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The kinetics of exsheathment of infective nematode larvae is disturbed in the presence of a tannin-rich plant extract (sainfoin) both in vitro and in vivo

Published online by Cambridge University Press:  08 March 2007

S. BRUNET ,
J. AUFRERE ,
F. El BABILI ,
I. FOURASTE  and
H. HOSTE
S. BRUNET
Affiliation:
Unité Mixte de Recherches 1225 INRA/DGER, ‘Interactions Hôte Agents Pathogènes’, École Nationale Vétérinaire de Toulouse, 23 chemin des Capelles, 31076 Toulouse, France
J. AUFRERE
Affiliation:
INRA, Unité de Recherche sur la Nutrition des Herbivores (équipe RAPA), Centre de Clermont Ferrand, Theix, 63122 Saint Genès Champanelle, France
F. El BABILI
Affiliation:
Unité Mixte de Recherche 152 IRD/UPS, 35 Chemin des Maraichers, 31062 Toulouse Cedex, France
I. FOURASTE
Affiliation:
Unité Mixte de Recherche 152 IRD/UPS, 35 Chemin des Maraichers, 31062 Toulouse Cedex, France
H. HOSTE*
Affiliation:
Unité Mixte de Recherches 1225 INRA/DGER, ‘Interactions Hôte Agents Pathogènes’, École Nationale Vétérinaire de Toulouse, 23 chemin des Capelles, 31076 Toulouse, France
*
*Corresponding author: Unité Mixte de Recherches 1225 INRA/DGER, ‘Interactions Hôte Agents Pathogènes’, École Nationale Vétérinaire de Toulouse, 23 Chemin des Capelles, F31076 Toulouse, France. Tel: +33 05 61 19 38 75. Fax: +33 05 61 19 32 43. E-mail: h.hoste@envt.fr
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Summary

The mode of action of bioactive plants on gastrointestinal nematodes remains obscure. Previous in vitro studies showed that exsheathment was significantly disturbed after contact with tannin-rich extracts. However, the role of important factors (extract concentration, parasite species) has not been assessed and no information is available on the occurrence in vivo. These questions represent the objectives of this study. The model incorporated the parasites Haemonchus contortus and Trichostrongylus colubriformis with sainfoin as the bioactive plant. A set of in vitro assays was performed, measuring the changes observed, after 3 h of contact with increasing concentrations of sainfoin, on the rate of artificial exsheathment. The results indicated that sainfoin extracts interfered with exsheathment in a dose-dependent manner and the process overall was similar for both nematodes. The restoration of control values observed after adding PEG to extracts confirms a major role for tannins. A second study was performed in vivo on rumen-cannulated sheep fed with different proportions of sainfoin in the diet to verify these in vitro results. The consumption of a higher proportion of sainfoin was indeed associated with significant delays in Haemonchus exsheathment. Overall, the results confirmed that interference with the early step of nematode infection might be one of the modes of action that contributes to the anthelmintic properties of tanniniferous plants.

Keywords

sainfoinparasitic nematodelarval exsheathmenttanninsHaemonchus contortusTrichostrongylus colubriformisrumen-cannulated sheep
Type
Research Article
Information
Parasitology , Volume 134 , Issue 9 , August 2007 , pp. 1253 - 1262
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Athanasiadou, S., Kyriazakis, I., Jackson, F. and 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, 205–219.CrossRefGoogle ScholarPubMed
Bahuaud, D., Martinez-Ortiz De Montellano, C., Chauveau, S., Prevot, F., Torres-Acosta, F., Fouraste, I. and Hoste, H. (2006). Effects of four tanniferous plant extracts on the in vitro exsheathment of third-stage larvae of parasitic nematodes. Parasitology 132, 545–554.CrossRefGoogle ScholarPubMed
Barrau, E., Fabre, N., Fouraste, I. and Hoste, H. (2005). Effect of bioactive compounds from sainfoin (Onobrychis viciifolia scop.) on the in vitro larval migration of Haemonchus contortus: role of tannins and flavonol glycosides. Parasitology 131, 531–538.CrossRefGoogle ScholarPubMed
Bravo, L. (1998). Polyphenols: chemistry, dietary sources, metabolism and nutritional significance. Nutrition Review 56, 317–333.CrossRefGoogle ScholarPubMed
Brunet, S. and Hoste, H. (2006). Monomers of condensed tannins affect the larval exsheathment of parasitic nematodes of ruminants. Journal of Agricultural and Food Chemistry 54, 7481–7487.CrossRefGoogle ScholarPubMed
Dakkak, A., Fioramonti, J. and Bueno, L. (1981). Haemonchus contortus third-stage larvae in sheep: kinetics of arrival into the abomasum and transformation during rumino-omasal transit. Research in Veterinary Science 31, 384–385.CrossRefGoogle ScholarPubMed
De Rosa, A. A., Chirgwin, S. R., Fletcher, J., Williams, J. C. and Klei, T. R. (2005). Exsheathment of Ostertagia ostertagi infective larvae following exposure to bovine rumen contents derived from low and high roughage diets. Veterinary Parasitology 129, 77–81.CrossRefGoogle ScholarPubMed
European Pharmacopea (2001). Détermination des tannins dans les drogues végétales. P. 107.Google Scholar
Hagerman, A. E., Rice, M. E. and Ritchard, N. T. (1998). Mechanisms of protein precipitation for two tannins, pentagalloyl glucose and epicatechin(4->8) catechin (procyanidin). Journal of Agricultural and Food Chemistry 46, 2590–2595.CrossRefGoogle Scholar
Hertzberg, H., Huwyler, U., Kohler, L., Rehbein, S. and Wanner, M. (2002). Kinetics of exsheathment of infective ovine and bovine strongylid larvae in vivo and in vitro. Parasitology 125, 65–70.CrossRefGoogle ScholarPubMed
Hoste, H., Gaillard, L. and Le Frileux, Y. (2005). Consequences of the regular distribution of sainfoin hay on gastrointestinal parasitism with nematodes and milk production in dairy goats. Small Ruminant Research 59, 265–271.CrossRefGoogle Scholar
Hoste, H., Jackson, F., Athanasiadou, S., Thamsborg, S. M. and Hoskin, S. O. (2006). The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology 22, 253–261.CrossRefGoogle ScholarPubMed
Jackson, F. and Coop, R. L. (2000). The development of anthelmintic resistance in sheep nematodes. Parasitology 120 (Suppl.), S95–S107.CrossRefGoogle ScholarPubMed
Kahn, L. P. and Diaz-Hernandez, A. (2000). Tannins with anthelmintic properties. In Tannins in Livestock and Human Nutrition: ACIAR Proceeding no. 92 International Workshop (ed. Brooker, J. D.), pp. 140–149. Adelaide, Australia.Google Scholar
Makkar, H. P. S., Blummel, M., Borowy, N. K. and Becker, K. (1995). Formation of complexes between polyvinyl pyrrolidones or polyethylene glycols and tannins, and their implication in gas production and the true digestibility in in vitro techniques. British Journal of Nutrition 73, 897–913.CrossRefGoogle ScholarPubMed
Makkar, H. P. S. (2006). Chemical and biological assays for quantification of major plant secondary metabolites. In Herbivores, Assessment of Intake, Digestibility and the Roles of Secondary Compounds (ed. Sandoval-Castro, C. A., DeB Hovell, F. D., Torres-Acosta, J. F. J. and Ayala-Burgos, A.), pp. 235–249. Nottingham University Press, Nottingham.Google Scholar
Marais, J. P. J., Mueller-Harvey, I., Brandt, E. V. and Ferreira, D. (2000). Polyphenols, condensed tannins and other natural products in Onobrychis viciifolia (sainfoin). Journal of Agricultural and Food Chemistry 48, 3440–3447.CrossRefGoogle ScholarPubMed
Min, B. R. and Hart, S. P. (2002). Tannins for suppression of internal parasites. Journal of Animal Science 81, 102–109.Google Scholar
Min, B. R., Hart, S. P., Miller, D., Tomita, G. M., Loetz, E. and Sahlu, T. (2005). The effects of grazing forage containing condensed tannins on gastro-intestinal parasite infection and milk composition in Angora does. Veterinary Parasitology 130, 105–113.CrossRefGoogle Scholar
Molan, A. L., Alexander, R. A., Brookes, I. M. and 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. Proceeding of the New Zealand Society of Animal Production 60, 21–25.Google Scholar
Molan, A., Duncan, A., Barry, T. and McNabb, W. C. (2003). 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, 209–218.CrossRefGoogle ScholarPubMed
Molan, A. L., Hoskin, O., Barry, T. and McNabb, W. C. (2000 c). Effect of condensed tannins extracted from four forages on the viability of the larvae of deer lungworms and gastrointestinal nematodes. Veterinary Research 147, 44–48.Google ScholarPubMed
Molan, A. L., Sivakumaran, S., Spencer, P. A. and Meagher, L. P. (2004). Green tea flavan-3-ols and oligomeric proanthocyanidins inhibit the motility of infective larvae of Teladorsagia circumcincta and Trichostrongylus colubriformis in vitro. Veterinary Science 7, 239–243.CrossRefGoogle Scholar
Molan, A. L., Waghorn, G. C., Min, B. M. and McNabb, W. C. (2000 b). The effect of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro. Folia Parasitologica 47, 39–44.CrossRefGoogle ScholarPubMed
Mueller-Harvey, I. (2006). Unravelling the conundrum of tannins in animal nutrition and health. Journal of Science, Food and Agriculture 86, 2010–2037.CrossRefGoogle Scholar
Niezen, J. H., Waghorn, T. S., Charleston, W. A. G. and Waghorn, G. C. (1995). Growth and gastrointestinal nematode parasitism in lambs grazing either lucerne (Medicago sativa) or sulla (Hedysarum coronarium) which contains condensed tannins. Journal of Agriculture Science 125, 281–289.CrossRefGoogle Scholar
Niezen, J. H., Robertson, H. A., Waghorn, G. C. and Charleston, W. A. G. (1998). Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Veterinary Parasitology 80, 15–27.CrossRefGoogle ScholarPubMed
Paolini, V., De La Farge, F., Prevot, F., Dorchies, PH. and Hoste, H. (2005). Effects of repeated distribution of sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Veterinary Parasitology 127, 277–283.CrossRefGoogle ScholarPubMed
Paolini, V., Dorchies, Ph. and Hoste, H. (2003 a). Effects of sainfoin hay on gastrointestinal infection with nematodes in goats. Veterinary Record 152, 600–601.CrossRefGoogle ScholarPubMed
Paolini, V., Fouraste, I. and Hoste, H. (2004). In vitro effects of three woody plant and sainfoin on third-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 129, 69–77.CrossRefGoogle Scholar
Paolini, V., Frayssines, A., De La Farge, F., Dorchies, Ph. and Hoste, H. (2003 b). Effects of condensed tannins on established populations and on incoming larvae of Trichostrongylus colubriformis and Teladorsagia circumcincta in goats. Veterinary Research 34, 331–339.CrossRefGoogle ScholarPubMed
Petronijevic, T. W. P., Rogers, W. P. and Somerville, R. I. (1985). Carbonic acid as the host signal for the development of parasitic stages of nematodes. International Journal for Parasitology 15, 661–667.CrossRefGoogle ScholarPubMed
Petronijevic, T. W. P., Rogers, W. P. and Somerville, R. I. (1986). Organic and inorganic acids as the stimulus for exsheathment of infective juveniles of nematodes. International Journal for Parasitology 16, 163–168.CrossRefGoogle ScholarPubMed
Petronijevic, T. W. P. and Rogers, W. P. (1987). Undissociated bases as the stimulus for the development of early parasitic stages of nematodes. International Journal for Parasitology 17, 911–915.CrossRefGoogle ScholarPubMed
Poncet-Legrand, C., Edelmann, A., Putaux, J. L., Cartalade, D., Sarni-Manchado, P. and Vernhet, A. (2006). Poly(L-proline) interactions with flavan-3-ols units: influence of the molecular structure and the polyphenol/protein ratio. Food Hydrocolloids 20, 687–697.CrossRefGoogle Scholar
Shaik, S. A., Terrill, T. H., Miller, J. E., Kouakou, B., Kannan, G., Kaplan, R. M., Burke, J. M. and Mosjidis, J. A. (2006). Sericea lespedeza hay as natural deworming agent against gastrointestinal nematode infection in goats. Veterinary Parasitology 139, 150–157.CrossRefGoogle Scholar
Silanikove, N., Perevolotsky, A. and Provenza, F. D. (2001). Use of tannin-binding chemicals to assay for tannins and their negative postingestive effects in ruminants. Animal Feed Science and Technology 91, 69–81.CrossRefGoogle Scholar
Sommerville, R. I. and Rogers, W. P. (1987). The nature and action of host signals. Advances in Parasitology 26, 239–293.CrossRefGoogle ScholarPubMed
Thamsborg, S. M., Mejer, H., Bandier, M. and Larsen, M. (2003). Influence of different forages on gastrointestinal nematode infections in grazing lambs. World Association for the Advancement of Veterinary Parasitology. The 19th International Conference, New Orleans, p. 189.Google Scholar
Waterman, P. G. (1999). The tannins – An overview. In Tannins in Livestock and Human Nutrition, Proceedings of an International Workshop (ed. Brooker, J. D.), pp. 10–13. Australian Centre for International Agricultural Research, Adelaide, Australia.Google Scholar