2018; 210: 917-921. https://doi.org/10.1016/j.chemosphere.2018.07.097
  6. Lu Z, Gan J, Cui X, Delgado-Moreno L, Lin K. Understanding the bioavailability of pyrethroids in the aquatic environment using chemical approaches. Environ Int 2019; 129: 194-207. https://doi.org/10.1016/j.envint.2019.05.035
  7. Hemingway J, Field L, Vontas J. An overview of insecticide resistance. Science 2002; 298: 96-97. https://doi.org/10.1126/science.1078052
  8. Ketterman AJ, Saisawang C, Wongsantichon J. Insect glutathione transferases. Drug Metab Rev 2011; 43: 253-265. https://doi.org/10.3109/03602532.2011.552911
  9. Zaim M, Guillet P. Alternative insecticides: an urgent need. Trends Parasitol 2002; 18: 161-163. https://doi.org/10.1016/S1471-4922(01)02220-6
  10. Liu N. Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Ann Rev Entomol 2015; 60: 537-559. https://doi.org/10.1146/annurev-ento-010814-020828
  11. Main BJ, Everitt A, Cornel AJ, Hormozdiari F, Lanzaro GC. Genetic variation associated with increased insecticide resistance in the malaria mosquito, Anopheles coluzzii. Parasit Vectors 2018; 11: 225 https://doi.org/10.1186/s13071-018-2817-5
  12. Dong K. A single amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroids insecticides in German cockroach. Insect Biochem Mol Biol 1997; 27: 93-100. https://doi.org/10.1016/S0965-1748(96)00082-3
  13. Busvine JR. Mechanism of resistance to insecticide in houseflies. Nature 1951; 168: 193-195. https://doi.org/10.1038/168193a0
  14. Soderlund DM, Knipple DC. The molecular biology of knockdown resistance to pyrethroids insecticides. Insec Biochem Mol Biol 2003; 33: 563-577. https://doi.org/10.1016/S0965-1748(03)00023-7
  15. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M. Comparative genomics: Insecticide resistance in mosquito vectors. Nature 2003; 423: 136-137.
  16. Weill M, Malcolm C, Chandre F, Mogensen K, Berthomieu A, Marquine M, Raymond M. The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 2004; 13: 1-7. https://doi.org/10.1111/j.1365-2583.2004.00452.x
  17. Lanzaro GC, Toure YT, Carnahan J, Zheng L, Dolo G, Traore S, Petrarca V, Vernick KD, Taylor CE. Complexities in the genetic structure of Anopheles gambiae populations in west Africa as revealed by microsatellite DNA analysis. Proc Natl Acad Sci USA 1998; 95: 14260-14265. https://doi.org/10.1073/pnas.95.24.14260
  18. Schmidt JM, Good RT, Appleton B, Sherrard J, Raymant GC, Bogwitz MR, Martin J, Daborn PJ, Goddard ME, Batterham P, Robin C. Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet 2010; 6: e1000998. https://doi.org/10.1371/journal.pgen.1000998
  19. Tanaka K, Mizusawa K, Saugsad ES. A Revision of the Adult and Larval Mosquitoes of Japan (including the Ryukyu Archipelago and the Ogasawara Islands) and Korea (Diptera: Culicidae). Ann Arbor, USA. American Entomological Institute. 1979.
  20. Lee KW. A Revision of the Illustrated Taxonomic Keys to Genera and Species of Female Mosquitoes of Korea. Seoul, Korea: Department of the Army, 5th Medical Detachment, 168th Medical Battalion, 18th Medical Command. 1998, pp 40.
  21. Jegal S, Jun H, Kim-Jeon MD, Park SH, Ahn SK, Lee J, Gong YW, Joo K, Kwon MJ, Roh JY, Lee WG, Lee W, Bahk YY, Kim TS. Three-year surveillance of culicine mosquiotes (Diptera: Culicidae) for flavivirus infections in Incheon metropolitan city and Hwaseong-si of Gyeonggi-do province, Republic of Korea. Acta Trop 2020; 202: 105258. https://doi.org/10.1016/j.actatropica.2019.105258
  22. Bahk YY, Jun H, Park SH, Jung H, Jegal S, Kim-Jeon MD, Roh JY, Lee WG, Ahn SK, Lee J, Joo K, Gong YW, Kwon MJ, Kim TS. Flaviviral disease mosquito vector surveillance in Incheon Metropolitan City and the Hwaseong area, Gyeonggi-do, Republic of Korea. Entomol Res 2020; 50: 3-13. https://doi.org/10.1111/1748-5967.12417
  23. World Health Organization. Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes [Internet]; [cited 2020 Mar 4] Available from: http://www.who.int/malaria/publications/atoz/9789241511575/en/.
  24. Foley DH, Klein TA, Lee IY, Kim MS, Wilkerson RC, Harrison G, Rueeda LM, Kim HC. Mosquito species composition and Plasmodium vivax infection rates on Baengyeong-do (Island), Republic of Korea. Korean J Parasitol 2011; 49: 313-316. https://doi.org/10.3347/kjp.2011.49.3.313
  25. Zaim M, Aitio A, Nakashima N. Safety of pyrethroid-treated mosquito nets. Med Vet Entomol 2000; 14: 1-5. https://doi.org/10.1046/j.1365-2915.2000.00211.x
  26. World Wildlife Fund. Hazards and Exposures Associated with DDT and Synthetic Pyrethroids used for Vector Control. Toronto, Canada. World Wildlife Fund; 1999.
  27. Martinez-Torres D, Chevillon C, Brun-Barale A, Berge JB, Pasteur N, Pauron D. Voltage-dependent Na+ channels in pyrethroid-resistant Culex pipiens L. mosquitoes. Pest Manag Sci 1999; 55: 1012-1020. https://doi.org/10.1002/(SICI)1096-9063(199910)55:10<1012::AID-PS39>3.0.CO;2-5
  28. Xu Q, Tain L, Zhang L, Liu N. Sodium channel genes and their differential genotypes at the F-to-F kdr locus in the mosquito Culex quinquefasciatus. Biochem Biophys Res Comm2011; 40: 645-649.
  29. Wang ZM, Li CX, Xing D, Yu YH, Liu N, Xue RD, Dong YD, Zhao TY. Detection and widespread distribution of sodium channel alleles characteristic of insecticide resistance in Culex pipiens complex mosquitoes in China. Med Vet Entomol 2012; 26: 228-232. https://doi.org/10.1111/j.1365-2915.2011.00985.x
  30. Diabate A, Brengues C, Baldet T, Dabire KR, Hougard JM, Akogbeto M, Kengne P, Simard F, Guillet P, Hemingway J, Chandre F. The spread of the Leu-Phe kdr mutation through Anopheles gambiae complex in Burkina Faso: genetic introgression and de novo phenomena. Tropical Med Int Health 2004; 9: 1267-1273. https://doi.org/10.1111/j.1365-3156.2004.01336.x
  31. Scott JG, Yoshimizu M, Kasal S. Pyrethroid resistance in Culex pipiens mosquitoes. Pest Biochem Physiol 2015; 120: 68-76. https://doi.org/10.1016/j.pestbp.2014.12.018
  32. Brooke BD. kdr: can a single mutation produce an entire insecticide resistance phenotype? Trans R Soc Trop Med Hyg 2008; 102: 524-525. https://doi.org/10.1016/j.trstmh.2008.01.001
  33. Rinkevich FD, Du Y, Dong K. Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic Biochem Physiol 2013; 106: 93-100. https://doi.org/10.1016/j.pestbp.2013.02.007
  34. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M. Comparative genomics: insecticide resistance in mosquito vectors. Nature 2003; 423: 136-137.
  35. Sinegre G, Jullian J, Gaven B. Acquisition progressive de la resistance a chlorpyiphos chez les larves de Culex pipiens (L) dans le midi la France. Parasitologia 1977; 19: 1-2.
  36. Tmimi FZ, Faraj C, BkhacheM, Mounaji K, Failloux AB, Sarih M. Insecticide resistance and target site mutations (G119S ace-1 and L1014F kdr) of Culex pipiens in Morocco. Parasit Vectors 2018; 11: 51 https://doi.org/10.1186/s13071-018-2625-y
  37. Chavasse DC, Yop HH. Chemical Methods for the Control of Vectors and Pests of Public Health Importance, Vol. 2. Geneva, Switzerland. World Health Organization. 1997, pp 129.
  38. Yeo IS. U.S. military administration's malaria control activities (1945-1948). Korean J Med Hist 2015; 24: 35-65. https://doi.org/10.13081/kjmh.2015.24.35
  39. Yadouleton A, Badirou K, Agbanrin R, Jost H, Attolou R, Srinivasan R, Padonou G, Akogbeto M. Insecticide resistance status in Culex quinquefasciatus in Benin. Parasit Vectors 2015; 8: 17. https://doi.org/10.1186/s13071-015-0638-3
  40. Antonio-Nkondjio C, Poupardin R, Tene BF, Kopya E, Costantini C, Awono-Ambene P, Wondji CS. Investigation of bendiocarb resistance in Anopheles gambiae populations from the city of Yaounde, Cameroon. Malar J 2016; 15: 424. https://doi.org/10.1186/s12936-016-1483-3