Biochemical Basis of Cyfluthrin and DDT Resistance in Anopheles stephensi (Diptera: Culicidae) in Malarious Area of Iran
-
Mohammad Amin Gorouhi
,
Mohammad Ali Oshaghi
,
Hassan Vatandoost
,
Ahmad Ali Enayati
,
Mohamad Reza Abai
,
Mohsen Karami
,
Yaser Salim-Abadi
,
Ahmad Ali Hanafi-Bojd
,
Abbas Aghaei-Afshar
,
Azim Paksa
,
Fatemeh Nikpoor
Abstract
Background: Anopheles stephensi is a key urban malaria vector in the Indian subcontinent and Middle East including south and southeast of Iran. Wide application of insecticides resulted in resistance of this species to various insecticides in these regions. This study was conducted to reveal the role of metabolic mechanisms in the development of resistance in An. stephensi to DDT and cyfluthrin.
Methods: Field mosquito specimens were collected from Chabahar Seaport, southeast corner of Iran, in 2015. Insecticide susceptibility and enzyme assays were conducted as recommended by WHO.
Results: Mean enzyme ratios were 3.95 and 3.04 for α- esterases and 2.40 and 1.97 for β- esterases in the DDT and cyfluthrin- resistant populations correspondingly compared with the susceptible strain. The GSTs enzyme mean activity ratios were 5.07 and 2.55 in the DDT and cyfluthrin- resistant populations compared with the susceptible beech strain. The cytochrome p450s enzyme ratios were 1.11 and 1.28 in the DDT and cyfluthrin- resistant populations respectively compared with the susceptible beech strain.
Conclusion: Metabolic mechanisms play a crucial role in the development of DDT and cyfluthrin resistance in An. stephensi, therefore, further evaluation of the mechanisms involved as well as implementation of proper insecticide resistance management strategies are recommended.
1. Norouzinejad F, Ghaffari F, Raeisi A (2016) Epidemiological status of ma¬laria in Iran, 2011–2014. Asian Pac J Trop Dis. 9: 1055−1061.
2. Azari-Hamidian S (2011) Larval habitat characteristics of the genus Anopheles (Diptera: Culicidae) and a checklist of mosquitoes in Guilan Province, north-ern Iran. Iran J Arthropod Borne Dis. 5 (1): 37−53.
3. Mehravaran A, Oshaghi M, Vatandoost H, Abai M, Ebrahimzadeh A, Roodi AM, Grouhi A (2011) First report on Anoph¬eles fluviatilis U in southeastern Iran. Acta Trop. 117: 76−81.
4. Naddaf Dezfouli S, Oshaghi M, Vatan-doost H, Assmar M (2003) rDNA-ITS2 based species-diagnostic polymerase chain reaction assay for identification of sibling species of anopheles fluviatilis in Iran. Southeast Asian J Trop Med Public Health. 34: 56−60.
5. Vatandoost H, Oshaghi M, Abaie M, Shahi M, Yaaghoobi F, Baghaii M, Hanafi-Bojd AA, Zamani G, Townson H (2006) Bionomics of Anopheles stephensi Liston in the malarious area of Hor¬mozgan Province, southern Iran, 2002. Acta Trop. 97: 196−203.
6. Karimian F, Oshaghi MA, Sedaghat MM, Waterhouse RM, Vatandoost H, Hanafi-Bojd AA, Ravasan NM, Chavshin AR (2014) Phylogenetic analysis of the ori¬ental-palearctic-afrotropical members of anopheles (Culicidae: Diptera) based on nuclear rDNA and mitochondrial DNA charac¬teristics. Jpn J Infect Dis. 67: 361−367.
7. Oshaghi M, Shemshad K, Yaghobi-Ershadi M, Pedram M, Vatandoost H, Abai M, Abai MR, Akbarzadeh K, Mohtarami F (2007) Genetic structure of the ma-laria vector Anopheles superpictus in Iran using mitochondrial cytochrome oxidase (COI and COII) and morpho-logic markers: A new spe¬cies com-plex? Acta Trop. 101: 241−248.
8. Oshaghi M, Vatandoost H, Gorouhi A,
Abai M, Madjidpour A, Arshi S, Sadeghi H, Nazari M, Mehravaran A (2011) Anophe¬line species composi¬tion in bor¬derline of Iran-Azerbaijan. Acta Trop. 119: 44−449.
9. Oshaghi M, Yaghobi-Ershadi M, Shemshad K, Pedram M, Amani H (2008) The Anopheles superpictus complex: in-troduction of a new malaria vector complex in Iran. Bull Soc Pathol Exot. 101: 429−434.
10. Sedaghat M, Linton YM, Oshaghi M, Vatandoost H, Harbach R (2003) The Anopheles maculipennis complex (Dip¬tera: Culicidae) in Iran: molecular characterization and recognition of a new species. Bull Entomol Res. 93: 527−535.
11. Feo ML, Eljarrat E, Manaca MN, Do¬baño C, Barcelo D, Sunyer J, Alonso PL, Menen¬dez C, Grimalt JO (2012) Pyre-throid use-malaria control and individual applications by households for other pests and home garden use. Environ International. 38: 67−72.
12. Gorouhi MA, Vatandoost H, Oshaghi MA, Raeisi A, Enayati AA, Mirhendi H, Hanafi-Bojd AA, Abai MR, Salim-Abadi Y, Rafi F (2016) Current sus-ceptibility status of Anopheles ste-phen¬si (Diptera: Culicidae) to differ-ent imagicides in a malarious area, south¬eastern of Iran. J Arthropod Borne Dis. 10(4): 493−500.
13. Vatandoost H, Hanafi-Bojd AA (2012) Indication of pyrethroid resistance in the main malaria vector, Anopheles ste-phensi from Iran. Asian Pac J Trop Med. 5: 722−726.
14. Raeisi A, Gouya MM, Nadim A, Ranjbar M, Hasanzehi A, Fallahnezhad M, Sakeni M, Safari R, Saffari M, Mashyekhi M, Ahmadi Kahnali A, Mirkhani V, Al-masian E, Faraji L, Paktinat Jalali B, Nikpour F (2013) De¬termination of ma¬laria epidemiological status in Iran's ma¬larious areas as base¬line in-formation for implementation of ma-laria elimination program in Iran. Iran J Public Health. 42: 326−333.
15. Abai M, Mehravaran A, Vatandoost H, Oshaghi MA, Javadian E, Mashayekhi M, Mosleminia A, Piyazak N, Edallat H, Mohtarami F, Jabbari H, Rafi F (2008) Comparative performance of imagicides on Anopheles stephensi, main malaria vector in a malarious ar-ea, southern Iran. J Vector Borne Dis. 45: 307−312.
16. Nejati J, Vatandoost H, Oshghi MA, Salehi M, Mozafari E, Moosa-Kazemi SH (2013) Some ecological attributes of ma¬larial vector Anopheles superpic¬tus Grassi in endemic foci in south¬eastern Iran. Asian Pac J Trop Biomed. 3: 1003−1008.
17. Soltani A, Vatandoost H, Oshaghi MA, Ravasan NM, Enayati AA, Asgarian F (2015) Resistance Mechanisms of Anoph-eles stephensi (Diptera: Cu¬licidae) to Temeph¬os. J Arthropod Borne Dis. 9: 71−83.
18. Syafruddin D, Hidayati AP, Asih PB, Hawley WA, Sukowati S, Lobo NF (2010) Detection of 1014F kdr muta-tion in four major Anopheline malaria vectors in Indonesia. Malar J. 9: 315− 323.
19. Soltani A, Vatandoost H, Oshaghi MA, Enayati AA, Raeisi A, Eshraghian MR, Soltan-Dallal MM, Hanafi-Bojd AA, Abai MR, Rafi F (2013) Baseline sus-ceptibility of different geographical strains of Anopheles stephensi (Dip-tera: Culicidae) to temephos in malari-ous areas of Iran. J Arthropod Borne Dis. 7: 56−65.
20. Chen L, Zhong D, Zhang D, Shi L, Zhou G, Gong M, Zhou H, Sun Y, Ma L, He J, Hong S, Zhou D, Xiong C, Chen C, Zou P, Zhu C, Yan G (2010) Molecu-lar ecology of pyrethroid knockdown re¬sistance in Culex pipiens pallens mos¬quitoes. PLoS One. 5(7): 1−9.
21. Enayati AA, Vatandoost H, Ladonni H,
Townson H, Hemingway J (2003) Mo-lecular evidence for a kdr-like pyre¬throid resistance mechanism in the ma¬laria vec¬tor mosquito Anopheles ste¬phensi. Med Vet Entomol. 17: 138−44.
22. Hemingway J (1983) The genetics of mal¬athion resistance in Anopheles ste-phen¬si from Pakistan. Trans R Soc Trop Med. 77: 106−108.
23. Lol JC, Castellanos ME, Liebman KA, Lenhart A, Pennington PM, Padilla NR (2013) Molecular evidence for histori-cal presence of knock-down resistance in Anopheles albimanus, a key malaria vector in Latin America. Parasit Vec-tors. 6: 268−278.
24. Safi NHZ, Ahmadi AA, Nahzat S, Zia-pour SP, Nikookar SH, Fazeli-Dinan M, Enayati A, Hemingway J (2017) Evidence of metabolic mechanisms playing a role in multiple insecticides resistance in Anopheles stephensi pop-u¬lations from Afghanistan. Malar J. 16: 100−107.
25. Singh OP, Dykes CL, Lather M, Agrawal OP, Adak T (2011) Knock-down resistance (kdr)-like mutations in the voltage-gated sodium channel of a malaria vector Anopheles stephensi and PCR assays for their detection. Mal J. 10: 59−68.
26. Coleman M, Hemingway J, Gleave KA, Wiebe A, Gething PW, Moyes CL (2017) Developing global maps of in¬secticide resistance risk to improve vec¬tor con-trol. Mal J. 16: 86−95.
27. World Health organization (2013) Test pro¬cedures for insecticide resistance mon-itoring in malaria vector mosqui¬toes. Geneva, World Health Organiza¬tion.
28. Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione S-transfer-ases and insecticide resistance Insect Mol Biol. 14: 3−8.
29. Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis
of insecticide resistance in mosqui-toes.
Insect Biochem Mol Biol. 34: 653−665.
30. Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa. 2078: 1−33.
31. Hemingway J (1989) A practical field and laboratory manual for the mecha-nistic detection of insecticide re¬sistance in insects. WHO TDR series book.
32. Montella IR, Martins AJ, Viana-Medeiros PF, Lima JBP, Braga IA, Valle D (2007) Insecticide resistance mechanisms of Bra¬zilian Aedes aegypti populations from 2001 to 2004: Am J Trop Med Hyg. 77: 467−477.
33. Rubert A, Guillon-Grammatico L, Chan-denier J, Dimier-Poisson I, Desou¬beaux G (2016) Insecticide resistance in Anoph¬eles mosquitoes: additional obstacles in the battle against malaria. Med Sante Trop. 26: 423−431.
34. World Health Organization (2012) Glob¬al plan for insecticide resistance man¬agement in malaria vectors (GPIRM). World Health Organization, Geneva.
35. Kasap H, Kasap M, Alptekin D, Lüleyap Ü, Herath P (2000) Insecticide re¬sistance in Anopheles sacharovi Favre in southern Turkey. Bull World Health Org. 78: 687−692.
36. Himeidan YE, Chen H, Chandre F, Don-nelly MJ, Yan G (2007) Permethrin and DDT resistance in the malaria vec¬tor Anoph¬eles arabiensis from Eastern Sudan. Am J Trop Med Hyg. 77: 1066− 1068.
37. Ganesh K, Urmila J, Vijayan V (2003) Payrethroid susceptibility and enzyme activity in two malaria vectors, Anoph¬eles stephensi (Liston) and An. culic¬ifacies (Giles) from Mysore, In-dia. In¬dian J Med Res. 117: 30−38.
38. Vulule J, Beach R, Atieli F, McAllister J, Brogdon W, Roberts JM, Mwangi RW, Hawley WA (1999) Elevated ox-idase and esterase levels associated with per¬methrin tolerance in Anophe-les gambiae from Kenyan villages us-ing permethrin impregnated nets. Med Vet Entomol. 13: 239−244.
39. Brogdon WG, McAllister JC, Corwin AM, Cordon-Rosales C (1999). Inde-pendent selection of multiple mecha-nisms for pyrethroid resistance in Gua¬temalan Anopheles albimanus (Diptera: Culicidae). J Med Entomol. 92: 298− 302.
40. Brogdon WG, Barber AM (1990) Fenitro¬thion-deltamethrin cross-resistance con¬ferred by esterases in Gua-temalan Anoph¬eles albimanus. Pestic Biochem Physiol. 37: 130−139.
41. Rongnoparut P, Boonsuepsakul S, Chareonviri¬yaphap T, Thanomsing N (2003) Cloning of cytochrome P450, CYP6P5, and CYP6AA2 from Anoph-eles minimus resistant to del¬tamethrin. J Vector Ecol. 28: 150−158.
42. Hemingway J (2000) The molecular ba-sis of two contrasting metabolic mech-anisms of insecticide resistance. Insect Biochem Mol Biol. 30: 1009−1015.
43. Scott J, Georghiou G (1986) Malathion-specific resistance in Anopheles ste¬phensi from Pakistan. J Am Mosq Con¬trol Assoc. 2: 29−32.
44. Enayati AA, Ladonni (2006) Biochemi-cal assay baseline data of permethrin resistance in Anopheles stephensi (Dip¬tera, Culicidae) from Iran. Pakistan J Biol Sci. 9: 1265−1270.
45. Hemingway J, Ranson H (2000) Insecti-cide resistance in insect vectors of hu-man disease. Annu Rev Entomol. 45: 371−391.
46. Limoee M, Enayati A, Ladonni H, Vatan-doost H, Baseri H, Oshaghi (2007) Var¬ious mechanisms responsi¬ble for permethrin metabolic resistance in seven field-collected strains of the German cockroach from Iran, Blattella germanica (L.) (Dictyoptera: Blattelli-dae). Pes¬tic Biochem Physiol. 87: 138−146.
47. Hargreaves K, Hunt R, Brooke B, Mthem¬bu J, Weeto M, Awolola T, Coetzee M (2003) Anopheles ara-biensis and An. quadriannulatus re-sistance to DDT in South Africa. Med Vet Entomol. 17: 417−422.
48. Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS (2010) Pyrethroid re-sistance in an Anopheles funestus pop-ulation from Uganda. PLoS One. 5(7): 1−8.
49. Corbel V, N’guessan R, Brengues C, Chan-dre F, Djogbenou L, Martin T, Akog-béto M, Hougard JM, Rowland M (2007) Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Be-nin, West Africa. Acta Trop. 101: 207−216.
2. Azari-Hamidian S (2011) Larval habitat characteristics of the genus Anopheles (Diptera: Culicidae) and a checklist of mosquitoes in Guilan Province, north-ern Iran. Iran J Arthropod Borne Dis. 5 (1): 37−53.
3. Mehravaran A, Oshaghi M, Vatandoost H, Abai M, Ebrahimzadeh A, Roodi AM, Grouhi A (2011) First report on Anoph¬eles fluviatilis U in southeastern Iran. Acta Trop. 117: 76−81.
4. Naddaf Dezfouli S, Oshaghi M, Vatan-doost H, Assmar M (2003) rDNA-ITS2 based species-diagnostic polymerase chain reaction assay for identification of sibling species of anopheles fluviatilis in Iran. Southeast Asian J Trop Med Public Health. 34: 56−60.
5. Vatandoost H, Oshaghi M, Abaie M, Shahi M, Yaaghoobi F, Baghaii M, Hanafi-Bojd AA, Zamani G, Townson H (2006) Bionomics of Anopheles stephensi Liston in the malarious area of Hor¬mozgan Province, southern Iran, 2002. Acta Trop. 97: 196−203.
6. Karimian F, Oshaghi MA, Sedaghat MM, Waterhouse RM, Vatandoost H, Hanafi-Bojd AA, Ravasan NM, Chavshin AR (2014) Phylogenetic analysis of the ori¬ental-palearctic-afrotropical members of anopheles (Culicidae: Diptera) based on nuclear rDNA and mitochondrial DNA charac¬teristics. Jpn J Infect Dis. 67: 361−367.
7. Oshaghi M, Shemshad K, Yaghobi-Ershadi M, Pedram M, Vatandoost H, Abai M, Abai MR, Akbarzadeh K, Mohtarami F (2007) Genetic structure of the ma-laria vector Anopheles superpictus in Iran using mitochondrial cytochrome oxidase (COI and COII) and morpho-logic markers: A new spe¬cies com-plex? Acta Trop. 101: 241−248.
8. Oshaghi M, Vatandoost H, Gorouhi A,
Abai M, Madjidpour A, Arshi S, Sadeghi H, Nazari M, Mehravaran A (2011) Anophe¬line species composi¬tion in bor¬derline of Iran-Azerbaijan. Acta Trop. 119: 44−449.
9. Oshaghi M, Yaghobi-Ershadi M, Shemshad K, Pedram M, Amani H (2008) The Anopheles superpictus complex: in-troduction of a new malaria vector complex in Iran. Bull Soc Pathol Exot. 101: 429−434.
10. Sedaghat M, Linton YM, Oshaghi M, Vatandoost H, Harbach R (2003) The Anopheles maculipennis complex (Dip¬tera: Culicidae) in Iran: molecular characterization and recognition of a new species. Bull Entomol Res. 93: 527−535.
11. Feo ML, Eljarrat E, Manaca MN, Do¬baño C, Barcelo D, Sunyer J, Alonso PL, Menen¬dez C, Grimalt JO (2012) Pyre-throid use-malaria control and individual applications by households for other pests and home garden use. Environ International. 38: 67−72.
12. Gorouhi MA, Vatandoost H, Oshaghi MA, Raeisi A, Enayati AA, Mirhendi H, Hanafi-Bojd AA, Abai MR, Salim-Abadi Y, Rafi F (2016) Current sus-ceptibility status of Anopheles ste-phen¬si (Diptera: Culicidae) to differ-ent imagicides in a malarious area, south¬eastern of Iran. J Arthropod Borne Dis. 10(4): 493−500.
13. Vatandoost H, Hanafi-Bojd AA (2012) Indication of pyrethroid resistance in the main malaria vector, Anopheles ste-phensi from Iran. Asian Pac J Trop Med. 5: 722−726.
14. Raeisi A, Gouya MM, Nadim A, Ranjbar M, Hasanzehi A, Fallahnezhad M, Sakeni M, Safari R, Saffari M, Mashyekhi M, Ahmadi Kahnali A, Mirkhani V, Al-masian E, Faraji L, Paktinat Jalali B, Nikpour F (2013) De¬termination of ma¬laria epidemiological status in Iran's ma¬larious areas as base¬line in-formation for implementation of ma-laria elimination program in Iran. Iran J Public Health. 42: 326−333.
15. Abai M, Mehravaran A, Vatandoost H, Oshaghi MA, Javadian E, Mashayekhi M, Mosleminia A, Piyazak N, Edallat H, Mohtarami F, Jabbari H, Rafi F (2008) Comparative performance of imagicides on Anopheles stephensi, main malaria vector in a malarious ar-ea, southern Iran. J Vector Borne Dis. 45: 307−312.
16. Nejati J, Vatandoost H, Oshghi MA, Salehi M, Mozafari E, Moosa-Kazemi SH (2013) Some ecological attributes of ma¬larial vector Anopheles superpic¬tus Grassi in endemic foci in south¬eastern Iran. Asian Pac J Trop Biomed. 3: 1003−1008.
17. Soltani A, Vatandoost H, Oshaghi MA, Ravasan NM, Enayati AA, Asgarian F (2015) Resistance Mechanisms of Anoph-eles stephensi (Diptera: Cu¬licidae) to Temeph¬os. J Arthropod Borne Dis. 9: 71−83.
18. Syafruddin D, Hidayati AP, Asih PB, Hawley WA, Sukowati S, Lobo NF (2010) Detection of 1014F kdr muta-tion in four major Anopheline malaria vectors in Indonesia. Malar J. 9: 315− 323.
19. Soltani A, Vatandoost H, Oshaghi MA, Enayati AA, Raeisi A, Eshraghian MR, Soltan-Dallal MM, Hanafi-Bojd AA, Abai MR, Rafi F (2013) Baseline sus-ceptibility of different geographical strains of Anopheles stephensi (Dip-tera: Culicidae) to temephos in malari-ous areas of Iran. J Arthropod Borne Dis. 7: 56−65.
20. Chen L, Zhong D, Zhang D, Shi L, Zhou G, Gong M, Zhou H, Sun Y, Ma L, He J, Hong S, Zhou D, Xiong C, Chen C, Zou P, Zhu C, Yan G (2010) Molecu-lar ecology of pyrethroid knockdown re¬sistance in Culex pipiens pallens mos¬quitoes. PLoS One. 5(7): 1−9.
21. Enayati AA, Vatandoost H, Ladonni H,
Townson H, Hemingway J (2003) Mo-lecular evidence for a kdr-like pyre¬throid resistance mechanism in the ma¬laria vec¬tor mosquito Anopheles ste¬phensi. Med Vet Entomol. 17: 138−44.
22. Hemingway J (1983) The genetics of mal¬athion resistance in Anopheles ste-phen¬si from Pakistan. Trans R Soc Trop Med. 77: 106−108.
23. Lol JC, Castellanos ME, Liebman KA, Lenhart A, Pennington PM, Padilla NR (2013) Molecular evidence for histori-cal presence of knock-down resistance in Anopheles albimanus, a key malaria vector in Latin America. Parasit Vec-tors. 6: 268−278.
24. Safi NHZ, Ahmadi AA, Nahzat S, Zia-pour SP, Nikookar SH, Fazeli-Dinan M, Enayati A, Hemingway J (2017) Evidence of metabolic mechanisms playing a role in multiple insecticides resistance in Anopheles stephensi pop-u¬lations from Afghanistan. Malar J. 16: 100−107.
25. Singh OP, Dykes CL, Lather M, Agrawal OP, Adak T (2011) Knock-down resistance (kdr)-like mutations in the voltage-gated sodium channel of a malaria vector Anopheles stephensi and PCR assays for their detection. Mal J. 10: 59−68.
26. Coleman M, Hemingway J, Gleave KA, Wiebe A, Gething PW, Moyes CL (2017) Developing global maps of in¬secticide resistance risk to improve vec¬tor con-trol. Mal J. 16: 86−95.
27. World Health organization (2013) Test pro¬cedures for insecticide resistance mon-itoring in malaria vector mosqui¬toes. Geneva, World Health Organiza¬tion.
28. Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione S-transfer-ases and insecticide resistance Insect Mol Biol. 14: 3−8.
29. Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis
of insecticide resistance in mosqui-toes.
Insect Biochem Mol Biol. 34: 653−665.
30. Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa. 2078: 1−33.
31. Hemingway J (1989) A practical field and laboratory manual for the mecha-nistic detection of insecticide re¬sistance in insects. WHO TDR series book.
32. Montella IR, Martins AJ, Viana-Medeiros PF, Lima JBP, Braga IA, Valle D (2007) Insecticide resistance mechanisms of Bra¬zilian Aedes aegypti populations from 2001 to 2004: Am J Trop Med Hyg. 77: 467−477.
33. Rubert A, Guillon-Grammatico L, Chan-denier J, Dimier-Poisson I, Desou¬beaux G (2016) Insecticide resistance in Anoph¬eles mosquitoes: additional obstacles in the battle against malaria. Med Sante Trop. 26: 423−431.
34. World Health Organization (2012) Glob¬al plan for insecticide resistance man¬agement in malaria vectors (GPIRM). World Health Organization, Geneva.
35. Kasap H, Kasap M, Alptekin D, Lüleyap Ü, Herath P (2000) Insecticide re¬sistance in Anopheles sacharovi Favre in southern Turkey. Bull World Health Org. 78: 687−692.
36. Himeidan YE, Chen H, Chandre F, Don-nelly MJ, Yan G (2007) Permethrin and DDT resistance in the malaria vec¬tor Anoph¬eles arabiensis from Eastern Sudan. Am J Trop Med Hyg. 77: 1066− 1068.
37. Ganesh K, Urmila J, Vijayan V (2003) Payrethroid susceptibility and enzyme activity in two malaria vectors, Anoph¬eles stephensi (Liston) and An. culic¬ifacies (Giles) from Mysore, In-dia. In¬dian J Med Res. 117: 30−38.
38. Vulule J, Beach R, Atieli F, McAllister J, Brogdon W, Roberts JM, Mwangi RW, Hawley WA (1999) Elevated ox-idase and esterase levels associated with per¬methrin tolerance in Anophe-les gambiae from Kenyan villages us-ing permethrin impregnated nets. Med Vet Entomol. 13: 239−244.
39. Brogdon WG, McAllister JC, Corwin AM, Cordon-Rosales C (1999). Inde-pendent selection of multiple mecha-nisms for pyrethroid resistance in Gua¬temalan Anopheles albimanus (Diptera: Culicidae). J Med Entomol. 92: 298− 302.
40. Brogdon WG, Barber AM (1990) Fenitro¬thion-deltamethrin cross-resistance con¬ferred by esterases in Gua-temalan Anoph¬eles albimanus. Pestic Biochem Physiol. 37: 130−139.
41. Rongnoparut P, Boonsuepsakul S, Chareonviri¬yaphap T, Thanomsing N (2003) Cloning of cytochrome P450, CYP6P5, and CYP6AA2 from Anoph-eles minimus resistant to del¬tamethrin. J Vector Ecol. 28: 150−158.
42. Hemingway J (2000) The molecular ba-sis of two contrasting metabolic mech-anisms of insecticide resistance. Insect Biochem Mol Biol. 30: 1009−1015.
43. Scott J, Georghiou G (1986) Malathion-specific resistance in Anopheles ste¬phensi from Pakistan. J Am Mosq Con¬trol Assoc. 2: 29−32.
44. Enayati AA, Ladonni (2006) Biochemi-cal assay baseline data of permethrin resistance in Anopheles stephensi (Dip¬tera, Culicidae) from Iran. Pakistan J Biol Sci. 9: 1265−1270.
45. Hemingway J, Ranson H (2000) Insecti-cide resistance in insect vectors of hu-man disease. Annu Rev Entomol. 45: 371−391.
46. Limoee M, Enayati A, Ladonni H, Vatan-doost H, Baseri H, Oshaghi (2007) Var¬ious mechanisms responsi¬ble for permethrin metabolic resistance in seven field-collected strains of the German cockroach from Iran, Blattella germanica (L.) (Dictyoptera: Blattelli-dae). Pes¬tic Biochem Physiol. 87: 138−146.
47. Hargreaves K, Hunt R, Brooke B, Mthem¬bu J, Weeto M, Awolola T, Coetzee M (2003) Anopheles ara-biensis and An. quadriannulatus re-sistance to DDT in South Africa. Med Vet Entomol. 17: 417−422.
48. Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS (2010) Pyrethroid re-sistance in an Anopheles funestus pop-ulation from Uganda. PLoS One. 5(7): 1−8.
49. Corbel V, N’guessan R, Brengues C, Chan-dre F, Djogbenou L, Martin T, Akog-béto M, Hougard JM, Rowland M (2007) Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Be-nin, West Africa. Acta Trop. 101: 207−216.
| Files | ||
| Issue | Vol 12 No 3 (2018) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v12i3.82 | |
| Keywords | ||
| Anopheles stephensi Insecticide Resistance mechanisms Malaria | ||
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How to Cite
1.
Gorouhi MA, Oshaghi MA, Vatandoost H, Enayati AA, Abai MR, Karami M, Salim-Abadi Y, Hanafi-Bojd AA, Aghaei-Afshar A, Paksa A, Nikpoor F. Biochemical Basis of Cyfluthrin and DDT Resistance in Anopheles stephensi (Diptera: Culicidae) in Malarious Area of Iran. J Arthropod Borne Dis. 2018;12(3):310-320.
