Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-18T05:43:10.841Z Has data issue: false hasContentIssue false

In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes

Published online by Cambridge University Press:  10 June 2004

V. PAOLINI
Affiliation:
Unité Mixte de Recherches 1225 INRA/DGER, ‘Interactions Hôte Pathogène’, Ecole Nationale Vétérinaire de Toulouse, 23 chemin des Capelles, F31076 Toulouse, France
I. FOURASTE
Affiliation:
Faculté des Sciences Pharmaceutiques, Université Paul Sabatier Toulouse III, 35 Chemin des Maraîchers, F31062 Toulouse, France
H. HOSTE
Affiliation:
Unité Mixte de Recherches 1225 INRA/DGER, ‘Interactions Hôte Pathogène’, Ecole Nationale Vétérinaire de Toulouse, 23 chemin des Capelles, F31076 Toulouse, France

Abstract

Most studies on the effects of tanniferous plants on nematodes have examined forages but have neglected the woody plants. Therefore, in vitro effects of extracts from 3 woody plants (Rubus fructicosus, Quercus robur, Corylus avellana) have been tested on trichostrongyles and compared to sainfoin, a legume forage. Because some in vivo results indicated that the effects of tannins differed depending on the parasitic species and/or stages, the effects were measured on 3rd-stage larvae (L3) and adult worms of Teladorsagia circumcincta, Haemonchus contortus and Trichostrongylus colubriformis. The effects of plant extracts varied according to the plant sources, the parasite species and stages. For the woody plants, significant inhibitory effects were obtained on both stages of abomasal species. Results for T. colubriformis were more variable. Effects of sainfoin extracts were significant on T. colubriformis and H. contortus L3, and on abomasal adult worms. In order to assess the implications of tannins, polyethylene glycol (PEG), an inhibitor of tannins, was added to hazel tree, oak and sainfoin extracts. Without PEG, significant inhibitory effects on L3 and adult worms were confirmed. After addition of PEG, the larval migration and motility of adult worms were restored in most cases. These results confirm variations in effects depending on factors related to plants or parasites and suggest that tannins are partly responsible for the effects.

Type
Research Article
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ATHANASIADOU, S., KYRIAZAKIS, I., JACKSON, F. & COOP, R. L. ( 2000 a). Effects of short term exposure to condensed tannins on adult T. colubriformis. Veterinary Record 146, 728732.Google Scholar
ATHANASIADOU, S., KYRIAZAKIS, I., JACKSON, F. & COOP, R. L. ( 2000 b). Consequences of long-term feeding with condensed tannins on sheep parasited with T. colubriformis. International Journal for Parasitology 30, 10251033.Google Scholar
ATHANASIADOU, S., KYRIAZAKIS, I., JACKSON, F. & COOP, R. L. ( 2001). Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep in vitro and in vivo studies. Veterinary Parasitology 99, 205219.CrossRefGoogle Scholar
DE BRUYNE, T., PIETERS, L., DEELSTRA, H. & VLIETINCK, A. ( 1999). Condensed vegetable tannins: Biodiversity in structure and biological activities. Biochemical Systematics and Ecology 27, 445459.CrossRefGoogle Scholar
FOO, L. Y., JONES, W. T., PORTER, L. J. & WILLIAMS, V. M. ( 1982). Proanthocyanidin polymers of fodder legumes. Phytochemistry 21, 933935.Google Scholar
FOO, L. Y., LU, Y., McNABB, W. C., WAGHORN, G. & ULYATT, M. J. ( 1997). Proanthocyanidins from Lotus pedunculatus. Phytochemistry 45, 16891696.CrossRefGoogle Scholar
FOO, L. Y., NEWMAN, R., WAGHORN, G., McNABB, W. C. & ULYATT, M. J. ( 1996). Proanthocyanidins from Lotus corniculatus. Phytochemistry 41, 617624.CrossRefGoogle Scholar
GARG, S. K., MAKKAR, H. P. S., NAGAL, K. B., SHARMA, S. K., WADHWA, D. R. & SINGH, B. ( 1992). Toxicological investigations into oak (Quercus incana) leaf poisoning in cattle. Veterinary Human Toxicology 34, 161164.Google Scholar
GORDON, I. J. ( 2003). Browsing and grazing ruminants: are they different beasts? Forest Ecology and Management 181, 1321.Google Scholar
GUARRERA, P. M. ( 1999). Traditional anthelmintic, antiparasitic and repellent uses of plants in Central Italy. Journal of Ethnopharmacology 68, 183192.CrossRefGoogle Scholar
JACKSON, F. S., BARRY, T. N., LASCANO, C. & PALMER, B. ( 1996). The extractable and bound condensed tannin content of leaves from tropical tree, shrub and forage legumes. Journal of Sciences, Food and Agriculture 71, 103110.3.0.CO;2-8>CrossRefGoogle Scholar
JACKSON, F. & COOP, R. L. ( 2000). The development of anthelmintic resistance in sheep nematodes. Parasitology 120, 95107.CrossRefGoogle Scholar
JEAN-BLAIN, C. ( 1998). Aspects nutritionnels et toxicologiques des tanins. Revue de Médecine vétérinaire 149, 911920.Google Scholar
JONES, W. T. & MANGAN, J. L. ( 1977). Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia scop.) with fraction 1 leaf protein and with submaxillary mucoprotein and their reversal by polyethylene glycol and pH. Journal of Sciences, Food and Agriculture 28, 126136.Google Scholar
KABASA, J. D., OPUDA-ASIBO, J. & TER MEULEN, U. ( 2000). The effect of oral administration of polyethylene glycol on faecal helminth egg counts in pregnant goats grazed on browse containing condensed tannins. Tropical Animal Health and Production 32, 7386.CrossRefGoogle Scholar
KAHIYA, C., MUKARATIRWA, S. & THAMSBORG, S. M. ( 2003). Effects of Acacia nilotica and Acacia karoo diets on Haemonchus contortus infection in goats. Veterinary Parasitology 29, 265274.CrossRefGoogle Scholar
KAHN, L. P. & DIAZ-HERNANDEZ, A. ( 2000). Tannins with anthelmintic properties. Tannins in Livestock and Human nutrition: Proceedings of an International workshop, Adelaide, Australia. ACLAR proceedings 92, 130138.Google Scholar
KUMAR, R. & VAITHIYANATHAN, S. ( 1990). Occurrence, nutritional significance and effect on animal productivity of tannins in tree leaves. Animal Feed Science and Technology 30, 2138.CrossRefGoogle Scholar
LANDAU, S., PEREVOLOTSKY, A., BONFIL, D., BARKAI, D. & SILANIKOVE, N. ( 2000). Utilization of low quality resources by small ruminants in Mediterranean agro-pastoral systems: the case of browse and aftermath cereal stubble. Livestock Production Science 64, 3949.CrossRefGoogle Scholar
MAKKAR, H. P. S. ( 2003). Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small Ruminant Research 49, 241256.CrossRefGoogle Scholar
MIN, B. R., POMROY, W. E., HART, S. P. & SAHLU, T. ( 2004). The effect of short-term consumption of a forage containing condensed tannins on gastro-intestinal nematode parasite infections in grazing wether goats. Small Ruminant Research 51, 279283.CrossRefGoogle Scholar
MOLAN, A. L., ALEXANDER, R. A., BROOKES, I. M. & McNABB, W. C. ( 2000 a). Effect of an extract from Sulla (Hedysarum coronarium) containing condensed tannins on the migration of three sheep gastrointestinal nematodes in vitro. Proceedings of New Zealand Society for Animal Production 60, 2125.Google Scholar
MOLAN, A., DUNCAN, A., BARRY, T. & McNABB, W. ( 2003 a). Effects of condensed tannins and crude sesquiterpene lactones extracted from chicory on the motility of larvae of deer lungworm and gastrointestinal nematodes. Parasitology International 52, 209218.Google Scholar
MOLAN, A. L., MEAGHER, L. P., SPENCER, P. A. & SIVAKUMARAN, S. ( 2003 b). Effect of flavan-3-ols on in vitro egg hatching, larval development and viability of infective larvae of Trichostrongylus colubriformis. International Journal for Parasitology 33, 16911698.Google Scholar
MOLAN, A. L., WAGHORN, G. C., MIN, B. R. & McNABB, W. C. ( 2000 b). The effect of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro. Folia Parasitologica 47, 3944.Google Scholar
MOLLE, G., DECANDIA, M., FOIS, N., LIGIOS, S., CABIDDU, A. & SITZIA, M. ( 2003). The performance of Mediterranean dairy sheep given access to sulla (Hedysarum coronarium L.) and annual ryegrass (Lolium rigidum Gaudin) pastures in different time proportions. Small Ruminant Research 49, 319328.Google Scholar
NIEZEN, J. H., CHARLESTON, W. A. G., ROBERTSON, H. A., SHELTON, D., WHAGHORN, G. C. & GREEN, R. ( 2002). The effect of feeding sulla (Hedysarum coronarium) or lucerne (Medicago sativa) on lamb parasite burdens and development of immunity to gastrointestinal nematodes. Veterinary Parasitology 105, 229245.CrossRefGoogle Scholar
NIEZEN, J. H., ROBERTSON, H. A., WAGHORN, G. C. & CHARLESTON, W. A. G. ( 1998 a). Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Veterinary Parasitology 80, 1527.Google Scholar
NIEZEN, J. H., WAGHORN, G. C. & CHARLESTON, W. A. G. ( 1998 b). Establishment and fecundity of Ostertagia circumcincta and Trichostrongylus colubriformis in lambs fed Lotus (L. pedunculatus) or perennial ryegrass (Lolium perenne). Veterinary Parasitology 78, 1321.Google Scholar
PAOLINI, V., BERGEAUD, J. P., GRISEZ, C., PREVOT, F., DORCHIES, Ph. & HOSTE, H. ( 2003 a). Effects of condensed tannins on goats experimentally infected with Haemonchus contortus. Veterinary Parasitology 113, 253261.Google Scholar
PAOLINI, V., DORCHIES, Ph. & HOSTE, H. ( 2003 b). Effects of sainfoin hay on gastrointestinal nematode infections in goats. Veterinary Record 152, 600601.Google Scholar
PAOLINI, V., FRAYSSINES, A., DE LA FARGE, F., DORCHIES, Ph. & HOSTE, H. ( 2003 c). Efficacy of condensed tannins on established populations and on incoming larvae of Trichostrongylus colubriformis and Teladorsagia circumcincta in goats. Veterinary Research 34, 331339.Google Scholar
RABEL, B., McGREGOR, R. & DOUCH, P. G. C. ( 1994). Improved bioassay for estimation of inhibitory effects of ovine gastrointestinal mucus and anthelmintics on nematode larval migration. International Journal for Parasitology 24, 671676.CrossRefGoogle Scholar
SILANIKOVE, N. ( 2000). The physiological basis of adaptation in goats to harsh environments. Small Ruminant Research 35, 181193.CrossRefGoogle Scholar
SILANIKOVE, N., GILBOA, N., PEREVOLOTSKY, A. & NITSAN, Z. ( 1996). Goats fed tannin-containing leaves do not exhibit toxic syndromes. Small Ruminant Research 21, 195201.CrossRefGoogle Scholar
SINGH, S., McCALLUM, J., GRUBER, M. Y., TOWERS, G. H. N., MUIR, A. D., BOHM, B. A., KOUPAI-ABYAZANI, M. R. & GLASS, A. D. M. ( 1997). Biosynthesis of flavan-3-ols by leaf extracts of Onobrychis viciifolia. Phytochemistry 44, 425432.CrossRefGoogle Scholar
TERRILL, T. H., WAGHORN, G. C., WOOLLEY, D. J., McNABB, W. C. & BARRY, T. N. ( 1994). Assay and digestion of 14 C-labelled condensed tannins in the gastrointestinal tract of sheep. British Journal of Nutrition 72, 467477.CrossRefGoogle Scholar
WAGHORN, G. C. & McNABB, W. C. ( 2003). Consequences of plant phenolic compounds for productivity and health for ruminants. Proceedings of the Nutrition Society 62, 383392.CrossRefGoogle Scholar
WAGLAND, B. M., JONES, W. O., HRIBAR, L., BENDIXSEN, T. & EMERY, D. L. ( 1992). A new simplified assay for larval migration inhibition. International Journal for Parasitology 22, 11831185.CrossRefGoogle Scholar