Short Communication

Molecular Study of Benzimidazole Resistance in Teladorsagia circumcincta Isolated from Sheep in North of Iran


Background: Resistance to benzimidazole (BZ) compounds is common in Teladorsagia circumcincta populations in sheep and goats worldwide. Given the importance of anthelmintic resistance and shortage of information on single nucleotide polymorphisms (SNPs) in this prevalent nematode in Iran, this study was conducted.

Methods: From June to September 2016, abomasa of 139 sheep of different sexes and ages in Amol City slaughterhouse, northern Iran were examined for isolation of nematodes. Totally 45 male T. circumcincta confirmed by both microscopical and nested-PCR-RFLP methods were included in this study. Susceptibility or resistance of each single T. circumcincta worm to benzimidazoles was assessed using allele-specific PCR.

Results: Frequency of genotypes in the present study were 33.33% heterozygote BZ and 66.67% BZ homozygote sensitive. No homozygote resistant worm was found.

Conclusion: Resistance against BZs in T. circumcincta of sheep has occurred at a low prevalence in the north of Iran. However, mutated genes might get dominant under drug selection in future. Hence, periodic investigations for early detection of mutated alleles in nematode populations using accurate and sensitive molecular methods such as PCR-RFLP is recommended.

Roeber F, Jex AR, Gasser RB. Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance-an Australian perspective. Parasites & Vectors. 2013;6(1):153.

Furtado LFV, de Paiva Bello ACP, Rabelo ÉML. Benzimidazole resistance in helminths: from problem to diagnosis. Acta Trop. 2016;162:95-102.

Shalaby HA. Anthelmintics resistance; how to overcome it? Iran J Parasitol. 2013;8(1):18-32.

Kaplan RM, Vidyashankar AN. An inconvenient truth: global worming and anthelmintic resistance. Vet Parasitol. 2012;186(1-2):70-8.

Eslami A, Nabavi L. Species of gastro-intestinal nematodes of sheep from Iran. Bull Soc Pathol Exot. 1976;69(1):92-5.

Eslami A, Meydani M, Maleki S, Zargarzadeh A. Gastrointestinal nematodes of wild sheep (Ovis orientalis) from Iran. J Wildl Dis. 1979;15(2):263-5.

Skerman KD, Shahlapoor AA, Eslami AH, Eliazian M. Observations on the incidence, epidemiology, control and economic importance of gastro-intestinal parasites of sheep and goats in Iran. Arch Razi Inst. 1970;22:187-96.

Eslami A, Rahbari S, Nikbin S. Gastro-intestinal nematodes of gazelle, Gazella subgutturosa, in Iran. Vet Parasitol. 1980;7:75-8.

Sazmand A, Joachim A. Parasitic diseases of camels in Iran (1931-2017)- A literature review. Parasite. 2017;24:21.

Gholamian A, Eslami A, Nabavi L, Rasekh AR. A field survey on resistance of gasterointestinal nematodes to levamisole in sheep in Khuzestan province of lran. J Fac Vet Med Uni Tehran. 2006;61(1):7-13. [In Persian with English summary].

Gholamian A, Eslami A, Nabavi L, Rasekh AR, Galedari H. A field survey on resistance to albendazole in gasterointestinal nematodes of sheep in Khozestan province of Iran. J Fac Vet Med Uni Tehran. 2007;62(1):45-51. [In Persian with English summary].

Gholamian A, Eslami A, Nabavi L, Rasekh AR, Galedari H. A survey on drug resistance in gastrointestinal nematodes of sheep using larval development assay. Iran Vet J. 2008;4(3):48-57.

Leignel V, Cabaret J. Massive use of chemotherapy influences life traits of parasitic nematodes in domestic ruminants. Funct Ecol. 2001;15(5):569-74.

Silvestre A, Cabaret J. Mutation in position 167 of isotype 1 β-tubulin gene of Trichostrongylid nematodes: role in benzimidazole resistance? Mol Biochem Parasitol. 2002;120(2):297-300.

Elard L, Humbert J. Importance of the mutation of amino acid 200 of the isotype 1 β-tubulin gene in the benzimidazole resistance of the small-ruminant parasite Teladorsagia circumcincta. Parasitol Res. 1999;85(6):452-6.

Ghisi M, Kaminsky R, Mäser P. Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Vet Parasitol. 2007;144(3):313-20.

Keegan JD, Good B, de Waal T, Fanning J, Keane OM. Genetic basis of benzimidazole resistance in Teladorsagia circumcincta in Ireland. Irish Vet J. 2017;70(1):8.

Nabavi R, Shayan P, Shokrani H, Eslami A, Bokaie S. Evaluation of benzimidazole resistance in Haemonchus contortus using comparative PCR-RFLP methods. Iran J Parasitol. 2011;6(2):45-53.

Shokrani H, Shayan P, Eslami A, Nabavi R. Benzimidazole-resistance in Haemonchus contortus: new PCR-RFLP method for the detection of point mutation at codon 167 of isotype 1 β-tubulin gene. Iran J Parasitol. 2012;7(4):41-8.

Gholamian A, Galehdari H, Eslami A, Nabavi L. Study of β-tubulin gene polymorphisms in Haemonchus contortus isolated from sheep populations in Khouzestan, southwestern Iran. Iran J Vet Res. 2007;8(3):239-43.

Shayan P, Borji H, Eslami A, Zakeri S. Isolation of DNA from a single helminth using new developed kit in Iran and its PCR analysis. Iran J Parasitol. 2007;2(2):34-9.

Shayan P, Eslami A, Borji H. Innovative restriction site created PCR-RFLP for detection of benzimidazole resistance in Teladorsagia circumcincta. Parasitol Res. 2007;100(5):1063-8.

Silvestre A, Humbert J-F. A molecular tool for species identification and benzimidazole resistance diagnosis in larval communities of small ruminant parasites. Exp Parasitol. 2000;95(4):271-6.

Humbert J-F, Elard L. A simple PCR method for rapidly detecting defined point mutations. Technic Tips Online. 1997;2(1):48-9.

Maghami G, Alavi A, Khalili K. Monieziose des ovins en Iran et son traitement par l'arseniate de plomb. Arch Razi Inst. 1959;11(1):44-7.

Shahlapour A, Eslami A, Eliazian H. Comparative anthelmintic tests in sheep and goats infected with gastro-intestinal nematodes and lungworms in Iran. Trop Anim Health Prod. 1970;2(4):223-34.

Eslami A. Efficacy of ivermectin against Setaria digitata in cattle. J Vet Parasitol. 1998;12(1):58-9.

Hosseini SH, Eslami A, Safari M. Evaluation of antihelminte efficacy of ivermectin against gastrointestinal nematods with emphasis on Bunostomum trigonocephalum in naturally infected sheep. Fac Vet Med Uni Tehran. 2000;55(1):39-41. [In Persian with English summary].

Leignel V, Silvestre A, Humbert J-F, Cabaret J. Alternation of anthelmintic treatments: a molecular evaluation for benzimidazole resistance in nematodes. Vet Parasitol. 2010;172(1):80-8.

Falzon LC, O’neill T, Menzies P, Peregrine A, Jones-Bitton A, Mederos A. A systematic review and meta-analysis of factors associated with anthelmintic resistance in sheep. Prev Vet Med. 2014;117(2):388-402.

Hosseinzadeh S, Rafat S, Moghaddam G, Shodja J, Nematollahi A, Shamsuddin M, et al. Microsatellite polymorphism in DRB2 gene and its relation to Haemonchus contortus parasites fecal egg count in Iranian Ghezel sheep. Iran J Ruminant Health Res. 2016;1(1):31-9.

Valilou RH, Rafat SA, Notter DR, Shojda D, Moghaddam G, Nematollahi A. Fecal egg counts for gastrointestinal nematodes are associated with a polymorphism in the MHC-DRB1 gene in the Iranian Ghezel sheep breed. Front Genetics. 2015;6:105.

Nabavi R, Eslami A, Shorkani HR, Bokaei S, Shayan P, Saadati D. Study on the prevalence, intensity, seasonal dynamics of abomasal helminths in sheep from different climatic zones of Iran. World Appl Sci J. 2011;12(4):441-5.

Sazmand A, Eigner B, Mirzaei M, Hekmatimoghaddam S, Harl J, Duscher GG, et al. Molecular identification of hemoprotozoan parasites in camels (Camelus dromedarius) of Iran. Iran J Parasitol. 2016;11(4):568-73.

Walker JG, Morgan ER. Generalists at the interface: nematode transmission between wild and domestic ungulates. Int J Parasitol Parasites Wildl. 2014;3:242–50.

Kaminsky R, Ducray P, Jung M, Clover R, Rufener L, Bouvier J, et al. A new class of anthelmintics effective against drug-resistant nematodes. Nature. 2008;452(7184):176.

Scott I, Pomroy W, Kenyon P, Smith G, Adlington B, Moss A. Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Vet Parasitol. 2013;198(1-2):166-71.

Bartley D, Devin L, Nath M, Morrison A. Selection and characterisation of monepantel resistance in Teladorsagia circumcincta isolates. Int J Parasitol Drugs Drug Resist. 2015;5(2):69-76.

Vercruysse J, Charlier J, Van Dijk J, Morgan ER, Geary T, von Samson-Himmelstjerna G, et al. Control of helminth ruminant infections by 2030. Parasitology. 2018:1-10.

IssueVol 14 No 4 (2019) QRcode
SectionShort Communication(s)
Sheep Anthelmintic resistance Teladorsagia Single nucleotide poly-morphism SNP β-tubulin

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
NEMATI R, BAHARI A, MAHMOODI P, SAZMAND A. Molecular Study of Benzimidazole Resistance in Teladorsagia circumcincta Isolated from Sheep in North of Iran. Iran J Parasitol. 2019;14(4):646-651.