Ace-1 Target Site Status and Metabolic Detoxification Associated with Bendiocarb Resistance in the Field Populations of Main Malaria Vector, Anopheles stephensi in Iran
-
Abdollah Badzohre
,
Mohammad Ali Oshaghi
,
Ahmad Ali Enayati
,
Seyed Hassan Moosa- Kazemi
,
Seyed Hassan Nikookar
,
Fahimeh Talebzadeh
,
Nazanin Naseri-Karimi
,
Ahmad Ali Hanafi-Bojd
,
Hassan Vatandoost
Abstract
Background: Anopheles stephensi is the main vector of malaria in Iran. This study aimed to determine the susceptibility of An. stephensi from the south of Iran to bendiocarb and to investigate biochemical and molecular resistance mechanisms in this species.
Methods: Wild An. stephensi were collected from Hormozgan Province and reared to the adult stage. The susceptibility test was conducted according to the WHO protocols using bendiocarb impregnated papers supplied by WHO. Also, field An. Stephensi specimens were collected from south of Kerman and Sistan and Baluchistan Provinces. To determine the G119S mutation in the acetylcholinesterase (Ace1) gene, PCR-RFLP using AluI restriction enzyme and PCR direct-sequencing were performed for the three field populations and compared with the available GenBank data. Also, biochemical assays were performed to measure alpha and beta esterases, insensitive acetylcholinesterase, and oxidases in the strains.
Results: The bioassay tests showed that the An. stephensi field strain was resistant to bendiocarb (mortality rate 89%). Ace1 gene analysis revealed no G119S in the three field populations. Blast search of sequences revealed 98–99% identity with the Ace1 gene from Pakistan and India respectively. Also, the results of biochemical tests revealed the high activity of non-sensitive acetylcholinesterase, alpha and beta-esterase in the resistant strain compared to the susceptible strain. No G119S was detected in this study additionally the enhanced enzyme activity of esterases and acetylcholinesterase suggesting that resistance was metabolic.
Conclusion: The use of alternative malaria control methods and the implementation of resistance management strategies are suggested in the study area.
1. Assogba BS, Djogbénou LS, Milesi P, Berthomieu A, Perez J, Ayala D, Chan-dre F, Makoutodé M, Labbé P, Weill M (2015) An ace-1 gene duplication resorbs the fitness cost associated with resistance in Anopheles gambiae, the main malaria mosquito. Sci Rep. 5: 14529.
2. Soltani A, Vatandoost H, Oshaghi MA, Ma¬leki-Ravasan N, Enayati AA, Asgarian F (2015) Resistance mechanisms of Anoph¬ eles stephensi (Diptera: Culicidae) to temeph¬os. J Arthropod Borne Dis. 9(1): 71–83.
3. Abbasi M, Hanafi-Bojd AA, Yaghoobi-Er-shadi MR, Vatandoost H, Oshaghi MA, Hazratian T, Sedaghat MM, Fekri S, Sa-fari R, Mojahedi AR, Salari Y (2019) Re¬sistance status of main malaria vector, Anopheles stephensi Liston (Diptera: Cu-licidae) to insecticides in a malaria En-demic Area, Southern Iran. Asian Pac J Tro Med. 12(1): 43–48.
4. Yared S, Gebressielasie A, Damodaran L, Bonnell V, Lopez K, Janies D, Carter TE (2020) Insecticide resistance in Anophe¬les stephensi in Somali Region, eastern Ethiopia. Malar J. 19(1): 180.
5. Fang Y, Shi WQ, Wu JT, Li YY, Xue JB, Zhang Y (2019) Resistance to pyrethroid and organophosphate insecticides, and the geographical distribution and polymor¬phisms of target-site mutations in volt¬age-gated sodium channel and acetylcho¬linesterase 1 genes in Anopheles sinensis populations in Shanghai, China. Parasit Vectors. 12(1): 396.
6. Ahoua Alou LP, Koffi AA, Adja MA, Tia E, Kouassi PK, Koné M, Chandre F (2010) Distribution of ace-1 R and resistance to carbamates and organophosphates in Anopheles gambiae ss populations from Côte d'Ivoire. Malar J. 9(1): 167.
7. Antonio-Nkondjio C, Poupardin R, Tene BF, Kopya E, Costantini C, Awono-Ambene P, Wondji CS (2016) Investigation of mech¬anisms of bendiocarb resistance in Anopheles gambiae populations from the city of Yaoundé, Cameroon. Malar J. 15 (1): 424.
8. Hemingway J (2000) The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochem Mol Biol. 30(11): 1009–1015.
9. Enayati A, Hanafi-Bojd AA, Sedaghat MM, Zaim M, Hemingway J (2020) Evolution of insecticide resistance and its mecha¬- nisms in Anopheles stephensi in the WHO Eastern Mediterranean Region. Malar J. 19(1): 258.
10. Ahmad M, Buhler C, Pignatelli P, Ranson H, Nahzat SM, Naseem M, Sabawoon MF, Siddiqi AM, Vink M (2016) Status of in¬secticide resistance in high-risk malaria provinces in Afghanistan. Malar J. 15: 98.
11. Casimiro S, Coleman M, Hemingway J, Sharp B (2006) Insecticide resistance in Anopheles arabiensis and Anopheles gam¬biae from Mozambique. J Med Entomol. 43(2): 276–282.
12. Wu ZM, Chu HL, Wang G, Zhu XJ, Guo XX, Zhang YM, Xing D, Yan T, Zhao MH, Dong YD, Li CX (2016) Multiple-insecticide resistance and classic gene mutations to Japanese encephalitis vector Culex tritaeniorhynchus from China. J Am Mosq Cont Assoc. 32(2): 144–151.
13. Munywoki DN, Kokwaro ED, Mwangangi JM, Muturi EJ, Mbogo CM (2021) In¬secticide resistance status in Anopheles gambiae (s.l) in coastal Kenya. Parasit Vectors. 14(1): 207.
14. Opondo KO, Jawara M, Cham S, Jatta E, Jarju L, Camara M, Sanneh F, Gaye PM, Jadama L, Ceesay S, Njie E (2019) Status of insecticide resistance in Anopheles gambiae (s.l) of The Gambia. Parasit Vectors. 12(1): 278.
15. Vontas J, Kioulos E, Pavlidi N, Morou E, Della Torre A, Ranson H (2012) Insecti-cide resistance in the major dengue vec-tors Aedes albopictus and Aedes aegypti. Pestic Biochem Physiol. 104(2): 126–131.
16. Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I, Raghavendra K, Pinto J, Corbel V, David JP, Weetman D (2017) Contemporary status of insecti¬cide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl Trop Dis. 11(7): e0005625.
17. Safi NH, Ahmadi AA, Nahzat S, Ziapour SP, Nikookar SH, Fazeli-Dinan M, Enayati A, Hemingway J (2017) Evidence of met¬ abolic mechanisms playing a role in mul-tiple insecticides resistance in Anopheles stephensi populations from Afghanistan. Malar J. 16(1): 100.
18. Vatandoost H, Hanafi-Bojd AA (2012) Indication of pyrethroid resistance in the main malaria vector, Anopheles stephen¬si from Iran. Asian Pac J Trop Med. 5(9): 722–726.
19. World Health Organization (2012) Global plan for insecticide resistance manage-ment in malaria vectors. World Health Organization, Geneva.
20. Djogbenou L, Labbe P, Chandre F, Pasteur N, Weill M (2009) Ace-1 duplication in Anopheles gambiae: a challenge for ma¬laria control. Malar J. 8: 70.
21. Weetman D, Mitchell SN, Wilding CS, Birks DP, Yawson AE, Essandoh J, Mawejje HD, Djogbenou LS, Steen K, Rippon EJ, Clarkson CS (2015) Con¬tem-porary evolution of resistance at the ma-jor insecticide target site gene Ace‐1 by mutation and copy number variation in the malaria mosquito Anopheles gambiae. Mol Ecol. 24(11): 2656–2672.
22. Aïkpon R, Agossa F, Ossè R, Oussou O, Aïzoun N, Oké-Agbo F, Akogbéto M (2013) Bendiocarb resistance in Anophe-les gambiae s.l. populations from Atacora department in Benin, West Africa: a threat for malaria vector control. Parasit Vec¬tors. 6: 192.
23. Dabiré KR, Diabaté A, Namontougou M, Djogbenou L, Kengne P, Simard F, Bass C, Baldet T (2009) Distribution of in-sensitive acetylcholinesterase (ace‐1R) in Anopheles gambiae s.l populations from Burkina Faso (West Africa). Trop Med Int Health. 14(4): 396–403.
24. Essandoh J, Yawson AE, Weetman D (2013) Acetylcholinesterase (Ace-1) target site mutation 119S is strongly diagnostic of carbamate and organophosphate re¬sistance in Anopheles gambiae ss and Anopheles coluzzii across southern Ghana. Malar J. 12(1): 404–414.
25. Weill M, Malcolm C, Chandre F, Mo-gensen K, Berthomieu A, Marquine M, Ray¬mond M (2004) The unique mutation in ace‐1 giving high insecticide resistance is eas¬ily detectable in mosquito vectors. Insect Mol Biol. 13(1): 1–7.
26. Azari-Hamidian Sh, Harbach RE (2009) Keys to the adult females and fourth-in-star larvae of the mosquitoes of Iran (Dip¬tera: Culicidae). Zootaxa. 2078: 1–33.
27. World Health Organization (2016) Mon-itoring and managing insecticide re-sistance in Aedes mosquito populations: interim guidance for entomologists, Geneva. Avail¬able at: https://www.who.int/publications/i/item/WHO-ZIKV-VC-16.1
28. Ossè R, Aikpon R, Padonou GG, Oussou O, Yadouléton A, Akogbéto M (2012) Evaluation of the efficacy of bendiocarb in indoor residual spraying against pyre-throid resistant malaria vectors in Benin: results of the third campaign. Parasit Vec¬tors. 5: 163.
29. Azizi K, Soltani A, Poodat A, Khodadadi M, Yaran M, Hasanvand B (2011) Sus-cep¬tibility of Anopheles stephensi against five current chemical insecticides. Hor¬mozgan Med J. 14(4): 305–311.
30. Safi NH, Ahmadi AA, Nahzat S, Warusa-vithana S, Safi N, Valadan R, Shemshad¬ian A, Sharifi M, Enayati A, Hemingway J (2019) Status of insecticide resistance and its biochemical and molecular mech¬anisms in Anopheles stephensi (Diptera: Culicidae) from Afghanistan. Malar J. 18 (1): 249.
31. Vatandoost H, Hanafi-Bojd AA, Nikpoor F, Raeisi A, Abai MR, Zaim M (2022) Situation of insecticide resistance in ma-laria vectors in the World Health Or¬gan-ization of Eastern Mediterranean region 1990–2020. Toxicol Res. 11(1): 1–21.
32. Susanna D, Pratiwi D (2021) Current status of insecticide resistance in malaria vec¬tors in the Asian countries: a systematic review. F1000 Res. 10: 200.
33. Kpanou CD, Sagbohan HW, Padonou GG, Ossè R, Salako AS, Fassinou AJ, Sovi A, Yovogan B, Adoha C, Sominahouin A, Ahogni I (2021) Susceptibility of Anoph¬eles gambiae sensu lato to different in¬sec¬ticide classes and mechanisms in¬volved in the South-North transect of Benin. J Entomol. 11(2): 25–37.
34. Olatunbosun-Oduola A, Abba E, Adelaja O, Taiwo-Ande A, Poloma-Yoriyo K, Samson-Awolola T (2019) Widespread report of multiple insecticide resistance in Anopheles gambiae sl mosquitoes in eight communities in southern Gombe, North-Eastern Nigeria. J Arthropod Borne Dis. 13(1): 50–61.
35. Wahedi J, Ande A, Oduola A, Obembe A (2021) Bendiocarb resistance and, kdr as¬sociated deltamethrin and DDT re-sistance in Anopheles gambiae s.l populations from North Eastern Adamawa State, Nigeria. Ceyl J Sci. 50(1): 63–73.
36. Matiya DJ, Philbert AB, Kidima W, Ma-towo JJ (2019) Dynamics and monitoring of insecticide resistance in malaria vec¬tors across mainland Tanzania from 1997 to 2017: a systematic review. Malar J. 18(1): 102.
37. Choi KS, Christian R, Nardini L, Wood OR, Agubuzo E, Muleba M, Munyati S, Ma¬kuwaza A, Koekemoer LL, Brooke BD, Hunt RH (2014) Insecticide resistance and role in malaria transmission of Anopheles funestus populations from Zambia and Zimbabwe. Parasit Vectors. 7: 464.
38. Chanda J, Saili K, Phiri F, Stevenson JC, Mwenda M, Chishimba S, Mulube C, Mamb¬we B, Lungu C, Earle D, Bennett A (2020) Pyrethroid and carbamate re-sistance in Anopheles funestus Giles along Lake Kariba in southern Zambia. Am J Trop Med Hyg. 103(2): 90–97.
39. Mekuriaw W, Yewhalaw D, Dugassa S, Taffese H, Bashaye S, Nigatu W, Masse¬bo F (2020) Distribution and trends of insecticide resistance in malaria vectors in Ethiopia (1986-2017): a review. Ethiop J Pub Heal Nut. 3(Special): 51–61.
40. Gorouhi MA, Oshaghi MA, Vatandoost H, Enayati AA, Raeisi A, Abai MR, Salim-Abadie Y, Hanafi-Bojd AA, Paksa A, Nikpoor F (2018) Biochemical basis of cyfluthrin and DDT resistance in Anoph¬eles stephensi (Diptera: Culicidae) in ma¬larious area of Iran. J Arthropod Borne Dis. 12(3): 310–320.
41. Singh OP, Dykes CL, Lather M, Agrawal OP, Adak T (2011) Knockdown resistance (kdr)-like mutations in the voltage-gated sodium channel of a malaria vector Anoph¬eles stephensi and PCR assays for their detection. Malar J. 10(1): 59.
42. Yavaşoglu Sİ, Yaylagül EÖ, Akıner MM, Ülger C, Çağlar SS, Şimşek FM (2019) Current insecticide resistance status in Anopheles sacharovi and Anopheles su-perpictus populations in former malaria endemic areas of Turkey. Acta Trop. 193: 148–157.
43. Nejati J, Moosa-Kazemi SH, Oshaghi MA, Badzohre A, Pirmohammadi M, Saeidi Z, Naseri-Karimi N, Parkhideh SZ, Vatan¬doost H (2021) Insecticide Resistance Status of Malaria Vectors in a Malarious Area, Southeast of Iran. J Arthropod Borne Dis. 15(3): 278–286.
44. Dzul FA, Patricia Penilla R, Rodríguez AD (2007) Susceptibility and inseticide re¬sistance mechanisms in Anopheles albi-manus from the southern Yucatan Penin¬sula, Mexico. Salud Publica Mex. 49(4): 302–311.
45. Akiner MM (2014) Malathion and propoxur resistance in Turkish populations of the Anopheles maculipennis Meigen (Dip¬tera: Culicidae) and relation to the in¬sensitive acetylcholinesterase. Turkiye Parazitol Derg. 38(2): 111–115.
46. Fournier D (2005) Mutations of acetyl¬cho-lin¬esterase which confer insecticide re-sistance in insect populations. Chem Biol Interac. 157: 257–261.
47. Mutero A, Pralavorio M, Bride JM, Four-nier D (1994) Resistance-associated point mutations in insecticide-insensitive ace¬tyl¬cholinesterase. Proc Natl Acad Sci U S A. 91(13): 5922–5926.
48. Guo D, Luo J, Zhou Y, Xiao H, He K, Yin C, Xu J, Li F (2017) ACE: an efficient and sensitive tool to detect insecticide resistance-associated mutations in insect acetylcholinesterase from RNA-Seq da¬ta. BMC bioinformatics. 18(1): 330.
49. Binyang AJ, Elanga-Ndille E, Tene-Fossog B, Ndo C, Nouage L, Assatse T, Fotso-Toguem Y, Tabue R, Zeukeng F, Nguiffo DN, Etang J (2022) Distribution of ac¬etylcholinesterase (Ace-1R) target-site G 119S mutation and resistance to carba¬mates and organophosphates in Anophe¬les gambiae sensu lato populations from Cameroon. Parasit Vectors. 15(1): 53.
50. Keïta M, Kané F, Thiero O, Traoré B, Zeukeng F, Sodio AB, Traoré SF, Djouaka R, Doumbia S, Sogoba N (2020) Ace¬tylcholinesterase (ace-1R) target site mu¬tation G119S and resistance to carba¬mates in Anopheles gambiae (sensu lato) populations from Mali. Parasit Vectors. 13(1): 283.
51. Chabi J, Baidoo PK, Datsomor AK, Okyere D, Ablorde A, Iddrisu A, Wilson MD, Dadzie SK, Jamet HP, Diclaro JW (2016) Insecticide susceptibility of natural pop¬ulations of Anopheles coluzzii and Anoph¬eles gambiae (sensu stricto) from Okyereko irrigation site, Ghana, West Africa. Para-sit Vectors. 9: 182.
52. Sy O, Sarr P, Assogba B, Ndiaye M, Dia A, Ndiaye A (2021) Detection of Kdr and Ace-1 mutations in wild populations of Anopheles arabiensis and An. melas in a residual malaria transmission area of Sen¬egal. Pestic Biochem Physiol. 173: 104783.
53. Liebman KA, Pinto J, Valle J, Palomino M, Vizcaino L, Brogdon W, Lenhart A (2015) Novel mutations on the ace-1 gene of the malaria vector Anopheles albimanus pro¬vide evidence for balancing selection in an area of high insecticide resistance in Peru. Malar J. 14: 74.
54. Tmimi F-Z, Faraj C, Bkhache M, Mounaji K, Failloux AB, Sarih Mh (2018) In-secticide resistance and target site muta-tions (G119S ace-1 and L1014F kdr) of Culex pipiens in Morocco. Parasit Vec-tors. 11(1): 51.
55. Ibrahim SS, Ndula M, Riveron JM, Irving H, Wondji CS (2016) The P450 CYP 6Z1 confers carbamate/pyrethroid cross‐re¬sistance in a major African malaria vec¬tor beside a novel carbamate‐insensitive N485I acetylcholinesterase‐1 mutation. Molec Eco. 25(14): 3436–3452.
56. Hasmiwati H, Rusjdi SR, Nofita E (2018) Detection of Ace-1 gene with insec¬ti-cides resistance in Aedes aegypti popula-tions from DHF-endemic areas in Pa-dang, Indonesia. J Biolo Divers. 19(1): 31–36.
57. Elanga-Ndille E, Nouage L, Ndo C, Bin-yang A, Assatse T, Nguiffo-Nguete D, Djonabaye D, Irving H, Tene-Fossog B, Wondji CS (2019) The G119S acetylcho¬linesterase (Ace-1) target site mutation confers carbamate resistance in the major malaria vector Anopheles gambiae from Cameroon: a challenge for the coming IRS Implementation. Genes. 10(10): 790.
2. Soltani A, Vatandoost H, Oshaghi MA, Ma¬leki-Ravasan N, Enayati AA, Asgarian F (2015) Resistance mechanisms of Anoph¬ eles stephensi (Diptera: Culicidae) to temeph¬os. J Arthropod Borne Dis. 9(1): 71–83.
3. Abbasi M, Hanafi-Bojd AA, Yaghoobi-Er-shadi MR, Vatandoost H, Oshaghi MA, Hazratian T, Sedaghat MM, Fekri S, Sa-fari R, Mojahedi AR, Salari Y (2019) Re¬sistance status of main malaria vector, Anopheles stephensi Liston (Diptera: Cu-licidae) to insecticides in a malaria En-demic Area, Southern Iran. Asian Pac J Tro Med. 12(1): 43–48.
4. Yared S, Gebressielasie A, Damodaran L, Bonnell V, Lopez K, Janies D, Carter TE (2020) Insecticide resistance in Anophe¬les stephensi in Somali Region, eastern Ethiopia. Malar J. 19(1): 180.
5. Fang Y, Shi WQ, Wu JT, Li YY, Xue JB, Zhang Y (2019) Resistance to pyrethroid and organophosphate insecticides, and the geographical distribution and polymor¬phisms of target-site mutations in volt¬age-gated sodium channel and acetylcho¬linesterase 1 genes in Anopheles sinensis populations in Shanghai, China. Parasit Vectors. 12(1): 396.
6. Ahoua Alou LP, Koffi AA, Adja MA, Tia E, Kouassi PK, Koné M, Chandre F (2010) Distribution of ace-1 R and resistance to carbamates and organophosphates in Anopheles gambiae ss populations from Côte d'Ivoire. Malar J. 9(1): 167.
7. Antonio-Nkondjio C, Poupardin R, Tene BF, Kopya E, Costantini C, Awono-Ambene P, Wondji CS (2016) Investigation of mech¬anisms of bendiocarb resistance in Anopheles gambiae populations from the city of Yaoundé, Cameroon. Malar J. 15 (1): 424.
8. Hemingway J (2000) The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochem Mol Biol. 30(11): 1009–1015.
9. Enayati A, Hanafi-Bojd AA, Sedaghat MM, Zaim M, Hemingway J (2020) Evolution of insecticide resistance and its mecha¬- nisms in Anopheles stephensi in the WHO Eastern Mediterranean Region. Malar J. 19(1): 258.
10. Ahmad M, Buhler C, Pignatelli P, Ranson H, Nahzat SM, Naseem M, Sabawoon MF, Siddiqi AM, Vink M (2016) Status of in¬secticide resistance in high-risk malaria provinces in Afghanistan. Malar J. 15: 98.
11. Casimiro S, Coleman M, Hemingway J, Sharp B (2006) Insecticide resistance in Anopheles arabiensis and Anopheles gam¬biae from Mozambique. J Med Entomol. 43(2): 276–282.
12. Wu ZM, Chu HL, Wang G, Zhu XJ, Guo XX, Zhang YM, Xing D, Yan T, Zhao MH, Dong YD, Li CX (2016) Multiple-insecticide resistance and classic gene mutations to Japanese encephalitis vector Culex tritaeniorhynchus from China. J Am Mosq Cont Assoc. 32(2): 144–151.
13. Munywoki DN, Kokwaro ED, Mwangangi JM, Muturi EJ, Mbogo CM (2021) In¬secticide resistance status in Anopheles gambiae (s.l) in coastal Kenya. Parasit Vectors. 14(1): 207.
14. Opondo KO, Jawara M, Cham S, Jatta E, Jarju L, Camara M, Sanneh F, Gaye PM, Jadama L, Ceesay S, Njie E (2019) Status of insecticide resistance in Anopheles gambiae (s.l) of The Gambia. Parasit Vectors. 12(1): 278.
15. Vontas J, Kioulos E, Pavlidi N, Morou E, Della Torre A, Ranson H (2012) Insecti-cide resistance in the major dengue vec-tors Aedes albopictus and Aedes aegypti. Pestic Biochem Physiol. 104(2): 126–131.
16. Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I, Raghavendra K, Pinto J, Corbel V, David JP, Weetman D (2017) Contemporary status of insecti¬cide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl Trop Dis. 11(7): e0005625.
17. Safi NH, Ahmadi AA, Nahzat S, Ziapour SP, Nikookar SH, Fazeli-Dinan M, Enayati A, Hemingway J (2017) Evidence of met¬ abolic mechanisms playing a role in mul-tiple insecticides resistance in Anopheles stephensi populations from Afghanistan. Malar J. 16(1): 100.
18. Vatandoost H, Hanafi-Bojd AA (2012) Indication of pyrethroid resistance in the main malaria vector, Anopheles stephen¬si from Iran. Asian Pac J Trop Med. 5(9): 722–726.
19. World Health Organization (2012) Global plan for insecticide resistance manage-ment in malaria vectors. World Health Organization, Geneva.
20. Djogbenou L, Labbe P, Chandre F, Pasteur N, Weill M (2009) Ace-1 duplication in Anopheles gambiae: a challenge for ma¬laria control. Malar J. 8: 70.
21. Weetman D, Mitchell SN, Wilding CS, Birks DP, Yawson AE, Essandoh J, Mawejje HD, Djogbenou LS, Steen K, Rippon EJ, Clarkson CS (2015) Con¬tem-porary evolution of resistance at the ma-jor insecticide target site gene Ace‐1 by mutation and copy number variation in the malaria mosquito Anopheles gambiae. Mol Ecol. 24(11): 2656–2672.
22. Aïkpon R, Agossa F, Ossè R, Oussou O, Aïzoun N, Oké-Agbo F, Akogbéto M (2013) Bendiocarb resistance in Anophe-les gambiae s.l. populations from Atacora department in Benin, West Africa: a threat for malaria vector control. Parasit Vec¬tors. 6: 192.
23. Dabiré KR, Diabaté A, Namontougou M, Djogbenou L, Kengne P, Simard F, Bass C, Baldet T (2009) Distribution of in-sensitive acetylcholinesterase (ace‐1R) in Anopheles gambiae s.l populations from Burkina Faso (West Africa). Trop Med Int Health. 14(4): 396–403.
24. Essandoh J, Yawson AE, Weetman D (2013) Acetylcholinesterase (Ace-1) target site mutation 119S is strongly diagnostic of carbamate and organophosphate re¬sistance in Anopheles gambiae ss and Anopheles coluzzii across southern Ghana. Malar J. 12(1): 404–414.
25. Weill M, Malcolm C, Chandre F, Mo-gensen K, Berthomieu A, Marquine M, Ray¬mond M (2004) The unique mutation in ace‐1 giving high insecticide resistance is eas¬ily detectable in mosquito vectors. Insect Mol Biol. 13(1): 1–7.
26. Azari-Hamidian Sh, Harbach RE (2009) Keys to the adult females and fourth-in-star larvae of the mosquitoes of Iran (Dip¬tera: Culicidae). Zootaxa. 2078: 1–33.
27. World Health Organization (2016) Mon-itoring and managing insecticide re-sistance in Aedes mosquito populations: interim guidance for entomologists, Geneva. Avail¬able at: https://www.who.int/publications/i/item/WHO-ZIKV-VC-16.1
28. Ossè R, Aikpon R, Padonou GG, Oussou O, Yadouléton A, Akogbéto M (2012) Evaluation of the efficacy of bendiocarb in indoor residual spraying against pyre-throid resistant malaria vectors in Benin: results of the third campaign. Parasit Vec¬tors. 5: 163.
29. Azizi K, Soltani A, Poodat A, Khodadadi M, Yaran M, Hasanvand B (2011) Sus-cep¬tibility of Anopheles stephensi against five current chemical insecticides. Hor¬mozgan Med J. 14(4): 305–311.
30. Safi NH, Ahmadi AA, Nahzat S, Warusa-vithana S, Safi N, Valadan R, Shemshad¬ian A, Sharifi M, Enayati A, Hemingway J (2019) Status of insecticide resistance and its biochemical and molecular mech¬anisms in Anopheles stephensi (Diptera: Culicidae) from Afghanistan. Malar J. 18 (1): 249.
31. Vatandoost H, Hanafi-Bojd AA, Nikpoor F, Raeisi A, Abai MR, Zaim M (2022) Situation of insecticide resistance in ma-laria vectors in the World Health Or¬gan-ization of Eastern Mediterranean region 1990–2020. Toxicol Res. 11(1): 1–21.
32. Susanna D, Pratiwi D (2021) Current status of insecticide resistance in malaria vec¬tors in the Asian countries: a systematic review. F1000 Res. 10: 200.
33. Kpanou CD, Sagbohan HW, Padonou GG, Ossè R, Salako AS, Fassinou AJ, Sovi A, Yovogan B, Adoha C, Sominahouin A, Ahogni I (2021) Susceptibility of Anoph¬eles gambiae sensu lato to different in¬sec¬ticide classes and mechanisms in¬volved in the South-North transect of Benin. J Entomol. 11(2): 25–37.
34. Olatunbosun-Oduola A, Abba E, Adelaja O, Taiwo-Ande A, Poloma-Yoriyo K, Samson-Awolola T (2019) Widespread report of multiple insecticide resistance in Anopheles gambiae sl mosquitoes in eight communities in southern Gombe, North-Eastern Nigeria. J Arthropod Borne Dis. 13(1): 50–61.
35. Wahedi J, Ande A, Oduola A, Obembe A (2021) Bendiocarb resistance and, kdr as¬sociated deltamethrin and DDT re-sistance in Anopheles gambiae s.l populations from North Eastern Adamawa State, Nigeria. Ceyl J Sci. 50(1): 63–73.
36. Matiya DJ, Philbert AB, Kidima W, Ma-towo JJ (2019) Dynamics and monitoring of insecticide resistance in malaria vec¬tors across mainland Tanzania from 1997 to 2017: a systematic review. Malar J. 18(1): 102.
37. Choi KS, Christian R, Nardini L, Wood OR, Agubuzo E, Muleba M, Munyati S, Ma¬kuwaza A, Koekemoer LL, Brooke BD, Hunt RH (2014) Insecticide resistance and role in malaria transmission of Anopheles funestus populations from Zambia and Zimbabwe. Parasit Vectors. 7: 464.
38. Chanda J, Saili K, Phiri F, Stevenson JC, Mwenda M, Chishimba S, Mulube C, Mamb¬we B, Lungu C, Earle D, Bennett A (2020) Pyrethroid and carbamate re-sistance in Anopheles funestus Giles along Lake Kariba in southern Zambia. Am J Trop Med Hyg. 103(2): 90–97.
39. Mekuriaw W, Yewhalaw D, Dugassa S, Taffese H, Bashaye S, Nigatu W, Masse¬bo F (2020) Distribution and trends of insecticide resistance in malaria vectors in Ethiopia (1986-2017): a review. Ethiop J Pub Heal Nut. 3(Special): 51–61.
40. Gorouhi MA, Oshaghi MA, Vatandoost H, Enayati AA, Raeisi A, Abai MR, Salim-Abadie Y, Hanafi-Bojd AA, Paksa A, Nikpoor F (2018) Biochemical basis of cyfluthrin and DDT resistance in Anoph¬eles stephensi (Diptera: Culicidae) in ma¬larious area of Iran. J Arthropod Borne Dis. 12(3): 310–320.
41. Singh OP, Dykes CL, Lather M, Agrawal OP, Adak T (2011) Knockdown resistance (kdr)-like mutations in the voltage-gated sodium channel of a malaria vector Anoph¬eles stephensi and PCR assays for their detection. Malar J. 10(1): 59.
42. Yavaşoglu Sİ, Yaylagül EÖ, Akıner MM, Ülger C, Çağlar SS, Şimşek FM (2019) Current insecticide resistance status in Anopheles sacharovi and Anopheles su-perpictus populations in former malaria endemic areas of Turkey. Acta Trop. 193: 148–157.
43. Nejati J, Moosa-Kazemi SH, Oshaghi MA, Badzohre A, Pirmohammadi M, Saeidi Z, Naseri-Karimi N, Parkhideh SZ, Vatan¬doost H (2021) Insecticide Resistance Status of Malaria Vectors in a Malarious Area, Southeast of Iran. J Arthropod Borne Dis. 15(3): 278–286.
44. Dzul FA, Patricia Penilla R, Rodríguez AD (2007) Susceptibility and inseticide re¬sistance mechanisms in Anopheles albi-manus from the southern Yucatan Penin¬sula, Mexico. Salud Publica Mex. 49(4): 302–311.
45. Akiner MM (2014) Malathion and propoxur resistance in Turkish populations of the Anopheles maculipennis Meigen (Dip¬tera: Culicidae) and relation to the in¬sensitive acetylcholinesterase. Turkiye Parazitol Derg. 38(2): 111–115.
46. Fournier D (2005) Mutations of acetyl¬cho-lin¬esterase which confer insecticide re-sistance in insect populations. Chem Biol Interac. 157: 257–261.
47. Mutero A, Pralavorio M, Bride JM, Four-nier D (1994) Resistance-associated point mutations in insecticide-insensitive ace¬tyl¬cholinesterase. Proc Natl Acad Sci U S A. 91(13): 5922–5926.
48. Guo D, Luo J, Zhou Y, Xiao H, He K, Yin C, Xu J, Li F (2017) ACE: an efficient and sensitive tool to detect insecticide resistance-associated mutations in insect acetylcholinesterase from RNA-Seq da¬ta. BMC bioinformatics. 18(1): 330.
49. Binyang AJ, Elanga-Ndille E, Tene-Fossog B, Ndo C, Nouage L, Assatse T, Fotso-Toguem Y, Tabue R, Zeukeng F, Nguiffo DN, Etang J (2022) Distribution of ac¬etylcholinesterase (Ace-1R) target-site G 119S mutation and resistance to carba¬mates and organophosphates in Anophe¬les gambiae sensu lato populations from Cameroon. Parasit Vectors. 15(1): 53.
50. Keïta M, Kané F, Thiero O, Traoré B, Zeukeng F, Sodio AB, Traoré SF, Djouaka R, Doumbia S, Sogoba N (2020) Ace¬tylcholinesterase (ace-1R) target site mu¬tation G119S and resistance to carba¬mates in Anopheles gambiae (sensu lato) populations from Mali. Parasit Vectors. 13(1): 283.
51. Chabi J, Baidoo PK, Datsomor AK, Okyere D, Ablorde A, Iddrisu A, Wilson MD, Dadzie SK, Jamet HP, Diclaro JW (2016) Insecticide susceptibility of natural pop¬ulations of Anopheles coluzzii and Anoph¬eles gambiae (sensu stricto) from Okyereko irrigation site, Ghana, West Africa. Para-sit Vectors. 9: 182.
52. Sy O, Sarr P, Assogba B, Ndiaye M, Dia A, Ndiaye A (2021) Detection of Kdr and Ace-1 mutations in wild populations of Anopheles arabiensis and An. melas in a residual malaria transmission area of Sen¬egal. Pestic Biochem Physiol. 173: 104783.
53. Liebman KA, Pinto J, Valle J, Palomino M, Vizcaino L, Brogdon W, Lenhart A (2015) Novel mutations on the ace-1 gene of the malaria vector Anopheles albimanus pro¬vide evidence for balancing selection in an area of high insecticide resistance in Peru. Malar J. 14: 74.
54. Tmimi F-Z, Faraj C, Bkhache M, Mounaji K, Failloux AB, Sarih Mh (2018) In-secticide resistance and target site muta-tions (G119S ace-1 and L1014F kdr) of Culex pipiens in Morocco. Parasit Vec-tors. 11(1): 51.
55. Ibrahim SS, Ndula M, Riveron JM, Irving H, Wondji CS (2016) The P450 CYP 6Z1 confers carbamate/pyrethroid cross‐re¬sistance in a major African malaria vec¬tor beside a novel carbamate‐insensitive N485I acetylcholinesterase‐1 mutation. Molec Eco. 25(14): 3436–3452.
56. Hasmiwati H, Rusjdi SR, Nofita E (2018) Detection of Ace-1 gene with insec¬ti-cides resistance in Aedes aegypti popula-tions from DHF-endemic areas in Pa-dang, Indonesia. J Biolo Divers. 19(1): 31–36.
57. Elanga-Ndille E, Nouage L, Ndo C, Bin-yang A, Assatse T, Nguiffo-Nguete D, Djonabaye D, Irving H, Tene-Fossog B, Wondji CS (2019) The G119S acetylcho¬linesterase (Ace-1) target site mutation confers carbamate resistance in the major malaria vector Anopheles gambiae from Cameroon: a challenge for the coming IRS Implementation. Genes. 10(10): 790.
| Files | ||
| Issue | Vol 17 No 3 (2023) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v17i3.14987 | |
| Keywords | ||
| Anopheles stephensi Malaria Insecticide resistance mechanism Bendiocarb Iran | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Badzohre A, Oshaghi MA, Enayati AA, Moosa- Kazemi SH, Nikookar SH, Talebzadeh F, Naseri-Karimi N, Hanafi-Bojd AA, Vatandoost H. Ace-1 Target Site Status and Metabolic Detoxification Associated with Bendiocarb Resistance in the Field Populations of Main Malaria Vector, Anopheles stephensi in Iran. J Arthropod Borne Dis. 2024;17(3):272–286.
