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Anthelmintic Resistance in Nematode Parasites of Sheep in Denmark with Special Emphasis on Levamisole Resistance in Ostertagia circumcincta

Ormemiddelresistens hos fårets parasitiske nematoder i Danmark med særlig vægt på levamisol resistens hos Ostertagia circumcincta

Acta Veterinaria Scandinavica volume 32, pages 145–154 (1991)Cite this article

Abstract

This study was undertaken to elucidate the presence of anthelmintic resistance in nematode parasites of sheep in Denmark. Twenty two flocks of sheep were selected for Faecal Egg Count Reduction (FECR) tests, based on a prior history of either the same anthelmintic, or anthelmintic class having been used 3 times or more over the previous 5 years. Evidence of anthelmintic resistance was detected in 7 flocks. Two flocks showed FECR of 88 % and 94 % after treatment with thiabendazole, FECR of another 2 were 90 % and 94 % following treatment with fenbendazole. Three flocks showed FECR of 73 %, 89 % and 94 %, respectively following the use of levamisole. Ostertagia circumcincta was isolated from 1 of the latter flocks and subjected to an in vivo controlled slaughter assay. Following treatment with levamisole at the recommended dose rate of 7.5 mg/kg, FECR was 44.5 % and worm counts were reduced by 67.7 %. These results were further substantiated by an in vitro egg hatch paralysis assay and by measuring pepsinogen levels in treated and non-treated lambs. This is the first instance of anthelmintic resistance in sheep nematodes in Scandinavia.

Sammendrag

Formålet med denne undersøgelse var at belyse forekomst af ormemiddelresistens hos fårets indvoldsorm i Danmark. Toogtyve fårebesætninger udvalgtes til en feltundersøgelse over ormemiddelresistens under anvendelse af en fækal æg reduktions test (eng. Faecal Egg Count Reduction (FECR) Test). Kriterierne for udvælgelse af besætningerne var, at samme ormemiddel eller ormemidler hørende til samme virkningsgruppe havde været anvendt til mindst 3 årlige behandlinger over en 5-årig periode. Der fandtes indikation på ormemiddelresistens i 7 besætninger. Efter behandling med thiabendazol fandtes FECR i to besætninger til henholdsvis 88 % og 94 %, i andre 2 besætninger var FECR 90 % og 94 % efter behandling med fenbendazol og i 3 besætninger fandtes FECR til 73 %, 89 % og 94 % ved behandling med levamisol. Fra 1 af de sidstnævnte besætninger isoleredes en population af Ostertagia circumcincta, som underkastedes en in vivo kontrolleret undersøgelse over resistens mod levamisol. Ved behandling af denne population med levamisol (7.5 mg/kg) fandtes FECR til 44.5 % og en reduktion i ormebyrden på 67.7 %, mens både ægudskillelse og ormeantallet reduceredes med 100% i en tilsvarende anthelmintisk følsom population. Resultaterne understøttedes af en in vitro egg hatch paralysis test samt af målinger af serumpepsinogen. Dette er det første tilfælde af ormemiddelresistens hos fårets indvoldsorm i Skandinavien.

References

  • Anon.: Report of the Working Party for the Animal Health Commitee of the Standing Commitee on Agriculture: Anthelmintic resistance. Ed. PJ Waller, SCA Technical Report Series – No. 28, CSIRO Australia, East Melbourne.

  • Bauer C, Feige N, Klatte D, Enninga J, Bürger HJ: Felduntersuchungen zur Anthelmintikaresistenz von Trichostrongyliden in hessischen Schafherden. (Field Investigations on Anthelmintic Resistance in Trichostrongyles of Sheep in Hessian Herds). Berl. und Münch. Tierarztl. Wschr. 1988, 101, 185–189.

    CAS  Google Scholar 

  • Bjørn H.: Ormemiddelresistens hos farets parasitiske nematoder. Undersøgelser i Danmark og Tanzania. (Anthelmintic resistance of the parasitic nematodes of sheep. Studies in Denmark and Tanzania). Ph. D. Thesis. Department of Veterinary Microbiology, Royal Veterinary and Agricultural University, Copenhagen, 1988.

  • Bjørn H, Roepstorff A, Nansen P, Waller PJ: A dose-response investigation on the level of resistance to pyrantel citrate on Oesophagostomum quadrispinulatum and Oesophagostomum dentatum of pigs. Vet. Parasitol. 1989, 31, 259–267.

    Article  Google Scholar 

  • Boersema JH, Lewing-Van der Weil PJ, Borgsteede FMH: Benzimidazole resistance in a field strain of Haemonchus contortus in the Netherlands. Vet. Rec. 1982, 110, 203–204.

    Article  CAS  Google Scholar 

  • Boersema JH, Borgsteede FMH, Eysker ME, Hendrikx WML, Jansen J, Mudde P: A survey on the occurrence of benzimidazole resistance in nematodes of sheep in the Netherland. Trop, geograph. Med. 1984, 36, 105.

    Google Scholar 

  • Britt DP: Benzimidazole-resistant nematodes in Britain. Vet. Rec. 1982, 110, 343–344.

    Article  CAS  Google Scholar 

  • Britt DP, Oakley GA: Anthelmintic evaluation of a thiabendazole-resistant strain of Ostertagia circumcincta from sheep in England. Vet. Parasitol. 1986, 19, 95–101.

    Article  CAS  Google Scholar 

  • Cawthorne RJG, Whitehead JD: Isolation of benzimidazole resistant strains of Ostertagia circumcincta from British sheep. Vet. Rec. 1983, 112, 274–277.

    Article  CAS  Google Scholar 

  • Cawthorne RJG, Cheong FH: Prevalence of anthelmintic resistant nematodes in sheep in south-east England. Vet. Rec. 1984, 114, 562–564.

    Article  CAS  Google Scholar 

  • Coles GC, East JM, Jenkins SN: The mechanism of action of the anthelmintic levamisole. Genetic Pharmacol. 1975, 66, 309–313.

    Article  Google Scholar 

  • Dash KM: Differential efficacy of levamisole and oxfendazole against male and female Tricho-strongylus colubriformis. Vet. Rec.. 1985 777, 502–503.

    Google Scholar 

  • Dobson RJ, Donald AD, Waller PJ, Snowdon KL: An egg-hatch assay for resistance to levamisole in trichostrongylid nematode parasites. Parasitol. 1986, 19, 77–84.

    CAS  Google Scholar 

  • Donald AD: The development of anthelmintic resistance in nematodes of grazing animals. In: Facts and Reflections IV. Resistance of Parasites to Anthelmintics. Eds. FHM Borgsteede, SvAa Henriksen and HJ Over. Central Veterinary Institute, Lelystad, The Netherlands 1983, 15–28.

  • Douvres FW: Morphogenesis of the Parasitic Stages of Trichostrongylus axei and Trichostron-gylus colibriformis, Nematode Parasites of Cattle. Proc. Helm. Soc. Wash. 1957, 4, 4–14.

    Google Scholar 

  • Drudge JH, Leland SE, Wyant ZN: Strain Variation in the Response of Sheep Nematodes to the Action of Phenothiazine. I. Studies on Mixed Infections in Experimental Animals. Amer. J. vet. Res., 1957, 18, 133–141.

    CAS  PubMed  Google Scholar 

  • Diiwel D, Schmid K, Bechmann G: Benzimidazol-resistente Haemonchus contortus beim Schaf in der BR Deutschland. (Benzimidazole Resistance in Haemonchus contortus of Sheep in The German Federal Republic). Berl. Münch. Tierärztl. Wschr. 1987, 99, 120–123.

    Google Scholar 

  • Finney DJ: Probit Analysis, 3rd edition, Cambridge University Press, Cambridge 1971.

  • Harrow ID, Gration KAF: Mode of action of the anthelmintic Morantel, Pyrantel and Levamisole on Muscle Cell Membrane of the Nematode Ascaris suum. Pestic. Sei., 1985, 16, 662–672.

    Article  CAS  Google Scholar 

  • Henriksen SV-AA: Modified and simple McMa-ster technique. In: Epidemiology and Control of nematodiasis in cattle. (Eds. P Nansen, RJ Jorgensen and EJL Soulsby). Martin Nijhoff Publishers, London 1981, pp. 45–50.

  • Jordi R: Untersuchungen zur Anthelmintika-Resi-stenz von Trichostrongyliden des Scharfes. (Investigations on Anthelmintic Resistance in Trichostrongyles of Sheep). Arch. Tierheilk.. 1980 722, 679–694.

    Google Scholar 

  • Kerboeuf D, Hubert J: Benzimidazole resistance in field strains of nematodes from goats in France. Vet. Rec. 1985, 116, 133.

  • Kerboeuf D, Hubert J, Mallet S: Haemonchus contortus: Infectivity and resistance to benzimidazoles. Vet. Rec. 1989, 124, 399–400.

    Article  CAS  Google Scholar 

  • Lacey E: The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles. Int. J. Parasitol. 1988, 18, 885–936.

    Article  CAS  Google Scholar 

  • Martin PJ: Development and control of resistance to anthelmintics. In Parasitology – Quo Vadit? Proc. VI. Int. Congr. Parasitol. (Ed. MJ Howell). Australian Academy of Science Canberry 1986, pp. 493–501.

  • Powers KG, Wood IB, Eckert J, Gibson T, Smith HJ: World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.). Guidelines for evaluating the efficacy of anthelmintics in ruminants (bovine and ovine). Vet. Parasitol. 1982, 10, 265–284.

    CAS  PubMed  Google Scholar 

  • Presidente PJA: Methods for detection of resistance to anthelmintics. In: Resistance in Nematodes to Anthelmintic Drugs. Eds. N. Anderson & PJ Waller. CSIRO, Division of Animal Health, Sydney 1985, pp. 13–17.

  • Prichard RK, Hall CA, Kelly JD, Martin ICA, Donald AD: The problem of anthelmintic resistance in nematodes. Aust. vet. J. 1980, 56, 239–251.

    Article  CAS  Google Scholar 

  • Ross JG, Purcell DA, Dow C, Todd JR: Experimental infection of calves with Trichostrongy-lus axel The course of development of infection and lesions in low level infections. Res. Vet. Sci. 1967, 8, 201–206.

    Article  CAS  Google Scholar 

  • Waller PJ: Anthelmintic Resistance in Nematode Parasites of Sheep. In Agricultural Zoology Reviews. Vol 1 (Gordon E. Russell), Intercept Ltd, Ponteland, Newcastle upon Tyne 1986, pp. 333–373.

  • Waller PJ, Prichard RK: Drug Resistance in Nematodes. In: Chemotherapy of Parasitic Diseases. (Eds. WC Campbell and RS Rew). Plenum Publishing Corporation, New York 1986, pp. 339–362.

  • Whitlock HV: The recovery and identification of first stage larvae of sheep nematodes. Aust. vet. J. 1959, 35, 310–316.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Veterinary Microbiology, Laboratory of Parasitology, Royal Veterinary and Agricultural University, Bulowsvej 13, DK-1870, Frederiksberg C, Denmark

    Henrik Bjørn, J. esper Monrad & Peter Nansen

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  1. Henrik Bjørn
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  2. J. esper Monrad
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  3. Peter Nansen
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Bjørn, H., esper Monrad, J. & Nansen, P. Anthelmintic Resistance in Nematode Parasites of Sheep in Denmark with Special Emphasis on Levamisole Resistance in Ostertagia circumcincta. Acta Vet Scand 32, 145–154 (1991). https://doi.org/10.1186/BF03546974

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Acta Veterinaria Scandinavica

ISSN: 1751-0147