Insecticide Resistance and Mechanisms of Culex pipiens Populations in the Mediterranean and Aegean Regions of Turkey During 2017–2018
,
Abstract
Background: Culex pipiens has a significant public health importance since it is an important vector of West Nile virus and Rift Valley fever virus. We, therefore, aimed to determine the insecticide resistance level in Cx. pipiens populations in the Aegean and Mediterranean regions of Turkey.
Methods: Bioassays have been carried out against Dichlorodiphenyltrichloroethane (DDT) (4%), Malathion (5%), Fenitrothion (1%), Propoxur (0.1%), Bendiocarb (0.1%), Permethrin (0.75%) and Deltamethrin (0.05%). Biochemical analyses have been performed to detect non-specific esterase, mixed function oxidase, glutathione-s-transferase and acetylcholinesterase levels. A knockdown resistance (kdr) (L1014F) and Acetylcholinesterase (Ace-1) (G119S) mutations have been detected by using allele-specific primers and a polymerase chain reaction (PCR) amplification of specific alleles (PASA) diagnostic test was performed for detection of F290V mutation.
Results: Bioassay results showed that all Cx. pipiens populations were resistant to DDT, Malathion, Fenitrothion, Bendiocarb, Propoxur and some of the populations have started to gain Permethrin and Deltamethrin resistance. Biochemical analyses results revealed that altered glutathione-s-transferases, P450 monooxygenases, esterase levels might be responsible for DDT, organophosphate, carbamate and pyrethroid resistance in Cx. pipiens populations. Results showed mild to high frequency of L1014F, low frequency of F290V but no Ace-1 G119S mutation within the populations. Additionally, acetylcholinesterase insensitivity was not significantly high within the most of these populations.
Conclusion: Overall results may help to fulfil the lacking information in the literature regarding insecticide resistance status and underlying mechanism of Culex pipiens populations of the Mediterranean and Aegean region of Turkey by using all bioassays, molecular tests and biochemical assays.
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2. Caraballo H (2014). Emergency Department Management of Mosquito-Borne Illness: Malaria, Dengue, and West Nile Virus. Emerg Med Pract. 16(5):1
3. World Health Organization (WHO) (2012). Global Plan for Insecticide Resistance Management in Malaria Vectors (GPIRM); WHO, Geneva, Switzerland.
4. Hemingway J (2014). The role of vector control in stopping the transmission of malaria: Threats and opportunities. Philos Trans R Soc Lond B Biol Sci. 369 (1645):20130431.
5. Brugman VA, Hernández-Triana LM, Medlock JM, Fooks AR, Carpenter S, Johnson N (2018). The role of culex pipiens L. (Diptera: Culicidae) in virüs transmission in Europe. Int J Environ Res Public Health.15(2): 389-397.
6. European Centre for Disease Prevention and Control (2019). West Nile virus infection. In: ECDC. Annual epidemiological report for 2018. Stockholm: ECDC.
7. Özkul A, Ergunay K, Koysuren A, Alkan F, Arsava EM, Tezcan S (2013). Concurrent occurrence of human and equine West Nile virus infections in Central Anatolia, Turkey: the first evidence for circulation of lineage 1 viruses. Int J Infect Dis. 17: 546–51.
8. Kalaycioglu H, Korukluoglu G, Ozkul A, Oncul O, Tosun S, Karabay O (2012). Emergence of West Nile virus infections in humans in Turkey, 2010 to 2011. Euro Surveill. 17(21):20182.
9. Denholm I, Rowlan MW (1992). Tactics for managing pesticide resistance in arthropods: Theory and practice. Annu Rev Entomol. 37: 91–112.
10. Akıner MM, Şimşek FM, Çağlar SS (2009). Insecticide resistance of Culex pipiens (Diptera: Culicidae) in Turkey. J. Pestic. Sci. 34(4): 259–264.
11. Akıner MM, Ekşi E (2015). Evaluation of insecticide resistance and biochemical mechanisms of Culex pipiens L. in four localities of east and middle mediterranean basin in Turkey. Int J Mosq Res. 2(3): 39-44.
12. Taşkın GB, Dogaroglu T, Kilic S, Doğaç E, Taskin V (2015). Pesticide Biochemistry and Physiology, Seasonal dynamics of insecticide resistance, multiple resistance, and morphometric variation in field populations of Culex pipiens. Pesti Biochem Phsiol. 129:14-27.
13. Guz N, Çağatay NS, Fotakis EA, Durmuşoğlu E, Vontas J (2020). Detection of diflubenzuron and pyrethroid resistance mutations in Culex pipiens from Muğla, Turkey. Acta Trop. 203:105294.
14. Alten SB, Çağlar SS. Vektör Ekolojisi ve Mücadelesi: Sıtma Vektörünün Biyo-Ekolojisi Mücadele Organizasyonu ve Yöntemleri. TC Sağlık Bakanlığı Sıtma Savaş Daire Başkanlığı ve Sağlık Projesi Genel Koordinatörlüğü Bizim Büro Basımevi 1998; pp. 242, Ankara.
15. Becker N, Petric D, Zgomba M, Boase C, Dahl C, Lane J, Kaiser A (2003). Mosquitoes and Their Control, Kluwer academic & Plenum publishers, New York.
16. WHO (World Health Organization) (1998). Techniques to detect insecticide resistance mechanisms (field and laboratory manual). WHO/CDS/CPC/MAL/98.6 WHO Department of Disease Prevention & Control WHO communicable diseases; Geneva, 35 p.
17. World Health Organization (2016). Test procedures for insecticide resistance monitoring in malaria vector mosquitoes – 2nd edition, Geneva.
18. Bradford MM (1976). A Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72: 248-254.
19. Brogdon WG, McAllister JC, Vulule J (1997). Haem peroxidase activity in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. J Am Mosq Control Assoc.13(3):233-237.
20. Martinez-Torres D, Chevillon C, Brun-Barale A, Berge JB, Pasteur N, Pauron D (1999). Voltage-dependent Na+ channels in pyrethroid- resistant Culex pipiens L mosquitoes. Pestic. Sci.55:1012–1020.
21. Weill M, Fort P, Berthomieu A, Dubois MP, Pasteur N, Raymond M (2002). A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and in non-homologous to the ace gene in Drosophila. Proc. Biol. Sci. 269: 2007–2016.
22. Rodriguez MM, Bisset CA, Fernandez J (2007). Levels of insecticide resistance and resistance mechanisms in Aedes aegypti from some Latin American countries. J. Am. Mosq. Cont. Assoc. 23:420-429.
23. Ocampo CB, Saalazar-Terreros MJ, Mina NJ, McAllister J, Brogdon WG (2011). Insecticide resistance status of Aedes aegypti in 10 localities in Colombia. Acta Trop 118: 37-44.
24. Akıner MM, Çaglar SS, Şimsek FM (2013). Yearly changes of insecticide susceptiblity and possible insecticide resistance mechanisms of Anopheles maculipennis Meigen (Diptera: Culicidae) in Turkey. Acta Trop. 126: 280-285.
25. Yavasoglu SI, Yaylagul, OE, Akıner M, Ulger C, Caglar SS, Simsek FM (2019). Current insecticide resistance status in Anopheles sacharovi and Anopheles superpictus populations in former malaria endemic areas of Turkey. Acta Trop.193: 148-157.
26. Hemingway J, Ranson H (2000). Insecticide resistance in insect vector of human disease. Annu. Rev. Entomol. 45:375–391.
27. Chiu TL, Wen Z, Rupasinghe SG, Schuler MA (2008). Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc. Natl. Acad. Sci.105 (26): 8855-8860.
28. Fotakis EA, Chaskopou- lou A, Grigoraki L,Tsiaman- tas A, Kounadi S, Georgiou L, VontasJ (2017) Analysis of population structure and insecticide resistance in mosquitoes of the genus Culex, Anopheles and Aedes from different environments of Greece with a history of mosquito borne disease transmission. Acta Trop. 174:29-37.
29. Tmimi F, Faraj C, Bkhache M, Mounaji K, Failloux A, Sarih M(2018) Insecticide resis- tance and target site mutations (G119S ace-1 and L1014F kdr) of Culex pipiens in Morocco. Parasit Vectors.11(1):51.
30. Xu Q, Wang H, Zhang L, Liu N(2016) Kdr allelic variation in pyrethroid re- sistant mosquitoes, Culex quinquefasciatus (S.). Biochem Biophys Res Commun. 345(2):774-80.
31. Johnson BJ, Fonseca DM(2016) Insec- ticide resistance alleles in wetland and residential populations of the West Nile virus vector Culex pipiens in NewJersey. Pest Manag Sci. 72(3):481-8.
32. Wang ZM, Li CX, Xing D, Yu YH, Liu N, Xue RD, Dong YD, Zhao TY(2012) Detection and widespread distribution of sodium channel alleles characteristic of insecticide resistance in Culex pipiens complex mosquitoes in China. Med Vet
Entomol. 26(2):228-32.
33. Ramsdale CD, Herath PR, Davidson G (1980)Recent developments of insecticide resistance in some Turkish Anophelines. J Trop Med Hyg.83(1):11-9.
34. Kasap H, Kasap M, Alptekin D, Lüleyap U,Herath P R (2000) Insecticide resistance in Anopheles sacharovi Favre in southern Turkey.Bull World Health Organ. 78(5):687-92.
35. Kioulos I, Kampouraki A, Morou E, Skavdis G,Vontas J(2014) Insecticide resistance status in the major West Nile virus vector Culex pipiens fromGreece. Pest Manag Sci. 70(4):623-7.
36. Sorokin N N, Zharov A A (1992) Insecticide resistance and irritability of Culex pipiens in Moscow.Med Parazitol (Mosk). (3):35-8.
37. Rahimi S, Vatandoost H, Abai MR, Raeisi A,Hana- fi-Bojd AA(2019) Status of resistant and knockdown of West Nile vector, Culex pipiens complex to different pesticides in Iran. J Arthropod Borne Dis. 13(3):284-296.
38. Berticat C, Boquien G, Ray- mond M, Chevillon C(2002) Insecticide re- sistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genet Res. 79(1):41-7.
39. Berticat C, Duron O, Heyse D, Raymond M (2004) Insecticide resistance genes confer a predation cost on mosquitoes, Culex pipiens. Genet Res. 83(3):189-96.
40. Bourguet D, Guillemaud T, Chevillon C, Raymond M(2004) Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens. Evolution. 58(1):128-35.
41. Gazave E, Chevillon C, Lenormand T, Mar- quine M, Raymond M (2001) Dissecting the cost of insecticide resistance genes during the overwintering period of the mosquito Culex pipiens. Heredity (Edinb). 87(Pt 4):441-8.
42. Labbé P, Berthomieu A, Ber- ticat C,Alout H, Raymond M, Lenormand T, Weill M(2007) Independent duplications of the acetylcholinesterase gene con- ferring insecticide resistance in the mosquito Cu lex pipiens. Mol Biol Evol. 24(4):1056-67.
43. Labbé P, Berticat C, Berth- omieu A, Unal S, Bernard C, Weill M, Lenormand T(2007) Forty years of erratic insecticide resistance evolution in the mosquito Culex pipiens. PLoS Genet. 3(11):e205.
44. Bkhache M, Tmimi F, Charafeddine O, Fila- li OB, Lemrani M, Labbé P, Sarih M(2019) G119S ace-1 mutation conferring in- secticide resistance detected in the Culex pipiens complex in Morocco. Pest Manag Sci. 75(1):286- 291.
2. Caraballo H (2014). Emergency Department Management of Mosquito-Borne Illness: Malaria, Dengue, and West Nile Virus. Emerg Med Pract. 16(5):1
3. World Health Organization (WHO) (2012). Global Plan for Insecticide Resistance Management in Malaria Vectors (GPIRM); WHO, Geneva, Switzerland.
4. Hemingway J (2014). The role of vector control in stopping the transmission of malaria: Threats and opportunities. Philos Trans R Soc Lond B Biol Sci. 369 (1645):20130431.
5. Brugman VA, Hernández-Triana LM, Medlock JM, Fooks AR, Carpenter S, Johnson N (2018). The role of culex pipiens L. (Diptera: Culicidae) in virüs transmission in Europe. Int J Environ Res Public Health.15(2): 389-397.
6. European Centre for Disease Prevention and Control (2019). West Nile virus infection. In: ECDC. Annual epidemiological report for 2018. Stockholm: ECDC.
7. Özkul A, Ergunay K, Koysuren A, Alkan F, Arsava EM, Tezcan S (2013). Concurrent occurrence of human and equine West Nile virus infections in Central Anatolia, Turkey: the first evidence for circulation of lineage 1 viruses. Int J Infect Dis. 17: 546–51.
8. Kalaycioglu H, Korukluoglu G, Ozkul A, Oncul O, Tosun S, Karabay O (2012). Emergence of West Nile virus infections in humans in Turkey, 2010 to 2011. Euro Surveill. 17(21):20182.
9. Denholm I, Rowlan MW (1992). Tactics for managing pesticide resistance in arthropods: Theory and practice. Annu Rev Entomol. 37: 91–112.
10. Akıner MM, Şimşek FM, Çağlar SS (2009). Insecticide resistance of Culex pipiens (Diptera: Culicidae) in Turkey. J. Pestic. Sci. 34(4): 259–264.
11. Akıner MM, Ekşi E (2015). Evaluation of insecticide resistance and biochemical mechanisms of Culex pipiens L. in four localities of east and middle mediterranean basin in Turkey. Int J Mosq Res. 2(3): 39-44.
12. Taşkın GB, Dogaroglu T, Kilic S, Doğaç E, Taskin V (2015). Pesticide Biochemistry and Physiology, Seasonal dynamics of insecticide resistance, multiple resistance, and morphometric variation in field populations of Culex pipiens. Pesti Biochem Phsiol. 129:14-27.
13. Guz N, Çağatay NS, Fotakis EA, Durmuşoğlu E, Vontas J (2020). Detection of diflubenzuron and pyrethroid resistance mutations in Culex pipiens from Muğla, Turkey. Acta Trop. 203:105294.
14. Alten SB, Çağlar SS. Vektör Ekolojisi ve Mücadelesi: Sıtma Vektörünün Biyo-Ekolojisi Mücadele Organizasyonu ve Yöntemleri. TC Sağlık Bakanlığı Sıtma Savaş Daire Başkanlığı ve Sağlık Projesi Genel Koordinatörlüğü Bizim Büro Basımevi 1998; pp. 242, Ankara.
15. Becker N, Petric D, Zgomba M, Boase C, Dahl C, Lane J, Kaiser A (2003). Mosquitoes and Their Control, Kluwer academic & Plenum publishers, New York.
16. WHO (World Health Organization) (1998). Techniques to detect insecticide resistance mechanisms (field and laboratory manual). WHO/CDS/CPC/MAL/98.6 WHO Department of Disease Prevention & Control WHO communicable diseases; Geneva, 35 p.
17. World Health Organization (2016). Test procedures for insecticide resistance monitoring in malaria vector mosquitoes – 2nd edition, Geneva.
18. Bradford MM (1976). A Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72: 248-254.
19. Brogdon WG, McAllister JC, Vulule J (1997). Haem peroxidase activity in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. J Am Mosq Control Assoc.13(3):233-237.
20. Martinez-Torres D, Chevillon C, Brun-Barale A, Berge JB, Pasteur N, Pauron D (1999). Voltage-dependent Na+ channels in pyrethroid- resistant Culex pipiens L mosquitoes. Pestic. Sci.55:1012–1020.
21. Weill M, Fort P, Berthomieu A, Dubois MP, Pasteur N, Raymond M (2002). A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and in non-homologous to the ace gene in Drosophila. Proc. Biol. Sci. 269: 2007–2016.
22. Rodriguez MM, Bisset CA, Fernandez J (2007). Levels of insecticide resistance and resistance mechanisms in Aedes aegypti from some Latin American countries. J. Am. Mosq. Cont. Assoc. 23:420-429.
23. Ocampo CB, Saalazar-Terreros MJ, Mina NJ, McAllister J, Brogdon WG (2011). Insecticide resistance status of Aedes aegypti in 10 localities in Colombia. Acta Trop 118: 37-44.
24. Akıner MM, Çaglar SS, Şimsek FM (2013). Yearly changes of insecticide susceptiblity and possible insecticide resistance mechanisms of Anopheles maculipennis Meigen (Diptera: Culicidae) in Turkey. Acta Trop. 126: 280-285.
25. Yavasoglu SI, Yaylagul, OE, Akıner M, Ulger C, Caglar SS, Simsek FM (2019). Current insecticide resistance status in Anopheles sacharovi and Anopheles superpictus populations in former malaria endemic areas of Turkey. Acta Trop.193: 148-157.
26. Hemingway J, Ranson H (2000). Insecticide resistance in insect vector of human disease. Annu. Rev. Entomol. 45:375–391.
27. Chiu TL, Wen Z, Rupasinghe SG, Schuler MA (2008). Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc. Natl. Acad. Sci.105 (26): 8855-8860.
28. Fotakis EA, Chaskopou- lou A, Grigoraki L,Tsiaman- tas A, Kounadi S, Georgiou L, VontasJ (2017) Analysis of population structure and insecticide resistance in mosquitoes of the genus Culex, Anopheles and Aedes from different environments of Greece with a history of mosquito borne disease transmission. Acta Trop. 174:29-37.
29. Tmimi F, Faraj C, Bkhache M, Mounaji K, Failloux A, Sarih M(2018) Insecticide resis- tance and target site mutations (G119S ace-1 and L1014F kdr) of Culex pipiens in Morocco. Parasit Vectors.11(1):51.
30. Xu Q, Wang H, Zhang L, Liu N(2016) Kdr allelic variation in pyrethroid re- sistant mosquitoes, Culex quinquefasciatus (S.). Biochem Biophys Res Commun. 345(2):774-80.
31. Johnson BJ, Fonseca DM(2016) Insec- ticide resistance alleles in wetland and residential populations of the West Nile virus vector Culex pipiens in NewJersey. Pest Manag Sci. 72(3):481-8.
32. Wang ZM, Li CX, Xing D, Yu YH, Liu N, Xue RD, Dong YD, Zhao TY(2012) Detection and widespread distribution of sodium channel alleles characteristic of insecticide resistance in Culex pipiens complex mosquitoes in China. Med Vet
Entomol. 26(2):228-32.
33. Ramsdale CD, Herath PR, Davidson G (1980)Recent developments of insecticide resistance in some Turkish Anophelines. J Trop Med Hyg.83(1):11-9.
34. Kasap H, Kasap M, Alptekin D, Lüleyap U,Herath P R (2000) Insecticide resistance in Anopheles sacharovi Favre in southern Turkey.Bull World Health Organ. 78(5):687-92.
35. Kioulos I, Kampouraki A, Morou E, Skavdis G,Vontas J(2014) Insecticide resistance status in the major West Nile virus vector Culex pipiens fromGreece. Pest Manag Sci. 70(4):623-7.
36. Sorokin N N, Zharov A A (1992) Insecticide resistance and irritability of Culex pipiens in Moscow.Med Parazitol (Mosk). (3):35-8.
37. Rahimi S, Vatandoost H, Abai MR, Raeisi A,Hana- fi-Bojd AA(2019) Status of resistant and knockdown of West Nile vector, Culex pipiens complex to different pesticides in Iran. J Arthropod Borne Dis. 13(3):284-296.
38. Berticat C, Boquien G, Ray- mond M, Chevillon C(2002) Insecticide re- sistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genet Res. 79(1):41-7.
39. Berticat C, Duron O, Heyse D, Raymond M (2004) Insecticide resistance genes confer a predation cost on mosquitoes, Culex pipiens. Genet Res. 83(3):189-96.
40. Bourguet D, Guillemaud T, Chevillon C, Raymond M(2004) Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens. Evolution. 58(1):128-35.
41. Gazave E, Chevillon C, Lenormand T, Mar- quine M, Raymond M (2001) Dissecting the cost of insecticide resistance genes during the overwintering period of the mosquito Culex pipiens. Heredity (Edinb). 87(Pt 4):441-8.
42. Labbé P, Berthomieu A, Ber- ticat C,Alout H, Raymond M, Lenormand T, Weill M(2007) Independent duplications of the acetylcholinesterase gene con- ferring insecticide resistance in the mosquito Cu lex pipiens. Mol Biol Evol. 24(4):1056-67.
43. Labbé P, Berticat C, Berth- omieu A, Unal S, Bernard C, Weill M, Lenormand T(2007) Forty years of erratic insecticide resistance evolution in the mosquito Culex pipiens. PLoS Genet. 3(11):e205.
44. Bkhache M, Tmimi F, Charafeddine O, Fila- li OB, Lemrani M, Labbé P, Sarih M(2019) G119S ace-1 mutation conferring in- secticide resistance detected in the Culex pipiens complex in Morocco. Pest Manag Sci. 75(1):286- 291.
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| Issue | Vol 15 No 4 (2021) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v15i4.10505 | |
| Keywords | ||
| Kdr Acetylcholinesterase Monooxygenase Glutathione S-Transferase | ||
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How to Cite
1.
Yavaşoğlu S, Şimşek F. Insecticide Resistance and Mechanisms of Culex pipiens Populations in the Mediterranean and Aegean Regions of Turkey During 2017–2018. J Arthropod Borne Dis. 2022;15(4):405-420.
