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The effect of dietary sainfoin (Onobrychis viciifolia) on local cellular responses to Trichostrongylus colubriformis in sheep

Published online by Cambridge University Press:  19 June 2008

L. RÍOS-DE ÁLVAREZ ,
A. W. GREER ,
F. JACKSON ,
S. ATHANASIADOU ,
I. KYRIAZAKIS  and
J. F. HUNTLEY
L. RÍOS-DE ÁLVAREZ*
Affiliation:
Instituto de Producción Animal, Facultad de Agronomía, Universidad Central de Venezuela, Venezuela Moredun Research Institute, Parasitology Division, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
A. W. GREER
Affiliation:
Agriculture and Life Sciences Division, PO Box 84, Lincoln University, Canterbury, New Zealand
F. JACKSON
Affiliation:
Moredun Research Institute, Parasitology Division, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
S. ATHANASIADOU
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh EH9 3JG, UK
I. KYRIAZAKIS
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh EH9 3JG, UK
J. F. HUNTLEY
Affiliation:
Moredun Research Institute, Parasitology Division, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
*
*Corresponding author: Instituto de Producción Animal, Facultad de Agronomía, Universidad Central de Venezuela, Venezuela. Tel: +582432454120. +584124767809. Fax: +582432454120. E-mail: [email protected]; [email protected]
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Summary

The effect of sainfoin (Onobrychis viciifolia) hay consumption on the pathophysiology and local cellular responses of growing lambs during infection with Trichostrongylus colubriformis was investigated. Thirty-two lambs, 16 weeks of age, were allocated to 1 of 4 treatment groups (n=8) that were offered either grass (G) or sainfoin (S) hay while concurrently either infected (+), or not (−) with 12 000 L3 T. colubriformis larvae per week for 6 weeks. Liveweight gains were affected by diet (P=0·002) and reduced by infection (P<0·005). Faecal egg count was reduced in S+ compared to G+from days 35 to 42 (P=0·001); however, total egg output, worm burdens at day 42 and worm fecundity were similar between diets (P>0·05). Feeding sainfoin appeared to enhance immune cell development with tissue eosinophils, mast cells and pan T cells present in greater concentrations in S+ than in G+ animals. However, further studies are required to determine if the enhanced immune cell development is a consequence of a greater nutrient supply or a direct influence of sainfoin metabolites on local inflammatory responses to the gastrointestinal nematode T. colubriformis.

Keywords

sainfoinOnobrychis viciifoliaTrichostrongylus colubriformisplant secondary metabolites (PSM)local immune responsenematodessheep
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 9 , August 2008 , pp. 1117 - 1124
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Athanasiadou, S., Kyriazakis, I. and Jackson, F. (2005). The effects of feeding Sainfoin hay in sheep parasitised with Trichostrongylus colubriformis. Annual Conference BSAS, 4–6th April 2005, York University, UK, p. 90. http://www.bsas.org.uk/downloads/annlproc/Pdf2005/090.pdfCrossRefGoogle Scholar
Balic, A., Bowles, V. M. and Meeusen, E. N. (2000). Cellular profiles in the abomasal mucosa and lymph node during primary infection with Haemonchus contortus in sheep. Veterinary Immunology and Immunopathology 75, 109–120. doi:10.1016/S0165-2427(00)00189-6CrossRefGoogle ScholarPubMed
Balic, A., Cunningham, C. P. and Meeusen, E. N. (2006). Eosinophil interactions with Haemonchus contortus larvae in the ovine gastrointestinal tract. Parasite Immunology 28, 107–115. doi:10.1111/j.1365-3024.2006.00816.xCrossRefGoogle 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 flavonols glycosides. Parasitology 131, 1–8. doi:10.1017/S0031182005008024CrossRefGoogle ScholarPubMed
Bown, M. D., Poppi, D. P. and Sykes, A. R. (1991). The effect of post-ruminal infusion of protein or energy on the pathophysiology of Trichostrongylus colubriformis infection and body composition in lambs. Australian Journal of Agricultural Research 42, 253–267. doi:10.1071/AR9910253Google Scholar
Christie, M. and Jackson, F. (1982). Specific identification of Strongyle eggs in small samples of sheep faeces. Research in Veterinary Science 32, 113–117.CrossRefGoogle ScholarPubMed
Coop, R. L., Huntley, J. F. and Smith, W. D. (1995). Effect of dietary protein supplementation on the development of immunity to Ostertagia circumcincta in growing lambs. Research in Veterinary Science 59, 24–29. doi:10.1016/0034-5288(95)90025-XCrossRefGoogle ScholarPubMed
Coop, R. L. and Kyriazakis, I. (2001). Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology 17, 325–330. doi:10.1016/S1471-4922(01)01900-6.CrossRefGoogle ScholarPubMed
Enerback, L. (1966). Mast cells in rat gastrointestinal mucosa.1. Effect of fixation. Acta Pathologica et Microbiologie Scandinavica 66, 289–302.CrossRefGoogle Scholar
Gonzales, L., Anderson, I., Deane, D., Summers, C. and Buxton, D. (2001). Detection of immune system cells in paraffin wax-embedded ovine tissues. Journal of Comparative Pathology 125, 41–47. doi:10.1053/jcpa.2001.0475CrossRefGoogle Scholar
Heckendorn, F., Häring, D. A., Maurer, V.Zinsstag, J., Langhans, W. and Hertzberg, H. (2006). Effect of sainfoin (Onobrychis viciifolia) silage and hay on established populations of Haemonchus contortus and Cooperia curticei in lambs. Veterinary Parasitology 142, 293–300. doi:10.1016/j.vetpar.2006.07.014CrossRefGoogle ScholarPubMed
Heckendorn, F., Häring, D. A., Maurer, V.Senn, M. W. and Hertzberg, H. (2007). Individual administration of three tanniferous forage plants to lambs artificially infected with Haemonchus contortus and Cooperia curticei. Veterinary Parasitology 146, 123–134. doi:10.1016/j.vetpar.2007.01.009CrossRefGoogle 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. doi:10.1016/j.smallrumres.2005.05.011CrossRefGoogle 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. doi:10.1016/j.pt.2006.04.004CrossRefGoogle ScholarPubMed
Huntley, J. F. (1992). Mast cells and basophils: A review of their heterogeneity and function. Journal of Comparative Pathology 107, 349–372. doi:10.1016/0021-9975(92)90010-RCrossRefGoogle Scholar
Ishikawa, N., Wakelin, D. and Mahida, Y. R. (1997). Role of T helper 2 cells in intestinal goblet cell hyperplasia in mice infected with Trichinella spiralis. Gastroenterology 113, 542–549. doi:10.1053/gast.1997.v113.pm9247474CrossRefGoogle ScholarPubMed
Kay, J. E. (1991). Mechanisms of T lymphocyte activation. Immunology Letters 29, 51–54. doi:10.1016/0165-2478(91)90198-JCrossRefGoogle ScholarPubMed
Khan, W. I. and Collins, S. M. (2004). Immune-mediated alteration in gut physiology and its role in host defence in nematode infection. Parasite Immunology 26, 319–326. doi:10.1111/j.0141-9838.2004.00740.xCrossRefGoogle ScholarPubMed
Lane, G. P. F. and Koivisto, J. M. (2005). A reassessment of the potential of Sainfoin (Onobrychis viciifolia Scop.) as a forage crop for the United Kingdom. [On-line]: http://www.royagcol.ac.uk/flg/pdf/Gerryposter.PDFGoogle Scholar
Lendrum, A. C. (1944). The staining of eosinophil polymorphs and enterochromaffin cells in histological sections. Journal of Pathology and Bacteriology 56, 441–443.CrossRefGoogle Scholar
Marais, J. P. J., Mueller-Harvey, I., Vincent Brandt, E. and Ferreira, D. (2000). Polyphenols, condensed tannins, and other natural products in Onobrychis viciifolia (Sainfoin). Journal of Agriculture and Food Chemistry 48, 3440–3447. doi:10.1021/jf000388hCrossRefGoogle ScholarPubMed
Mantle, M. and Allen, A. (1978). A colorimetric assay for glycoproteins based on the periodic acid/Schiff stain. Biochemical Society Transactions 6, 607–609.CrossRefGoogle ScholarPubMed
Menke, K. H. and Steingass, H. (1988). Estimation of the energetic feed value from chemical analysis and in vitro gas production using rumen fluid. Animal Research Development 28, 7–55.Google Scholar
Miller, H. R. P. (1984). The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology 6, 167–259. doi:10.1016/0165-2427(84)90051-5CrossRefGoogle ScholarPubMed
Miller, H. R. P, Huntley, J. F. and Wallace, G. R. (1981) Immune exclusion and mucus trapping during the rapid expulsion of Nippostrongylus braziliensis from primed rats. Immunology 44, 419–429.Google Scholar
Newlands, G. F. J., Huntley, J. F. and Miller, H. R. P. (1984). Concomitant detection of mucosal mast cells and eosinophils in the intestines of normal and Nippostrongylus-immune rats. A re-evaluation of histochemical and immunocytochemical techniques. Histochemistry 81, 585–589.CrossRefGoogle ScholarPubMed
Newlands, G. F. J., Miller, H. R. P. and Jackson, F. (1990). Immune exclusion of Haemonchus contortus larvae in the sheep: effects on gastric mucin of immunization, larval challenge and treatment with dexamethasone. Journal of Comparative Pathology 102, 433–442. doi:10.1016/S0021-9975(08)80164-8.CrossRefGoogle ScholarPubMed
Paolini, V., Bergeaud, J. P., Grisez, C., Prevot, F., Dorchies, P. and Hoste, H. (2003 a). Effects of condensed tannins on goats experimentally infected with Haemonchus contortus. Veterinary Parasitology 113, 253–261. doi:10.1016/S0304-4017(03)00064-5CrossRefGoogle ScholarPubMed
Paolini, V., Dorchies, PH. and Hoste, H. (2003 b). Effects of Sainfoin hay on gastrointestinal nematodes in goats. Veterinary Record 152, 600–601.CrossRefGoogle ScholarPubMed
Paolini, V., Fouraste, I. and Hoste, H. (2004). In vitro effects of three woody plants and Sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 129, 69–77. doi:10.1017/S0031182004005268CrossRefGoogle ScholarPubMed
Paolini, V., Prevot, F., Dorchies, PH. and Hoste, H. (2005 a). Lack of effect of quebracho and Sainfoin hay on incoming third-stage larvae of Haemonchus contortus in goats. Veterinary Journal 170, 260–263. doi:10.1016/j.tvjl.2004.05.001CrossRefGoogle ScholarPubMed
Paolini, V., De La Farge, F., Prevot, F., Dorchies, PH. and Hoste, H. (2005 b). Effects of the repeated distribution of Sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Veterinary Parasitology 127, 277–283. doi:10.1016/j.vetpar.2004.10.015CrossRefGoogle ScholarPubMed
Pemberton, A. D., Knight, P. A., Gamble, J., Colledge, W. H., Lee, J-K, Pierce, M. and Miller, H. R. P. (2004). Innate BALB/c enteric epithelial responses to Trichinella spiralis: Inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. Journal of Immunology 173, 1894–1901.CrossRefGoogle ScholarPubMed
Porter, L. J., Hrstich, L. N. and Chan, B. G. (1986). The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223–230. doi:10.1016/S0031-9422(00)94533-3CrossRefGoogle Scholar
Price, M. L. and Butler, L. G. (1977). Rapid visual estimation and spectrophotometric determination of tannin content of sorghum grain. Journal of Agricultural and Food Chemistry 25, 1268–1273.CrossRefGoogle Scholar
Ramírez-Restrepo, C. A. and Barry, T. N. (2005). Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants. Animal Feed Science and Technology 120, 179–201. doi:10.1016/j.anifeedsci.2005.01.015CrossRefGoogle Scholar
Seaton, D. S., Jackson, F., Smith, W. D. and Angus, K. W. (1989). Development of immunity to incoming radiolabelled larvae in lambs continuously infected with Trichostrongylus vitrinus. Research in Veterinary Science 46, 22–26.CrossRefGoogle ScholarPubMed
Tzamaloukas, O., Athanasiadou, S., Kyriazakis, I., Huntley, J. F. and Jackson, F. (2006). The effect of chicory (Chicorium intybus) and sulla (Hedysarium coronarium) on larval development and mucosal cell responses of growing lambs challenged with Teladorsagia circumcincta. Parasitology 132, 419–426. doi:10.1017/S0031182006001363CrossRefGoogle Scholar
Waghorn, G. (2007). Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production–progress and challenges. Animal Feed Science and Technology (in the Press) doi:10.1016/j.anifeedsci.2007.09.013Google Scholar
Young, N. M., Williams, R. E., Roy, C. and Yaguchi, M. (1982). Structural comparison of the lectin from Sainfoin (Onobrychis viciifolia) with concanavalin A and other D-mannose specific lectins. Canadian Journal of Biochemistry 60, 933–941.CrossRefGoogle ScholarPubMed