Acquired immunity to endoparasites in sheep interacts with anthelmintic treatment to influence selection for anthelmintic resistance

AIM: To test the hypothesis that anthelmintic treatment of animals with a well-developed immunity to endoparasites will be more selective for anthelmintic resistance than treatment of animals that are not immunocompetent. METHODS: In Experiment 1, five pregnant, mixed-aged ewes, and five newly weaned 3-month-old lambs were housed indoors, and infected three times a week with a mixture of albendazole-resistant and -susceptible Teladorsagia (=Ostertagia) circumcincta larvae for 12 weeks. In Experiment 2, six two-tooth ewes, six 9-month-old lambs, and 10 newly weaned 3-month-old lambs were infected three times a week with a mixture of albendazole-resistant and -susceptible Trichostrongylus colubriformis larvae for 10 weeks over the winter months of June to August. Egg-hatch assays (EHA) were performed on a weekly basis, to determine the resistance status of eggs passed before and after a treatment with albendazole, that was given at least one week after the infections became patent. RESULTS: Faecal nematode egg counts (FEC) indicated that mature ewes and immunocompetent lambs restricted the establishment of parasite larvae, especially after the anthelmintic treatment. Although EHA were completed for T. circumcincta, the numbers of eggs recovered from the ewes were too few to allow accurate comparisons of anthelmintic resistance status between ewes and lambs. In Experiment 2, viable infections of T. colubriformis only developed in five 9-month-old and five 3-month-old lambs after anthelmintic treatment. Comparison of the concentrations of anthelmintic needed to kill 50% of the eggs (LC(50)) from the lambs showed that where host immunity restricted the establishment of new infection after anthelmintic treatment, the resistance status of eggs passed remained high until the end of the study. In contrast, where new infections established, the resistance status of eggs in the faeces declined to levels close to those prior to anthelmintic treatment. CONCLUSIONS: The results support the conclusion that older animals are more refractory to the establishment of ingested parasite larvae, and that this reduces the dilution of resistant worms surviving an anthelmintic treatment. Surviving resistant worms are therefore likely to make a greater proportional contribution to the resulting population of parasites on pasture. The findings support the view that treating mature sheep with an anthelmintic should be considered a higher-risk practice for selecting anthelmintic-resistant parasites, than treating lambs.