Hidden in plain sight - multiple resistant species within a strongyle community

McIntyre, J., Hamer, K., Morrison, A. A., Bartley, D. J., Sargison, N., Devaney, E. and Laing, R. (2018) Hidden in plain sight - multiple resistant species within a strongyle community. Veterinary Parasitology, 258, pp. 79-87. (doi: 10.1016/j.vetpar.2018.06.012) (PMCID:PMC6052248)

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Ovine parasitic gastroenteritis is a complex disease routinely treated using anthelmintics. Although many different strongyle species may contribute to parasitic gastroenteritis, not all are equally pathogenic: in temperate regions, the primary pathogen is Teladorsagia circumcincta. In this study we investigated benzimidazole and ivermectin resistance on a commercial sheep farm in southeast Scotland. We assessed the impact of species diversity on the diagnosis of resistance using the faecal egg count reduction test and in vitro bioassays, and correlated the results with the frequency of benzimidazole resistance-associated genotypes measured in the T. circumcincta population by pyrosequencing of the β-tubulin isotype-1 gene. Faecal egg count reduction test results showed efficacies of 65% for albendazole and 77% for ivermectin, indicating moderate resistance levels on the farm. However, PCR speciation of the same populations pre- and post-treatment revealed that removal of susceptible species had masked the presence of a highly resistant population of T. circumcincta. Less than 25% of individuals in the pre-treatment populations were T. circumcincta, the remainder consisting of Cooperia curticei, Chabertia ovina, Oesophagostomum venulosum and Trichostrongylus spp. In contrast, post-treatment with albendazole or ivermectin, the majority (88% and 100% respectively) of the populations consisted of T. circumcincta. The egg hatch test for benzimidazole resistance and the larval development test for ivermectin resistance were carried out using eggs obtained from the same populations and the results were broadly consistent with the faecal egg count reduction test. Thirty individual T. circumcincta from each sampling time point were assessed for benzimidazole resistance by pyrosequencing, revealing a high frequency and diversity of resistance-associated mutations, including within the population sampled post-ivermectin treatment. These results highlight the potential diversity of parasite species present on UK farms, and their importance in the diagnosis of anthelmintic resistance. On this particular farm, we demonstrate the presence of a highly dual-resistant population of T. circumcincta, which was strongly selected by treatment with either benzimidazoles or ivermectin, while other potentially less pathogenic species were removed.

Item Type:Articles
Additional Information:This work was funded by BBSRC (grant numbers BBN50385X/1 and BB/M003949/1), AHDB Beef and Lamb and the KTN (6130010011).
Glasgow Author(s) Enlighten ID:Devaney, Professor Eileen and McIntyre, Dr Jennifer and Laing, Dr Roz and Hamer, Miss Kim
Authors: McIntyre, J., Hamer, K., Morrison, A. A., Bartley, D. J., Sargison, N., Devaney, E., and Laing, R.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:Veterinary Parasitology
ISSN (Online):1873-2550
Published Online:11 June 2018
Copyright Holders:Copyright © 2018 The Authors
First Published:First published in Veterinary Parasitology 258:79-87
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
636401The BUG consortium Building Upon the Genome: using H. contortus genomic resources to develop novel interventions to control endemic GI parasitesEileen DevaneyBiotechnology and Biological Sciences Research Council (BBSRC)BB/M003949/1RI BIODIVERSITY ANIMAL HEALTH & COMPMED