Development of strategies to reduce anthelmintic use in livestock

Abstract

Gastrointestinal nematode (GIN) infections are one of the main health challenges in small ruminant and beef cattle systems, leading to reduced production and welfare globally. GIN are traditionally controlled with anthelmintic drugs, however due to regulations in organic farming systems and the rise in anthelmintic resistance, alternatives are sought after. One such alternative is the use of bioactive plant feeding, due to the presence of plant secondary (or specialised) metabolites (PSMs) that have been shown to demonstrate anthelmintic activity.

This thesis focussed on the investigation of the anthelmintic activity of the perennial shrub heather (Ericaceae family) which is rich in PSMs, such as proanthocyanidins, and the plant is highly abundant across Europe indicating its amenability as an animal feed. The anthelmintic efficacy of heather extract was tested in vitro against Teladorsagia circumcincta and Trichostrongylus colubriformis eggs and infective larvae, as these species are two of the most prevalent small ruminant GIN in Europe. The efficacies of Calluna vulgaris extracts were compared across country of origin of the heather, the season in which the heather was sampled, and for Spanish samples, the efficacy of heather species was compared; C. vulgaris and Erica cinerea. To identify the key active compounds within the heather extracts, egg hatch assays were carried out using extracts incubated with polyvinyl polyrrolidone (PVPP), a chemical with the ability to block the activity of tannins and some galloylated flavonoids. The heather extracts were chemically analysed to quantify the relevant polyphenol subgroups present, and the chemical composition of the extracts was associated with the anthelmintic activity observed. This work provided in vitro evidence that heather has anthelmintic potential; the anthelmintic properties were characterised and quantified in vitro, and specific compounds identified that were associated with the anthelmintic effects on different GIN species and life stages.

An in vivo study in domestic sheep (Ovis aries) was carried out using six groups of 10 Texel-cross lambs, grouped according to diet (heather or control hay), infection status (infected or uninfected) and the presence or absence of nematophagous fungi supplementation. In addition to the anthelmintic effects shown by PSM consumption, these compounds can also exhibit anti-nutritional effects within the animal. The aim of this study was to test the trade-off between the anti-nutritional and the curative effects of feeding heather to T. circumcincta infected lambs. As sustainable alternatives to anthelmintics are unlikely to be used in isolation, within this study we also tested the combination of feeding heather and a nematophagous fungi; Duddingtonia flagrans. It was observed that heather consumption at 20% of dry matter intake resulted in significantly lower egg output in infected lambs, although heather-fed lambs showed lower bodyweight compared to hay-fed lambs. Heather feeding had no impact on D. flagrans trapping ability, which indicates that these two alternatives could be used together to improve parasite control in animals. This work showed how heather feeding can exhibit anthelmintic effects, but care may be needed to reduce any anti-nutritional effects on performance.

A systematic review was carried out to explore the anthelmintic efficacies shown by a wide range of bioactive plants, which contained polyphenolic compounds thought to be acting on GIN. The aim was to determine the considerations of using bioactive plant feeding as an effective and feasible alternative control method, and if in vitro testing is an accurate predictor of in vivo anthelmintic activity. The studies included in the systematic review had to fulfil the criteria: i) quantified the polyphenol content in the plants used, ii) measured bioactive plant intake by the study animals so the intake of polyphenols could be associated with any egg output reductions, and iii) all controls in place. The review highlighted a need for standardisation of protocols used to analyse polyphenol content of bioactive plants, to aid identification of effective doses and active compounds that should be focused on when selecting or breeding bioactive plants.

Overall, the thesis demonstrated the potential of feeding bioactive plants such as heather to aid a reduction in anthelmintic drug use to control common parasite infections in livestock, and it explores which considerations are needed before farmers can maximise the efficacy of plants in the diet of ruminants.