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Influence of sustained deworming pressure on the anthelmintic resistance status in strongyles of sheep under field conditions

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Abstract

Anthelmintic resistance (AR) status in Madras Red sheep from selected field flocks of a government funded scheme, covered by regular, sustained anthelmintic treatment for more than 10 years was determined. Parameters such as fecal egg count reduction test (FECRT), larval paralysis assay (LPA), and allele-specific-PCR (AS-PCR) were used to test the efficacy of fenbendazole, tetramisole, and ivermectin at recommended doses, in two seasons. Sheep belonging to non-beneficiary farmers were used as controls. Mean FECRT values of beneficiary group during winter and summer seasons were 77.77 and 76.04, 93.65 and 92.12, and 95.37 and 98.06 %, respectively, for fenbendazole, tetramisole, and ivermectin. In the non-beneficiary groups, the corresponding values were 74.82 and 81.09 %, 96.05 and 97.40 %, and 97.26 and 98.23 %, respectively. The results revealed resistance to fenbendazole, suspect resistance to tetramisole and susceptibility to ivermectin in beneficiary flock. In non-beneficiary flock, while resistance was noticed against fenbendazole, both tetramisole and ivermectin were effective. FECR values were found to be significantly different between beneficiary and non-beneficiary groups against tetramisole. The results of LPA confirmed this finding, as 50 % of the Haemonchus contortus larvae were paralyzed at the concentration of 0.0156 μg/ml in the beneficiary group, while those of non-beneficiary groups required lower concentrations of 0.0078 μg/ml. AS-PCR revealed the predominance of heterozygous susceptible population of H. contortus in the beneficiary group. In this study, resistance to fenbendazole was confirmed in both the beneficiary and non-beneficiary groups and this could be attributed to frequent use of benzimidazoles as seen from the deworming records. Emergence of tetramisole resistance was detected in the beneficiary group, where the drug was used continuously for 4 years. Ivermectin was found to be effective in all the flocks. It is recommended that the practice of routine deworming of three to four times a year should be avoided, as it can lead to emergence of anthelmintic resistance.

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References

  • Amulya, G., Sudharani, R., Ismail Shareef, M. and Gopinath, S.M., 2015. Anthelmintics and anthelmintic resistance against gastrointestinal nematodes of small ruminants. Indian Journal of Veterinary and Animal Sciences Research, 44, 67 - 77.

    Google Scholar 

  • Anon., 2004. Annual progress report: All India Network Program on Gastrointestinal Parasitism, CSWRI, Avikanagar, pp. 1–45.

    Google Scholar 

  • Bal, M.S., Mahajan, V., Verma Alka, S. and Sharma, S., 2007. Outbreak of parasitic gastroenteritis in sheep and goats. Journal of Veterinary Parasitology, 21, 93-95.

    Google Scholar 

  • Bowman, D.D., 2014. Georgis’ Parasitology for Veterinarians (10th edn). Elsevier Health Sciences, PP: 302.

  • Busin, V., Kenyon, F., Parkin, T., McBean, D., Laing, N., Sargison, N.D. and Ellis, K., 2014. Production impact of a targeted selective treatment system based on live weight gain in a commercial flock. Veterinary, 200, 248-52.

    Article  CAS  Google Scholar 

  • Butter, B.S., Rai, H.S., Singh, N.K., Jyoti, Haque, M. and Rath, S.S., 2012. Emergence of anthelmintic resistance in an organized sheep farm in Punjab. Journal of Veterinary Parasitology 26, 69-71.

    Google Scholar 

  • Chandra, S., Prasad, A., Sankar, M., Yadav, N. and Dalal, S., 2014. Molecular diagnosis of benzimidazole resistance Haemonchus contortus in sheep from different geographic regions of North India. Veterinary World 7: 337-341.

    Article  CAS  Google Scholar 

  • Chaudhri, S.S., Gupta, S. K. and Bisla, R.S., 2007. Resistance of gastrointestinal nematodes to tetramisole hydrochloride, morantel tartrate and fenbendazole in sheep of Haryana. Journal of Veterinary Parasitology. 21, 113-115.

    Google Scholar 

  • Coles, G.C., Bauer, C., Borgsteede, F.H.M., Geerts, S., Klei, T.R., Taylor, M.A. and Waller, P.J., 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Journal of Veterinary Parasitology, 44, 35-44.

    Article  CAS  PubMed  Google Scholar 

  • Coles, G.C., Jackson, F., Pomroy, W.E., Prichad, R.K., George von Samson- Himmelstjerna, Silvestre, A., Taylor, M.A. and Vercruysse, J., 2006. The detection of anthelmintic resistance in nematodes of veterinary importance. Journal of Veterinary Parasitology, 136, 167-185.

    Article  CAS  PubMed  Google Scholar 

  • Das, M., and S. Singh, 2005. Anthelmintic resistance to nematodes in sheep and goat farms in Hisar. Journal of Veterinary Parasitology, 19, 103-106.

    Google Scholar 

  • Easwaran, C., Harikrishnan, T.J. and Raman, M., 2009. Multiple anthelmintic resistance in GI nematodes of sheep in South India. Veterinarski Arhiv, 79, 611- 620.

    CAS  Google Scholar 

  • Geurden, T., Chartier, C., Fanke, J., Di Regalbono, A.F., Traversa, D., von Samson-Himmelstierna, G., Demeler, J., Vanimisetti, H.B., Bartram, D.J. and Denwood, M.J., 2014. Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe. International Journal for Parasitology: Drugs and Drug Resistance, 5, 163-171.

    Google Scholar 

  • Gill, B.S., 1996. Anthelmintic resistance in India. Journal of Veterinary Parasitology, 63, 173-176.

    Article  CAS  PubMed  Google Scholar 

  • Holsback, L., Luppi, P.A.R., Silva, C.S., Negrao, G.K., Conde, G., Gabriel, V.H., Balestrieri, J.V. and Tomazella, L., 2016. Anthelmintic efficiency of doramectin, fenbendazole, and nitroxynil, in combination or individually, in sheep worm control. Brazilian Journal of Veterinary Parasitology. Doi: 10.1590/S1984-29612016025 .

    PubMed  Google Scholar 

  • Humbert, J.F., Cabaret, J., Elard, L., Leignel, V. and Silvestre, A., 2001. Molecular approaches to studying benzimidazole resistance in trichostrongylid nematode parasites of small ruminants. Journal of Veterinary Parasitology, 101, 405-414.

    Article  CAS  PubMed  Google Scholar 

  • Jaiswal, A.K., Sudan, V., Shanker, D. and Kumar, P., 2013. Emergence of ivermectin resistance in gastrointestinal nematodes of goats in a semi-organized farm of Mathura district, India. Veterinarski Arhiv, 83, 275-280.

    CAS  Google Scholar 

  • MAFF, 1971. Manual of veterinary parasitological laboratory techniques. Ministry of Agriculture, Fisheries and Food, Technical Bulletin, HMSO, London, pp. 36-42.

    Google Scholar 

  • Maharshi, A.K., Swarnkar, C.P., Singh, D., Manohar, G.S. and Ayub, M., 2011. Status of anthelmintic resistance in gastrointestinal nematodes of sheep in Rajasthan, Indian Journal of Animal Sciences, 81, 105-109.

    Google Scholar 

  • Manikkavasagan, I., Bino Sundar, S.T. and Raman, M., 2013. Survey on anthelmintic resistance to gastrointestinal nematodes in unorganized goat farms of Tamil Nadu. Journal of Parasitic Diseases, 37, 1-3.

    Google Scholar 

  • Martin, P.J. and Le Jambre, L.F., 1979. Larval paralysis as an in vitro assay of levamisole and morantel tartrate resistance in Ostertagia spp. Veterinary Science Communications, 3, 159-164.

    Article  Google Scholar 

  • Moredun Research Institute (SOP), 2000. Laboratory techniques for the diagnosis, culture and identification of nematodes infecting small ruminants, U. K.

  • Palcy, C., Silvestre, A., Sauve, C., Cortet, J. and Cabaret, J., 2010. Benzimidazole resistance in Trichostrongylus axei in sheep: long-term monitoring of affected sheep and genotypic evaluation of the parasite. The Veterinary Journal, 183, 68-74.

    Article  CAS  PubMed  Google Scholar 

  • Pape, M., Posedi, J., Failing, K., Schnieder, T. and Von Samson-Himmelstierna, G., 2003. Analysis of the beta-tubulin codon 200 genotype distribution in a benzimidazole-susceptible and resistant cyathostome population. Journal of Parasitology, 127, 53-59.

    Article  CAS  Google Scholar 

  • Redman, E., Whitelaw, F., Tait, A., Burgess, C., Bartley, Y., Skuce, P., Jackson, F. and Gilleard, J., 2015. The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps. PLOS Neglected Tropical Diseases, 9: e0003494.

    Article  PubMed  PubMed Central  Google Scholar 

  • Silvestre, A. and Humbert, J.F., 2000. A molecular tool for species identification and benzimidazole resistance diagnosis in larval communities of small ruminant parasites. Experimental Parasitology, 95, 271-276.

    Article  CAS  PubMed  Google Scholar 

  • Soulsby, E.J.L., 1982. Helminth, arthropods and protozoa of domesticated animals. 7th Edition. ELBS and Bailliere Tindall, London. pp 227.

    Google Scholar 

  • Swarnkar, C.P. and Singh, D., 2010. Worm-control practices, anthelmintic use and its implication on anthelmintic resistance in gastrointestinal nematodes of sheep in Rajasthan. The Indian Journal of Animal Sciences, 80, 593-600.

    Google Scholar 

  • Swarnkar, C.P., Khan, F.A., Singh, D. and Bhagwan, P.S.K., 1999. Further studies on anthelmintic resistance in sheep at an organized farm in arid region of Rajasthan. Journal of Veterinary Parasitology, 82, 81 – 84.

    Article  CAS  PubMed  Google Scholar 

  • Tiwari, J., Kolte, A.P., Kumar, S., Swarnkar, C.P., Singh, D. and Pathak, K.M.L., 2007. Diagnosis of benzimidazole resistance in Haemonchus contortus in sheep by allele specific PCR. Asian-Australian Journal of Animal Sciences, 20, 7-11.

    Article  CAS  Google Scholar 

  • Van Wyk, J.A. and Mathew, E., 2013. Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical guide. Onderstepoort Journal of Veterinary Research, 80, 1-14.

    Google Scholar 

  • Varshney, T.R. and Singh, Y.P., 1976. A note on development of resistance of Haemonchus contortus worm against phenothiazine and thiabendazole in sheep. The Indian Journal Animal Sciences, 46, 666-668.

    CAS  Google Scholar 

  • Yadav, P. and Singh, R., 2011. A review on anthelmintic drugs and their future scope International Journal of Pharmacy and Pharmaceutical Sciences, 3, 17-21.

    Google Scholar 

  • Yadav, C.L., Uppal, R.P. and Kalra, S., 1993. An outbreak of haemonchosis associated with anthelmintic resistance in sheep. International Journal of Parasitology, 23, 411-413.

    Article  CAS  PubMed  Google Scholar 

  • Yadav, C.L., Kumar, R., Uppal, R.P. and Verma, S.P., 1995. Multiple anthelmintic resistance in Haemonchus contortus on a sheep farm in India. Journal of Parasitology, 60, 355-360.

    CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Indian Council of Agricultural Research scheme on Network Project on Sheep Improvement for the logistic assistance and the farmers of the constituent flocks for extending their support. They thank the Director for Centre for Animal Production Studies, TANUVAS, Chennai, for granting permission to carry out the research. The cooperation and help from staff of NWPSI during the study period is acknowledged.

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Correspondence to M. K. Vijayasarathi.

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Vijayasarathi, M.K., Sreekumar, C., Venkataramanan, R. et al. Influence of sustained deworming pressure on the anthelmintic resistance status in strongyles of sheep under field conditions. Trop Anim Health Prod 48, 1455–1462 (2016). https://doi.org/10.1007/s11250-016-1117-3

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