Document Type : Original Article

Authors

1 Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

2 Department of Pathobiology,Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

3 Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

Abstract

Pyrethroid insecticides target voltage-gated sodium channels (VGSCs) that are essential for electrical signaling in the nervous system of insects. Three-point mutations at the corresponding amino acid sequence positions M815I, T917I, and L920F located in domain II conferring the knockdown resistance (kdr) are the most important mutations in pyrethroid-resistant lice worldwide. In addition, six new mutations have been reported in the extracellular loops IIS1-2 (H813P) and IIS5 (I927F, L928A, R929V, L930M, L932M) in the α- subunit of the sodium channel in lice. The aim of this study was to detect alleles resistant to pyrethroids in the domain II (S5-S6) of the VGSC gene in goat biting louse. Goat biting lice were collected from five provinces in the west and northwest of Iran. Genomic DNA was extracted from goat biting lice and Bovicola (Damalinia) caprae species was confirmed by amplifying the cytochrome oxidase subunit I (COXI) gene. A fragment in the domain II (S5-S6) of the VGSC gene was amplified using the specific primers and the resultant polymerase chain reaction products were sequenced. Substitutions T917I, L920F, I927F, L928A, R929V and L930M were identified in the examined sequences. The results showed that all the examined lice had at least one mutation in their VGSC gene associated with pyrethroid resistance or new mutations. The presence of these mutated alleles in the VGSC gene may be due to the long-term and multiple use of pyrethroids against arthropods. Thus, the molecular detection of resistance to pyrethroid insecticides in goat chewing lice can help plot a kdr frequency map to enact effective policies to control caprine pediculosis.

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Main Subjects

  1. Syamsul VS, Okene IA, Yahya SN, et al. Prevalence of ectoparasitism on small ruminants in Kelantan, Malaysia. Trop Life Sci Res 2020; 31(1): 45-56.
  2. Ajith Y, Dimri U, Singh SK, et al. Lice induced immuno-oxidative wreckage of goats. Vet Parasitol 2017; 242: 24-30.
  3. Ajith Y, Dimri U, Gopalakrishnan A, et al. A field study on the efficacy of ivermectin via subcutaneous route against chewing lice (Bovicola caprae) infestation in naturally infested goats. Onderstepoort J Vet Res 2019; 86(1): e1-e5.
  4. Meguini MN, Righi S, Zeroual F, et al. Inventory of lice of mammals and farmyard chicken in North-eastern Algeria. Vet World 2018; 11(3): 386-396.
  5. Bass C, Schroeder I, Turberg A, et al. Identification of mutations associated with pyrethroid resistance in the para-type sodium channel of the cat flea, Ctenocephalides felis. Insect Biochem Mol Biol 2004; 34(12): 1305-1313.
  6. Mckiernan F, O’Connor J, Minchin W, et al. A pilot study on the prevalence of lice in Irish beef cattle and the first Irish report of deltamethrin tolerance in Bovicola bovis. Ir Vet J 2021; 74: 20.doi:1186/s13620-021-00198-y.
  7. Narahashi T. Neuronal ion channels as the target sites of insecticides. J Pharmacol Toxicol 1996; 79(1): 1-14.
  8. Catterall WA. From ionic currents to molecular mechanisms: the structure and function of voltage- gated sodium channels. Neuron 2000; 26(1): 13-25.
  9. Soderlund DM, Bloomquist JR. Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 1989; 34: 77-96.
  10. Rinkevich FD, Du Y, Dong K. Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic Biochem Physiol 2013; 106(3): 93-100.
  11. Singh OP, Dykes CL, Sharma G, et al. L1014F-kdr mutation in Indian Anopheles subpictus (Diptera: Culicidae) arising from two alternative transversions in the voltage-gated sodium channel and a single PIRA-PCR for their detection. J Med Entomol 2015; 52(1): 24-27.
  12. Fabro J, Sterkel M, Capriotti N, et al. Identification of a point mutation associated with pyrethroid resistance in the para-type sodium channel of Triatoma infestans, a vector of Chagas’ disease. Infect Genet Evol 2012; 12(2): 487-491.
  13. Yoon KS, Kwon DH, Strycharz JP, et al. Biochemical and molecular analysis of deltamethrin resistance in the common bed bug (Hemiptera: Cimicidae). J Med Entomol 2008; 45(6): 1092-1101.
  14. Rosario-Cruz R, Guerrero FD, Miller RJ, et al. Molecular survey of pyrethroid resistance mechanisms in Mexican field populations of Rhipicephalus (Boophilus) microplus. Parasitol Res 2009; 105(4): 1145-1153.
  15. Liu Z, Valles SM, Dong K. Novel point mutations in the German cockroach para sodium channel gene are associated with knockdown resistance (kdr) to pyrethroid insecticides. Insect Biochem Mol Biol 2000; 3(10): 991-997.
  16. Gellatly KJ, Krim S, Palenchar DJ, et al. Expansion of the knockdown resistance frequency map for human head lice (Phthiraptera: Pediculidae) in the United States using quantitative sequencing. J Med Entomol 2016; 53(3): 653-659.
  17. Rust MK, Vetter R, Denholm I, et al. Susceptibility of adult cat fleas (Siphonaptera: Pulicidae) to insecticides and status of insecticide resistance mutations at the Rdl and knockdown resistance loci. Parasitol Res 2015; 114(Suppl 1): S7-S18.
  18. Eremeeva ME, Capps D, Winful EB, et al. Molecular markers of pesticide resistance and pathogens in human head lice (Phthiraptera: Pediculidae) from rural Georgia, USA. J Med Entomol 2017; 54(4): 1067-1072.
  19. Lee SH, Gao JR, Yoon KS, et al. Sodium channel mutations associated with knockdown resistance in the human head louse, Pediculus capitis (De Geer). Pestic Biochem Physiol 2003; 75(3): 79-91.
  20. Wall RL, Shearer D. Veterinary ectoparasites: biology, pathology and control. 2nd New Jersey, USA: John Wiley & Sons 2008; 167-173.
  21. Rafyi A, Rak H. Parasitology of arthropods (entomology) [Persian]. Tehran, Iran: Tehran University Perss 1985; 266-267.
  22. Folmer O, Black M, Hoeh W, et al. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994; 3(5): 294- 299.
  23. Toloza AC, Ascunce MS, Reed D, et al. Geographical distribution of pyrethroid resistance allele frequency in head lice (Phthiraptera: Pediculidae) from Argentina. J Med Entomol 2014; 51(1): 139-144.
  24. Tamura K, Stecher G, Peterson D, et al. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30(12): 2725-2729.
  25. Garg SK, Katoch R, Bhushan C. Efficacy of flumethrin pour-on against Damalinia caprae of goats (Capra hircus). Trop Anim Health Prod 1998; 30(5): 273-278.
  26. Kasai S, Ishii N, Natsuaki M, et al. Prevalence of kdr-like mutations associated with pyrethroid resistance in human head louse populations in Japan. J Med Entomol 2009; 46(1): 77-82.
  27. Firooziyan S, Sadaghianifar A, Taghilou B, et al. Identification of novel voltage-gated sodium channel mutations in human head and body lice (Phthiraptera: Pediculidae). J Med Entomol 2017; 54(5): 1337-1343.
  28. Kristensen M. Identification of sodium channel mutations in human head louse (Anoplura: Pediculidae) from Denmark. J Med Entomol 2005; 42(5): 826-829.
  29. Kristensen M, Knorr M, Rasmussen AM, et al. Survey of permethrin and malathion resistance in human head lice populations from Denmark. J Med Entomol 2006; 43(3): 533-538.
  30. Durand R, Bouvresse S, Andriantsoanirina V, et al. High frequency of mutations associated with head lice pyrethroid resistance in schoolchildren from Bobigny, France. J Med Entomol 2011; 48(1): 73-75.
  31. Yoon KS, Gao JR, Lee SH, et al. Permethrin-resistant human head lice, Pediculus capitis, and their treatment. Arch Dermatol 2003; 139(8): 994-1000.
  32. Lee SH, Yoon KS, Williamson MS, et al. Molecular analysis of kdr-like resistance in permethrin-resistant strains of head lice, Pediculus capitis. Pestic Biochem Physiol 2000; 66(2): 130-143.
  33. Drali R, Benkouiten S, Badiaga S, et al. Detection of a knockdown resistance mutation associated with permethrin resistance in the body louse Pediculus humanus corporis by use of melting curve analysis genotyping. J Clin Microbiol 2012; 50(7): 2229-2233.
  34. Kwon DH, Yoon KS, Strycharz JP, et al. Determination of permethrin resistance allele frequency of human head louse populations by quantitative sequencing. J Med Entomol 2008; 45(5): 912-920.
  35. Schuler TH, Martinez-Torres D, Thompson AJ, et al. Toxicological, electrophysiological, and molecular characterisation of knockdown resistance to pyrethroid insecticides in the diamondback moth, Plutella xylostella (L.). Pestic Biochem Physiol 1998; 59(3): 169-182.
  36. Gao JR, Yoon KS, Lee SH, et al. Increased frequency of the T929I and L932F mutations associated with knockdown resistance in permethrin-resistant populations of the human head louse, Pediculus capitis, from California, Florida, and Texas. Pestic Biochem Physiol 2003; 77(3): 115-124.
  37. Thomas DR, McCarroll L, Roberts R, et al. Surveillance of insecticide resistance in head lice using biochemical and molecular methods. Arch Dis Child 2006; 91(9): 777-778.
  38. Ghavami MB, Haghi FP, Alibabaei Z, et al. First report of target site insensitivity to pyrethroids in human flea, Pulex irritans (Siphonaptera: Pulicidae). Pestic Biochem Physiol 2018; 146: 97-105.