Evaluation of Pyrethroid Susceptibility in Culex pipiens of Northern Izmir Province, Turkey
,
Abstract
Background: Mosquitoes, being a nuisance species, are considered as one of the most important species in public health control programs due to their role as a vector in mosquito-borne diseases observed in humans and animals. We evaluated the susceptibility status of Culex pipiens collected from northern Izmir, Turkey in 2011-16.
Methods: Mosquito larvae, collected from three different locations in northern İzmir, were reared in the laboratory. Adult susceptibility bioassays were performed using the WHO insecticide-impregnated papers including deltamethrin 0.05%, permethrin 0.75%, α-cypermethrin 0.05% and cyfluthrin 0.15%. In addition, adult bioassays were performed after the pre-exposure to piperonyl butoxide (PBO) to determine the contribution of P450 detoxification enzymes to the phenotypic resistance.
Results: In all of the three populations, high levels of resistance were observed (mortalities<63%) to all of the four pyrethroids. Different pyrethroids but with the same mode of action can exhibit significantly different phenotypic resistance in a single population. PBO bioassays also showed that P450 detoxification enzymes can have diverse effects on different pyrethroids.
Conclusion: Using just one chemical in a class of insecticide can be misleading for resistance studies.
1. Tuzun N (2010) Mosquito species and repro-duction areas on the Datca peninsula. [PhD thesis]. Ege University, Izmir (in Turkish).
2. Marquardt WC, Black WC, Freier JE, Hage-dorn H, Moore C, Hemingway J, Higgs S, James A, Kondratieff B (2005) Biology of Disease Vectors. Elsevier, Burlington.
3. Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A (2010) Mos-quitoes and Their Control, 2nd edition. Springer, New York.
4. Nauen R (2007) Insecticide resistance in dis-ease vectors of public health importance. J Med Entomol. 63: 628–633.
5. Rinkevich FD, Du Y, Dong K (2013) Diver-sity and convergence of sodium channel mutations involved in resistance to pyre-throids. Pestic Biochem Physiol. 106: 93–100.
6. Zhu F, Lavine L, O’Neal S, Lavine M, Foss C, Walsh D (2016) Insecticide resistance and management strategies in urban eco-systems. Insects. 7(1): 1–26.
7. Wang ZM, Li CX, Xing D, Yu YH, Liu N, Xue RD, Dong YD, Zhao TY (2012) De-tection and widespread distribution of so-dium channel alleles characteristic of in-secticide resistance in Culex pipiens com-plex mosquitoes in China. Medical and Veterinary Entomology. 26: 228–232.
8. Dong K, Du Y, Rinkevich F, Nomura Y, Xu P, Wang L, Silver K, Zhorov BS (2014) Molecular biology of insect sodium chan-nels and pyrethroid resistance. Insect Bi-ochemistry and Molecular Biology. 50: 1–17.
9. David JP, Ismail HM, Chandor-Proust A, Paine MJI (2013) Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos Trans R Soc Lond B Biol Sci. 368: 20120429.
10. Zhong D, Chang X, Zhou G, He Z, Fu F, Yan Z, Zhu G, Xu T, Bonizzoni M, Wang MH, Cui L, Zheng B, Chen B, Yan G (2013) Relationship between knock-down resistance, metabolic detoxification and organismal resistance to pyrethroids in Anopheles sinensis. PLoS One. 8(2): e55475.
11. Shi L, Hu H, Ma K, Zhou D, Yu J, Zhong D, Fang F, Chang X, Hu S, Zou F, Wang W, Sun Y, Shen B, Zhang D, Ma L, Zhou G, Yan G, Zhu C (2015) De-velopment of resistance to pyrethroid in Culex pipiens pallens population under different insecticide selection pressures. PLoS Negl Trop Dis. 9(8): e0003928.
12. Hemingway J, Small GJ, Monro A, Sawyer BV, Kasap H (1992) Insecticide resistance gene frequencies in Anopheles sacharovi populations of the Cukurova plain, Ada-na Province, Turkey. Med Vet Entomol. 6: 342–348.
13. Kasap H, Kasap M, Alptekin D, Lüleyap Ü, Herath PRJ (2000) Insecticide resistance in Anopheles sacharovi Favre in southern Turkey. Bulletin of the World Health Organization. 78: 687–692.
14. Lüleyap HU, Alptekin D, Kasap H, Kasap M (2002) Detection of knockdown re-sistance mutations in Anopheles sacharovi (Diptera: Culicidae) and genetic distance with Anopheles gambiae (Diptera: Cu-licidae) using cDNA sequencing of the voltage-gated sodium channel gene. J Med Entomol. 39: 870–874.
15. Akiner MM, Simsek FM, Caglar SS (2009) Insecticide resistance of Culex pipiens (Diptera: Culicidae) in Turkey. J Pestic Sci. 34: 259–264.
16. Akiner MM, Caglar SS, Simsek FM (2013) Yearly changes of insecticide susceptibility and possible insecticide resistance mech-anisms of Anopheles maculipennis Meig-
en (Diptera: Culicidae) in Turkey. Acta Trop. 126: 280–285.
17. Akiner MM (2014) Malathion and propoxur resistance in Turkey populations of the Anopheles maculipennis Meigen (Diptera: Culicidae) and relation to the insensitive acetylcholinesterase. Turkiye Parazitol Derg. 38: 111–115 (in Turkish).
18. Taskin BG, Dogaroglu T, Kilic S, Dogac E, Taskin V (2016) Seasonal dynamics of insecticide resistance, multiple resistance, and morphometric variation in field pop-ulations of Culex pipiens. Pestic Biochem Physiol. 129: 14–27.
19. Kioulos I, Kampouraki A, Morou E, Skav-dis G, Vontas J (2014) Insecticide re-sistance status in the major West Nile vec-tor Culex pipiens from Greece. Pest Manag Sci. 70: 623–627.
20. Salim-Abadi Y, Oshaghi MA, Enayati AA, Abai RA, Vatandoost H, Eshraghian MR, Mirhendi H, Hanafi-Bojd AA, Gorouhi MA, Rafi F (2016) High insecticides re-sistance in Culex pipiens (Diptera: Cul-cidae) from Tehran, capital of Iran. J Ar-thropod-Borne Dis. 10(4): 483–492.
21. Fathian M, Vatandoost H, Moosa-Kazemi SH, Raeisi A, Yaghoobi-Ershadi MR, Oshaghi MA, Sedaghat MM (2015) Sus-ceptibility of Culicidae mosquitoes to some insecticides recommended by WHO in a malaria endemic area of southeastern Iran. J Arthropod-Borne Dis. 9(1): 22–34.
22. Ataie A, Moosa-Kazemi SH, Vatandoost H, Yaghoobi-Ershadi MR, Bakhshi H, Anjomruz M (2015) Assessing the sus-ceptibility status of mosquitoes (Diptera: Culicidae) in a dirofilariasis focus, north-western Iran. J Arthropod-Borne Dis. 9 (1): 7–21.
23. Gibb T, Oseto CY (2006) Arthropod col-lection and identification field and la-boratory techniques. Elsevier, Burlington.
24. Merdivenci A (1984) Mosquitoes in Tur-key. Istanbul University Cerrahpaşa Med-ical Faculty Press, Istanbul (in Turkish).
25. Darsie Jr RE, Samanidou-Voyadjoglou A (1997) Keys for the identification of the mosquitoes of Greece. Journal of the Amer-ican Mosquito Control Association. 13: 247–254.
26. Darsie Jr RE, Ward RA (2005) Identifica-tion and Geographical Distribution of the Mosquitoes of North America, North Mex-ico. University Press of Florida, Florida.
27. Cutwa MM, O’Meara GF (2017) Photo-graphic guide to common mosquitoes of Florida. Available at: http://www.gamosquito.org/resources/IDatlas.pdf (accessed 15 August 2017).
28. WHO (2016) Test Procedures for Insecti-cide Resistance Monitoring in Malaria Vector Mosquitoes. WHO Library Cata-loguing-in-Publication Data, Geneva.
29. Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM (2002) The role of agricul-tural use of incesticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. The American Society of Tropical Medicine and Hygiene. 67: 617–622.
30. Yoo DH, Shin EH, Lee DK, Ahn YJ, Chang KS, Kim HK, Kim SY, Park C (2013) In-secticide susceptibility of field-collected populations of Culex tritaeniorhynchus in the Republic of Korea. J Insect Sci. 13: 2.
31. Kudom AA, Mensah BA, Froeschl G, Rinder H (2015) DDT and pyrethroid resistance status and laboratory evaluation of bio-efficacy of long lasting insecticide treated nets against Culex quinquefasciatus and Culex decens in Ghana. Acta Trop. 150: 122–130.
32. Weerasinghe IS, Kasai S, Shono T (2001) Correlation of pyrethroid structure and resistance level in Culex quinquefasciatus say from Saudi Arabia. J Pesticide Sci. 26: 158–161.
33. Burton MJ, Mellor IR, Duce IR, Davies TGE, Field LM, Williamson MS (2011)
Differential resistance of insect sodium channels with kdr mutations to deltame-thrin, permethrin and DDT. Insect Bio-chem Mol Biol. 41: 723–732.
34. Scott JG, Yoshimizu MH, Kasai S (2015) Pyrethroid resistance in Culex pipiens mos-quitoes. Pestic Biochem Physiol. 120: 68–76.
35. Selvi S, Edah MA, Nazni WA, Lee HL, Azahari AH (2007) Characterization on malathion and permethrin resistance by bioassays and the variation of esterase activity with the life stages of the mos-quito Culex quinquefasciatus. Tropical Biomedicine. 24: 63–75.
36. 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. Medical and Veteri-nary Entomology. 27: 156–164.
37. Allossogbe M, Gnanguenon V, Yovogan B, Akinro B, Anagonou R, Agossa F, Houtoukpe A, Padonou GG, Akogbeto M (2017) WHO cone bio-assays of classical and new-generation long-lasting insecti-cidal nets call for innovative insecticides targeting the knock-down resistance mech-anism in Benin. Malar J. 16(1): 77.
38. Rakotoson JD, Fornadel CM, Belemvire A, Norris LC, George K, Caranci A, Lucas B, Dengala D (2017) Insecticide resistance status of three malaria vectors, Anopheles gambiae (s.l.), An. funestus and An. mascarensis, from the south, central and east coasts of Madagascar. Parasites and Vectors. 10(1): 396.
39. McAbee RD, Kang KD, Stanich MA, Christiansen JA, Wheelock CE, Inman AD, Hammock BD, Cornel AJ (2003) yrethroid tolerance in Culex pipiens pipiens var molestus from Marin Coun-ty, California. Pest Manag Sci. 60: 359–368.
2. Marquardt WC, Black WC, Freier JE, Hage-dorn H, Moore C, Hemingway J, Higgs S, James A, Kondratieff B (2005) Biology of Disease Vectors. Elsevier, Burlington.
3. Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A (2010) Mos-quitoes and Their Control, 2nd edition. Springer, New York.
4. Nauen R (2007) Insecticide resistance in dis-ease vectors of public health importance. J Med Entomol. 63: 628–633.
5. Rinkevich FD, Du Y, Dong K (2013) Diver-sity and convergence of sodium channel mutations involved in resistance to pyre-throids. Pestic Biochem Physiol. 106: 93–100.
6. Zhu F, Lavine L, O’Neal S, Lavine M, Foss C, Walsh D (2016) Insecticide resistance and management strategies in urban eco-systems. Insects. 7(1): 1–26.
7. Wang ZM, Li CX, Xing D, Yu YH, Liu N, Xue RD, Dong YD, Zhao TY (2012) De-tection and widespread distribution of so-dium channel alleles characteristic of in-secticide resistance in Culex pipiens com-plex mosquitoes in China. Medical and Veterinary Entomology. 26: 228–232.
8. Dong K, Du Y, Rinkevich F, Nomura Y, Xu P, Wang L, Silver K, Zhorov BS (2014) Molecular biology of insect sodium chan-nels and pyrethroid resistance. Insect Bi-ochemistry and Molecular Biology. 50: 1–17.
9. David JP, Ismail HM, Chandor-Proust A, Paine MJI (2013) Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos Trans R Soc Lond B Biol Sci. 368: 20120429.
10. Zhong D, Chang X, Zhou G, He Z, Fu F, Yan Z, Zhu G, Xu T, Bonizzoni M, Wang MH, Cui L, Zheng B, Chen B, Yan G (2013) Relationship between knock-down resistance, metabolic detoxification and organismal resistance to pyrethroids in Anopheles sinensis. PLoS One. 8(2): e55475.
11. Shi L, Hu H, Ma K, Zhou D, Yu J, Zhong D, Fang F, Chang X, Hu S, Zou F, Wang W, Sun Y, Shen B, Zhang D, Ma L, Zhou G, Yan G, Zhu C (2015) De-velopment of resistance to pyrethroid in Culex pipiens pallens population under different insecticide selection pressures. PLoS Negl Trop Dis. 9(8): e0003928.
12. Hemingway J, Small GJ, Monro A, Sawyer BV, Kasap H (1992) Insecticide resistance gene frequencies in Anopheles sacharovi populations of the Cukurova plain, Ada-na Province, Turkey. Med Vet Entomol. 6: 342–348.
13. Kasap H, Kasap M, Alptekin D, Lüleyap Ü, Herath PRJ (2000) Insecticide resistance in Anopheles sacharovi Favre in southern Turkey. Bulletin of the World Health Organization. 78: 687–692.
14. Lüleyap HU, Alptekin D, Kasap H, Kasap M (2002) Detection of knockdown re-sistance mutations in Anopheles sacharovi (Diptera: Culicidae) and genetic distance with Anopheles gambiae (Diptera: Cu-licidae) using cDNA sequencing of the voltage-gated sodium channel gene. J Med Entomol. 39: 870–874.
15. Akiner MM, Simsek FM, Caglar SS (2009) Insecticide resistance of Culex pipiens (Diptera: Culicidae) in Turkey. J Pestic Sci. 34: 259–264.
16. Akiner MM, Caglar SS, Simsek FM (2013) Yearly changes of insecticide susceptibility and possible insecticide resistance mech-anisms of Anopheles maculipennis Meig-
en (Diptera: Culicidae) in Turkey. Acta Trop. 126: 280–285.
17. Akiner MM (2014) Malathion and propoxur resistance in Turkey populations of the Anopheles maculipennis Meigen (Diptera: Culicidae) and relation to the insensitive acetylcholinesterase. Turkiye Parazitol Derg. 38: 111–115 (in Turkish).
18. Taskin BG, Dogaroglu T, Kilic S, Dogac E, Taskin V (2016) Seasonal dynamics of insecticide resistance, multiple resistance, and morphometric variation in field pop-ulations of Culex pipiens. Pestic Biochem Physiol. 129: 14–27.
19. Kioulos I, Kampouraki A, Morou E, Skav-dis G, Vontas J (2014) Insecticide re-sistance status in the major West Nile vec-tor Culex pipiens from Greece. Pest Manag Sci. 70: 623–627.
20. Salim-Abadi Y, Oshaghi MA, Enayati AA, Abai RA, Vatandoost H, Eshraghian MR, Mirhendi H, Hanafi-Bojd AA, Gorouhi MA, Rafi F (2016) High insecticides re-sistance in Culex pipiens (Diptera: Cul-cidae) from Tehran, capital of Iran. J Ar-thropod-Borne Dis. 10(4): 483–492.
21. Fathian M, Vatandoost H, Moosa-Kazemi SH, Raeisi A, Yaghoobi-Ershadi MR, Oshaghi MA, Sedaghat MM (2015) Sus-ceptibility of Culicidae mosquitoes to some insecticides recommended by WHO in a malaria endemic area of southeastern Iran. J Arthropod-Borne Dis. 9(1): 22–34.
22. Ataie A, Moosa-Kazemi SH, Vatandoost H, Yaghoobi-Ershadi MR, Bakhshi H, Anjomruz M (2015) Assessing the sus-ceptibility status of mosquitoes (Diptera: Culicidae) in a dirofilariasis focus, north-western Iran. J Arthropod-Borne Dis. 9 (1): 7–21.
23. Gibb T, Oseto CY (2006) Arthropod col-lection and identification field and la-boratory techniques. Elsevier, Burlington.
24. Merdivenci A (1984) Mosquitoes in Tur-key. Istanbul University Cerrahpaşa Med-ical Faculty Press, Istanbul (in Turkish).
25. Darsie Jr RE, Samanidou-Voyadjoglou A (1997) Keys for the identification of the mosquitoes of Greece. Journal of the Amer-ican Mosquito Control Association. 13: 247–254.
26. Darsie Jr RE, Ward RA (2005) Identifica-tion and Geographical Distribution of the Mosquitoes of North America, North Mex-ico. University Press of Florida, Florida.
27. Cutwa MM, O’Meara GF (2017) Photo-graphic guide to common mosquitoes of Florida. Available at: http://www.gamosquito.org/resources/IDatlas.pdf (accessed 15 August 2017).
28. WHO (2016) Test Procedures for Insecti-cide Resistance Monitoring in Malaria Vector Mosquitoes. WHO Library Cata-loguing-in-Publication Data, Geneva.
29. Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM (2002) The role of agricul-tural use of incesticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. The American Society of Tropical Medicine and Hygiene. 67: 617–622.
30. Yoo DH, Shin EH, Lee DK, Ahn YJ, Chang KS, Kim HK, Kim SY, Park C (2013) In-secticide susceptibility of field-collected populations of Culex tritaeniorhynchus in the Republic of Korea. J Insect Sci. 13: 2.
31. Kudom AA, Mensah BA, Froeschl G, Rinder H (2015) DDT and pyrethroid resistance status and laboratory evaluation of bio-efficacy of long lasting insecticide treated nets against Culex quinquefasciatus and Culex decens in Ghana. Acta Trop. 150: 122–130.
32. Weerasinghe IS, Kasai S, Shono T (2001) Correlation of pyrethroid structure and resistance level in Culex quinquefasciatus say from Saudi Arabia. J Pesticide Sci. 26: 158–161.
33. Burton MJ, Mellor IR, Duce IR, Davies TGE, Field LM, Williamson MS (2011)
Differential resistance of insect sodium channels with kdr mutations to deltame-thrin, permethrin and DDT. Insect Bio-chem Mol Biol. 41: 723–732.
34. Scott JG, Yoshimizu MH, Kasai S (2015) Pyrethroid resistance in Culex pipiens mos-quitoes. Pestic Biochem Physiol. 120: 68–76.
35. Selvi S, Edah MA, Nazni WA, Lee HL, Azahari AH (2007) Characterization on malathion and permethrin resistance by bioassays and the variation of esterase activity with the life stages of the mos-quito Culex quinquefasciatus. Tropical Biomedicine. 24: 63–75.
36. 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. Medical and Veteri-nary Entomology. 27: 156–164.
37. Allossogbe M, Gnanguenon V, Yovogan B, Akinro B, Anagonou R, Agossa F, Houtoukpe A, Padonou GG, Akogbeto M (2017) WHO cone bio-assays of classical and new-generation long-lasting insecti-cidal nets call for innovative insecticides targeting the knock-down resistance mech-anism in Benin. Malar J. 16(1): 77.
38. Rakotoson JD, Fornadel CM, Belemvire A, Norris LC, George K, Caranci A, Lucas B, Dengala D (2017) Insecticide resistance status of three malaria vectors, Anopheles gambiae (s.l.), An. funestus and An. mascarensis, from the south, central and east coasts of Madagascar. Parasites and Vectors. 10(1): 396.
39. McAbee RD, Kang KD, Stanich MA, Christiansen JA, Wheelock CE, Inman AD, Hammock BD, Cornel AJ (2003) yrethroid tolerance in Culex pipiens pipiens var molestus from Marin Coun-ty, California. Pest Manag Sci. 60: 359–368.
| Files | ||
| Issue | Vol 12 No 4 (2018) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v12i4.355 | |
| Keywords | ||
| Bioassay Insecticide resistance Pyrethroids PBO Culex pipiens | ||
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How to Cite
1.
Guntay O, Yikilmaz MS, Ozaydin H, Izzetoglu S, Suner A. Evaluation of Pyrethroid Susceptibility in Culex pipiens of Northern Izmir Province, Turkey. J Arthropod Borne Dis. 2018;12(4):370-377.
