Assessment of the anthelmintic activity of medicinal plant extracts and purified condensed tannins against free-living and parasitic stages of Oesophagostomum dentatum.

Andrew R Williams,Stig M Thamsborg,Christos Fryganas,Honorata M Ropiak,Olivier Desrues,Irene Mueller-Harvey

doi:10.1186/s13071-014-0518-2

Andrew R Williams, Stig M Thamsborg + Show 4 more

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https://doi.org/10.1186/s13071-014-0518-2

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Abstract

BackgroundPlant-derived condensed tannins (CT) show promise as a complementary option to treat gastrointestinal helminth infections, thus reducing reliance on synthetic anthelmintic drugs. Most studies on the anthelmintic effects of CT have been conducted on parasites of ruminant livestock. Oesophagostomum dentatum is an economically important parasite of pigs, as well as serving as a useful laboratory model of helminth parasites due to the ability to culture it in vitro for long periods through several life-cycle stages. Here, we investigated the anthelmintic effects of CT on multiple life cycle stages of O. dentatum.MethodsExtracts and purified fractions were prepared from five plants containing CT and analysed by HPLC-MS. Anthelmintic activity was assessed at five different stages of the O. dentatum life cycle; the development of eggs to infective third-stage larvae (L3), the parasitic L3 stage, the moult from L3 to fourth-stage larvae (L4), the L4 stage and the adult stage.ResultsFree-living larvae of O. dentatum were highly susceptible to all five plant extracts. In contrast, only two of the five extracts had activity against L3, as evidenced by migration inhibition assays, whilst three of the five extracts inhibited the moulting of L3 to L4. All five extracts reduced the motility of L4, and the motility of adult worms exposed to a CT-rich extract derived from hazelnut skins was strongly inhibited, with electron microscopy demonstrating direct damage to the worm cuticle and hypodermis. Purified CT fractions retained anthelmintic activity, and depletion of CT from extracts by pre-incubation in polyvinylpolypyrrolidone removed anthelmintic effects, strongly suggesting CT as the active molecules.ConclusionsThese results suggest that CT may have promise as an alternative parasite control option for O. dentatum in pigs, particularly against adult stages. Moreover, our results demonstrate a varied susceptibility of different life-cycle stages of the same parasite to CT, which may offer an insight into the anthelmintic mechanisms of these commonly found plant compounds.

Highlights

Plant-derived condensed tannins (CT) show promise as a complementary option to treat gastrointestinal helminth infections, reducing reliance on synthetic anthelmintic drugs
It is apparent that CT can have anthelmintic effects; reduced worm burdens have been reported in rats administered CT in the diet, or in livestock grazing forages containing CT [13,14]
In the present study we investigated 1) whether CT have direct anthelmintic activity against O. dentatum in vitro, and 2) which stages of the life cycle of this parasite were targeted by CT

Summary

Introduction

Plant-derived condensed tannins (CT) show promise as a complementary option to treat gastrointestinal helminth infections, reducing reliance on synthetic anthelmintic drugs. Control of helminths relies almost exclusively on a limited number of synthetic anthelmintic drugs The limitations of this reliance on chemotherapy are the threat of parasites developing resistance to drug treatment (already widespread in some livestock production systems) [4,5] , the cost of drugs for small-scale farmers in developing countries and for some helminths, lack of efficacy of current available drugs [1]. Proanthocyanidins are a diverse and widely-occurring group of compounds, and consist of polymers of either catechin and/or epicatechin (termed procyanidins - PC), or of gallocatechin and/or epigallocatechin (termed prodelphinidins - PD), with hetero-polymers being common [10] They are found in plant material from both tropical and temperate areas, and have been widely investigated for their antioxidant and anti-inflammatory properties [11,12]. Much work remains to be done to establish the spectra of activity of CT, i.e. the range of helminth species that are susceptible, and what stages of the life cycle are targeted by these molecules

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