1UMR 1225 INRA / DGER, 23 Chemin des Capelles, F31076 Toulouse FRANCE; 2Scottish Agricultural College,
Animal Nutrition and Health Department, Edinburgh, UK.; 3Moredun Research Institute, Parasitology Division, Edinburgh, UK.; 4Université Paul Sabatier, Faculté des Sciences Pharmaceutiques, F31062 Toulouse France; 5Unidad de Sanidad Animal, SIA, 50080
Zaragoza, Spain; 6KVL, Department of Animal Science and Animal Health, Royal Veterinary and Agricultural University, DK1870.
Denmark.
Introduction
In recent years, there has been a growing interest to seek alternative, sustainable methods to control gastrointestinal trichostrongyles in domestic ruminants (Waller et al , 1999). This is due to the constant development of resistant strains of gastrointestinal nematodes to broad spectrum anthelmintics (Jackson and Coop, 2000) and also, in order to respond to the increasing demand of consumers for reducing the use of chemicals in farming industry and the related products. Therefore, these alternative solutions also present major interest in organic farming (OF) systems, where the administration of chemical drugs is strongly regulated and should be restricted to curative purpose. Among the currently investigated options, there is a growing body of evidence to suggest that the consumption of some bioactive plants can, in certain circumstances, be associated with negative effects on the nematode populations of the gastrointestinal tract in small ruminants. These plants, therefore, seem to represent an attractive solution against the parasitic nematodes, and their use is compatible with the principles of organic farming.
Bioactive plants in nematode control
The first evidence on the anthelmintic properties of bioactive plants has been acquired on infected sheep in grazing conditions (Niezen et al, 1995; 1998a). They indicated that sheep grazing some legume forages, like sulla (Hedysarium coronarium) sainfoin, (Onobrychis viciifolia), birdsfoot trefoil (L. corniculatus) or maku (Lotus pedunculatus) presented less severe parasitic infections, as measured by reductions in nematode egg excretion and decreases in worm populations, compared to sheep grazing pastures seeded with control, tannin-free plants, such as plantain, lucerne or ryegrass (Niezen et al, 1998a, Marley et al, 2003). In most cases, these negative consequences on nematode populations have been associated with improved production performances of the parasitised hosts (Niezen et al, 1998a; 1998b, Marley et al, 2003). One common characteristic of those legume forages associated with reduced levels of parasitism was the presence of moderate to high concentrations of condensed tannins (Kahn and Diaz, 2000). Similar results were obtained in goats grazing Lespedeza serecea, another tanniferous plant, when compared to the control group grazing on tall festuque, a non tanniferous forages (Min and Hart, 2002; Min et al,2003).
The role of tannins
These anthelmintic properties of tannins were further explored in indoor conditions in experimentally infected sheep and goats. The parasite species used for the experimental infections corresponded to the most frequent and pathogenic ones occurring in these two small ruminant species. Quebracho, i.e. extracts of the bark from South American trees, Schinopsis spp
was used as a rich source of tannins, since these polyphenolic compounds represented 50 to 70 % of the DM. By comparison to control animals, the administration of quebracho drenches have been associated in both host species either with reductions in nematode larval establishment, in the fertility of female worms or in the number of adult worms (Athanasiadou et al, 2000a and b; Athanasiadou et al, 2001; Paolini et al, 2003a and 2003b).
On the other hand, these various studies have also underlined that several factors contribute to modulate the in vivo effects of tannins on worm biology. The response to quebracho differed between the abomasal and the intestinal nematode species (Athanasiadou et al, 2001). Moreover, the efficiency against the worm populations seems to depend on the tannin concentrations (Athanasiadou et al, 2001). Last, in goats, variations in effects were observed depending on the parasitic stage submitted to the action of tannins (Paolini et al, 2003b). Moreover, differences are also suspected to exist between sheep and goats.
In vitro studies have also been performed which aimed at measuring the effects of various plant extracts on different parasitic stages (eggs, larvae or adult worms) and/or nematode species in order to confirm the in vivo results. Such in vitro studies enabled to screen the anthelmintic properties associated with extracts from a large range of tanniferous plants, either legume forages, aromatic or woody plants which are naturally consumed by small ruminants in grazing or browsing conditions (Molan et al, 2000a and b ; Athanasiadou et al, 2001; Paolini et al 2004). In some cases, these in vitro results also provided indications on the possible mechanisms explaining the anthelmintic properties associated with the plant extracts. In particular, the use of some specific inhibitors of tannins, like polyethylene glycol (PEG), helps to confirm the role of these polyphenolic compounds in the detrimental effects on the parasitic stages. A bulk of evidence acquired from different in vitro studies supports the view that condensed tannins are involved in the anthelmintic properties of the tested bioactive plants (Molan et al, 2000a and 2000b ; Molan et al., 2003, Paolini et al, 2004). However, some studies also indicated that the potential implication of other plant secondary metabolites should not be rejected (Molan et al,
2003b; Paolini et al, 2004).
Two main mechanisms have been proposed to explain the effects of tannins on gastrointestinal nematodes. The first hypothesis supports the view that some plant secondary metabolites, and particularly tannins, may have direct anthelmintic properties. This is mainly supported by the results of in vitro assays where any host influence is absent (Molan et al, 2000a and 2000b ; Molan et al., 2003, Paolini et al, 2004) and also by the results of short term in vivo studies (Athanasiadou et al, 2000a). On the other hand, it has been proposed that the benefits of tanniferous plant consumption could also be related to indirect effects of tannins, through a reduction of ruminal degradation of the diet proteins and subsequently, an increase in the flow of digestible proteins in the small intestine of the parasitised host (Mangan et al, 1988) Since protein supplementations have been regularly associated with an improvement of the host resilience and
resistance, it is postulated that such nutritional impact of tannins could partly explain their antiparasitic properties (Coop and Kyriazakis , 2001).
Although the mechanisms explaining the observed effects of tanniferous plants remain unidentified, some studies have yet explored what could be the possible modes of application of these bioactive plants in farm conditions. The advantages associated with the incorporation of “anthelmintic pastures” in the grazing systems have received much attention (Niezen et al, 1995, 1998; Marley et al, 2003; Thamsborg et al, 2003). However, some studies have also illustrated the consequences on parasite biology due to the regular, repeated administration of hay from a legume forage, the sainfoin (Paolini et al, 2003 c). Last, because woody plants and bushes are tannin-rich plants, the possible benefits related to the exploitation of rangelands should also receive more attention, in order to assess to what extent the content of woody plants in secondary metabolites can explain the lower levels of nematode infections usually associated with the exploitation of rangelands (Hoste et al, 2001, Kabasa et al, 2000, Kahiya et al 2003).
Limitations to bioactive plants in helminth control
Some current limits in the use of bioactive plants have been identified. Agronomical considerations oblige to choose the species or varieties of plants that are well-adapted to the various local environmental conditions encountered in the different climatic areas. On the other hand, since a majority of the plant secondary metabolites are also known to have some anti- nutritional properties when consumed in excessive amounts (Mangan, 1988; Jean Blain 1998), the balance between the positive effects of plant secondary metabolite in infected animals and their potential negative consequences on host physiology needs to be clearly assessed. Lastly, there is a need to identify precisely the mechanisms of action of these compounds towards nematodes. Knowing these mechanisms will help to understand the origins of the variability observed in the results and to correct them.
Overall, the results accumulated since a decade on these interactions between bioactive plants and infected small ruminants represent one of the most promising option to reduce the reliance on chemotherapy and to achieve a sustainable control of gastrointestinal nematodes both in conventional and organic farming systems. Further basic studies are necessary to favour the implementation in the farms.
Acknowledgments
This work received the financial support from the European Union (Project WORMCOPS, QLK5-CT 2001-01843) and is part of a collaboration between Denmark, Great-Britain, Spain, Sweden, The Netherlands and France.
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