Molecular evidence of potential albendazole-resistance in Teladorsagia circumcincta in Iraqi sheep

Authors

  • Yousef Mirzaei Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran; Department of Medical Biochemical Analysis, Cihan University-Erbil, Kurdistan Region, Iraq https://orcid.org/0000-0002-0160-2412
  • Mohammad Yakhchali Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
  • Karim Mardani Faculty of Science, University of Melbourne, Melbourne, Australia https://orcid.org/0000-0002-2327-0535

DOI:

https://doi.org/10.17420/ap7003.534

Keywords:

Teladorsagia circumcincta, albendazole, sheep, Soran, Iraq

Abstract

Gastrointestinal nematodes infection is one of the major health problems in the livestock industry in many parts of the world and Iraq. Anthelmintic drugs are heavily relied upon to control them so that repeated use lead to development of anthelmintic resistance. The present study was carried out to detect the albendazole-resistance in Teladorsagia circumcincta from Iraqi sheep in Soran district, Kurdistan Region. A total of 140 sheep abomasa were randomly collected. Allele-specific PCR (ASP) was used to investigate the frequency of single nucleotide polymorphisms (SNPs) in codon 200 of isotype I β-tubulin gene. The frequency of the homozygous susceptible (SS), homozygous resistant (rr) and heterozygous susceptible (Sr) were 60.9%, 0.0% and 39.1% in the examined T. circumcincta isolates, respectively. From the results of the present study, it was concluded that T. circumcincta was sensitive to albendazole however; the presence of resistance allele in some populations may lead to the emergence of resistant individuals in the region.

References

Githigia S., Thamsborg S., Munyua W., Maingi N. 2001. Impact of gastrointestinal helminths on production in goats in Kenya. Small Ruminant Research 42: 21–29. https://doi.org/10.1016/S0921-4488(01)00240-1

Roeber F., Aaron A.R., Gasser R.B. 2013. 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 6: 1–13. https://doi.org/10.1186/1756-3305-6-153

Sharma D., Vatsya S., Kumar R.R. 2016. Impact of treatment of gastrointestinal nemathelminths on body weight of sheep and goats. Journal of Parasitic Diseases 40: 801–804. https://doi.org/10.1007/s12639-014-0581-9

Taylor M.A., Coop R.L., Wall R.L. 2015. Veterinary parasitology. 4th ed., John Wiley & Sons.

Nemati R., Bahari A., Mahmoodi P., Sazmand A. 2019. Molecular study of benzimidazole resistance in Teladorsagia circumcincta isolated from sheep in North of Iran. Iranian Journal of Parasitology 14: 646.

Stear M.J., Piedrafita D., Sloan S., Alenizi D., Cairns C., Jenvey C. 2019. Teladorsagia circumcincta. Wiki Journal of Science 2(1): 4. https://doi.org/10.15347/WJS/2019.004

Elseadawy R., Abbas I., Al-Araby M., Hildreth M.B., Abu-Elwafa S. 2019. First evidence of Teladorsagia circumcincta infection in sheep from Egypt. Journal of Parasitology 105: 484-490.

Stear M.J., Bishop S.C., Henderson N.G., Scott I. 2003. A key mechanism of pathogenesis in sheep infected with the nematode Teladorsagia circumcincta. Animal Health Research Reviews 4(1): 45–52. https://doi.org/10.1079/AHRR200351

Sargison N., Wilson D., Bartely D., Penny C., Jackson F. 2007. Haemonchosis and Teladorsagiosis in a Scottish sheep flock putatively associated with the overwintering of hypobiotic fourth stage larvae. Veterinary Parasitology 147: 326–331. https://doi.org/10.1016/j.vetpar.2007.04.011

Jabbar A., Iqbal Z., Kerboeuf D., Muhammad G., Khan M.N., Afaq M. 2006. Anthelmintic resistance: the state of play revisited. Life Sciences 79: 2413–2431. https://doi.org/10.1016/j.lfs.2006.08.010

Keegan J.D., Good B., De Waal T., Fanning J., Keane O.M. 2017. Genetic basis of benzimidazole resistance in Teladorsagia circumcincta in Ireland. Irish Veterinary Journal 70: 1–4. https://doi.org/10.1186/s13620-017-0087-8

Samson-Himmelstjerna G., Blackhall W., McCarthy J., Skuce P. 2007. Single nucleotide polymorphism (SNP) markers for benzimidazole resistance in veterinary nematodes. Parasitology 134: 1077–1086. https://doi.org/10.1017/S0031182007000054

Gaudet M., Fara A.G., Beritognolo I., Sabatti M. 2009. Allele-specific PCR in SNP genotyping: Single Nucleotide Polymorphisms. Methods in Molecular Biology 578: 415–424. https://doi.org/10.1007/978-1-60327-411-1_26

Papadopoulos E., Gallidis E., Ptochos S. 2012. Anthelmintic resistance in sheep in Europe: a selected review. Veterinary Parasitology 189: 85–88. https://doi.org/10.1016/j.vetpar.2012.03.036

Mustafa S.I., Schwarzacher T., Heslop-Harrison J. 2018. Complete mitogenomes from Kurdistani sheep: abundant centromeric nuclear copies representing diverse ancestors. Mitochondrial DNA Part A 29: 1180–1193. https://doi.org/10.1080/24701394.2018.1431226

Humbert J.F., Elard L. 1997. A simple PCR method for rapidly detecting defined point mutations. Technical Tips Online 2: 48–49. https://doi.org/10.1016/S1366-2120(08)70030-8

Elard L., Cabaret J., Humbert J.F. 1999. PCR diagnosis of benzimidazole-susceptibity or-resistance in natural populations of the small ruminant parasite, Teladorsagia circumcincta. Veterinary Parasitology 80: 231–237. https://doi.org/10.1016/S0304-4017(98)00214-3

Al-Farwachi M.K., Mohamed E. 2008. Evaluation the effect of albendazole against nematodes in sheep in Mosul, Iraq. Iraqi Journal of Veterinary Sciences 22: 5–7.

Avramenko R.W., Redman E.M., Melville L., Bartely Y., Wit J., Queiroz C., Bartely D.J., Gilleard J.S. 2019. Deep amplicon sequencing as a powerful new tool to screen for sequence polymorphisms associated with anthelmintic resistance in parasitic nematode populations. International Journal for Parasitology 49: 13–26. https://doi.org/10.1016/j.ijpara.2018.10.005

Esteban-Ballesteros M., Rojo-Vázquez F.A., Skuce P.J., Melville L., González-Lanza C., Martínez- Valladares M. 2017. Quantification of resistant alleles in the β-tubulin gene of field strains of gastrointestinal nematodes and their relation with the faecal egg count reduction test. BMC Veterinary Research 13: 1–8. https://doi.org/10.1186/s12917-017-0992-9

Kaplan R.M., Vidyashankar A.N. 2012. An inconvenient truth: global worming and anthelmintic resistance. Veterinary Parasitology 186: 70–78. https://doi.org/10.1016/j.vetpar.2011.11.048

Traversa D., Von Samson-Himmelstjerna G. 2016. Anthelmintic resistance in sheep gastro-intestinal strongyles in Europe. Small Ruminant Research 135: 75–80. https://doi.org/10.1016/j.smallrumres.2015.12.014

Gárcia C.M.B., Sprenger L.K., Ortiz E.B., Molento M.B. 2016. First report of multiple anthelmintic resistance in nematodes of sheep in Colombia. Anais da Academia Brasileira de Ciências 88: 397–402. https://doi.org/10.1590/0001-3765201620140360

Mickiewicz M., Czopowicz M., Kawecka- Grochocka E., Moroz A., Szaluś-Jordanow O., Várady M., Königová A., Spinu M., Górski P., Bagnicka E. 2020. The first report of multidrug resistance in gastrointestinal nematodes in goat population in Poland. BMC Veterinary Research 16: 1–12. https://doi.org/10.1186/s12917-020-02501-5

Chandrawathani, P., Waller P.J., Adnan M., Höglund J. 2003. Evolution of high-level, multiple anthelmintic resistance on a sheep farm in Malaysia. Tropical Animal Health and Production 35: 17–25. https://doi.org/10.1023/a:1022023620599

Sutherland I.A., Damsteegt A., Miller C.M., Leathwick D. 2008. Multiple species of nematodes resistant to Avermectin and a benzimidazole- levamisole combination on a sheep farm in New Zealand. New Zealand Veterinary Journal 56: 67–70. https://doi.org/10.1080/00480169.2008.36810

Höglund J., Gustafsson K., Ljungström B.L., Engström A., Donnan A., Skuce P. 2009. Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the β-tubulin gene. Veterinary Parasitology 161: 60–68. https://doi.org/10.1016/j.vetpar.2008.12.001

Martínez-Valladares M., Donnan A., Geldhof P., Jackson F., Rojo-Vázquez F.A., Skuce P. 2012. Pyrosequencing analysis of the beta-tubulin gene in Spanish Teladorsagia circumcincta field isolates. Veterinary Parasitology 184: 371–376. https://doi.org/10.1186/s13071-020-04320-x

Shalaby H.A. 2013. Anthelmintics resistance; how to overcome it? Iranian Journal of Parasitology 8: 18.

Elard L., Sauve C., Humbert J. 1998. Fitness of benzimidazole-resistant and-susceptible worms of Teladorsagia circumcincta, a nematode parasite of small ruminants. Parasitology 117: 571–578. https://doi.org/10.1017/s0031182098003436

Silvestre A., Cabaret J., Humbert J.F. 2001. Effect of benzimidazole under-dosing on the resistant allele frequency in Teladorsagia circumcincta (Nematoda). Parasitology 123: 103–111. https://doi.org/10.1017/s0031182001008009

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Published

2025-03-15

How to Cite

Mirzaei, Y., Yakhchali, M., & Mardani, K. (2025). Molecular evidence of potential albendazole-resistance in Teladorsagia circumcincta in Iraqi sheep. Annals of Parasitology, 70(3), 159–164. https://doi.org/10.17420/ap7003.534

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Original papers