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The effect of chicory (Cichorium intybus) and sulla (Hedysarum coronarium) on larval development and mucosal cell responses of growing lambs challenged with Teladorsagia circumcincta

  • O. TZAMALOUKAS (a1) (a2), S. ATHANASIADOU (a1), I. KYRIAZAKIS (a1) (a3), J. F. HUNTLEY (a2) and F. JACKSON (a2)...

The aim of this study was to investigate the effects of grazing different bioactive forages on acquired immunity against Teladorsagia circumcinta infection. The development of immunity was assessed by following the response of trickle-infected lambs grazing chicory (Cichorium intybus; IC), sulla (Hedysarum coronarium; IS) or grass/clover (Lolium perenne/Trifolium repens; IGC), to a single challenge infection. Parasite-naive lambs, grazing grass/clover, were also challenged with the single infection dose providing the uninfected control (UGC) group. Trickle infection significantly reduced worm establishment, inhibited larval development and increased mucosal mast cell (MMC) and globule leucocyte (GL) cells. Grazing treatment (chicory, sulla or grass/clover) significantly affected adult worm (P<0·05), late-L4 (P<0·01) and mid-L4 (P<0·01) larval-stage recoveries of the trickle-infected lambs, with IGC group always carrying higher worm burdens than either IC or IS lambs. MMC and GL cells of trickle-infected lambs were positively correlated with the proportion of early-L4 worms recovered and negatively correlated with both the proportion of adult worms recovered and the total worm establishment, suggesting that the observed effects were due to an enhanced immune response. The results suggest elevated immune responses against T. circumcincta infections in growing lambs grazing on either sulla or chicory compared to those grazing on grass/clover, probably due to differences in forage nutritional values.

Corresponding author
Scottish Agricultural College, Sir Stephen Watson Building, Bush Estate, Penicuik, Midlothian EH26 0PH, UK. Tel: +44 131 535 3058. Fax: +44 131 535 3121. E-mail:
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AGRICULTURAL AND FOOD RESEARCH COUNCIL ( 1993). Energy and Protein Requirements of Ruminants. An Advisory Manual Prepared by AFRC Technical Committee on Responses to Nutrients. CAB International, Wallingford, UK.
Athanasiadou, S., Tzamaloukas, O., Kyriazakis, I., Jackson, F. and Coop, R. L. ( 2005). Testing for direct anthelmintic effects of bioactive forages against Trichostrongylus colubriformis in grazing sheep. Veterinary Parasitology 127, 233243. DOI: 10.1016/j.vetpar.2004.09.031
Balic, A., Bowles, V. M. and Meeusen, E. N. T. ( 2000). The immunology of gastrointestinal nematode infections in ruminants. Advances in Parasitology 45, 181241.
Barrett, M., Jackson, F. and Huntley, J. F. ( 1998). Pathogenicity and immunogenicity of different isolates of Teladorsagia circumcincta. Veterinary Parasitology 76, 95104.
Barry, T. N. ( 1998). The feeding value of chicory (Cichorium intybus) for ruminant livestock. Journal of Agricultural Science, Cambridge 131, 251257.
Bown, M. D., Poppi, D. P. and Sykes, A. R. ( 1991). The effects 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, 253267.
Christie, M. and Jackson, F. ( 1982). Specific identification of strongyle eggs in small samples of sheep faeces. Research in Veterinary Science 32, 113117.
Coop, R. L. and Kyriazakis, I. ( 1999). Nutrition-parasite interaction. Veterinary Parasitology 84, 187204.
Coop, R. L., Sykes A. R. and Angus, K. W. ( 1982). The effect of 3 levels of intake of Ostertagia circumcincta larvae on growth rate, food intake, and body composition of growing lambs. Journal of Agricultural Science, Cambridge 98, 247255.
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, 2429.
Denham, D. A. ( 1969). The development of Ostertagia circumcincta in lambs. Journal of Helminthology 43, 299310.
Fraser, T. J., Cosgrove, G. P., Thomas, W. J., Stevens, D. R. and Hickey, M. J. ( 1988). Performance of Grasslands Puna chicory. Proceedings of the New Zealand Grassland Association 49, 193196.
Houdijk, J. G. M., Kyriazakis, I., Coop, R. L. and Jackson, F. ( 2001). The expression of immunity to Teladorsagia circumcincta in ewes and its relationship to protein nutrition depend on body protein reserves. Parasitology 122, 661672.
Huntley, J. F., Patterson, M., Mackellar, A., Jackson, F., Stevenson, L. M. and Coop, R. L. ( 1995). A comparison of the mast cell and eosinophil responses of sheep and goats to gastrointestinal nematode infections. Research in Veterinary Science 58, 510.
Jackson, F. and Coop, R. L. ( 2000). The development of anthelmintic resistance in sheep nematodes. Parasitology 120 (Suppl.), S95S107.
Jackson, E., Jackson, F. and Smith, W. D. ( 1984). Comparison of saline incubation and pepsin digestion as methods for recovering Ostertagia circumcincta larvae from the abomasum of sheep. Research in Veterinary Science 36, 380381.
Komolong, M., Nicol, A. M., Poppi, D. P., Fraser, T. J. and Kirsopp, S. ( 1992). Nutrient supply for lamb growth from Grasslands Puna chicory (Cichorium intybus) and wana cocksfoot (Dactylis glomerata). Proceedings of the New Zealand Society of Animal Production 52, 8587.
Macaldowie, C., Jackson, F., Huntley, J., Mackellar, A. and Jackson, E. ( 2003). A comparison of larval development and mucosal mast cell responses in worm-naive goat yearlings, kids and lambs undergoing primary and secondary challenge with Teladorsagia circumcincta. Veterinary Parasitology 114, 113. DOI: 10.1016/S0304-4017(03)00110-9.
Marley, C. L., Cook, R., Keatinge, R., Barrett, J. and Lampkin, N. H. ( 2003). The effect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Veterinary Parasitology 112, 147155. DOI: 10.1016/S03044017(02)00412-2.
Min, B. R., Barry, T. N., Attwood, G. T. and McNabb, W. C. ( 2003). The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Animal Feed Science and Technology 106, 319. DOI: 10.1016/S03778401(03)00041-5.
MINISTRY OF AGRICULTURE, FOOD AND FISHERIES ( 1986). The Analysis of Agricultural Materials. A Manual of the Analytical Methods used by the Agricultural Development and Advisory Service, 3rd Edn. Her Majesty's Stationery Office, London.
Molan, A. L., Alexander, R. A., Brookes, I. M. and McNabb, W. C. ( 2000). Effects of an extract from sulla (Hedysarum coronarium) containing condensed tannins on the migration of three sheep gastrointestinal nematodes in vitro. Proceedings of the New Zealand Society of Animal Production 60, 2125.
Molan, A. L., Duncan, A. J., Barry, T. N. 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, 209218. DOI: 10.1016/S1383-5769(03)00011-4.
Niezen, J. H., Waghorn, T. S., Raufaut, K., Robertson, H. A. and McFarlane, R. G. ( 1994). Lamb weight gain and faecal egg count when grazing one of seven herbages and dosed with larvae for six weeks. Proceedings of the New Zealand Society of Animal Production 54, 1518.
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 Agricultural Science, Cambridge 125, 281289.
Niezen, J. H., Charleston, W. A. G., Robertson, H. A., Shelton, D., Waghorn, G. C. and 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.
Porter, L. J., Hrstich, L. N. and Chan, B. G. ( 1986). The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223230.
Scales, G. H., Knight, T. L. and Saville, D. J. ( 1994). Effect of herbage species and feeding level on internal parasites and production performance of grazing lambs. New Zealand Journal of Agricultural Research 38, 237247.
Smith, W. D., Jackson, F., Jackson, E. and Williams, J. ( 1985). Age immunity to Ostertagia circumcincta: Comparison of the local immune responses of four-and-a-half and ten-month-old lambs. Journal of Comparative Pathology 95, 235245.
Stear, M. J., Strain, S. and Bishop, S. C. ( 1999). How lambs control infection with Ostertagia circumcincta. Veterinary Immunology and Immunopathology 72, 213218.
Tzamaloukas, O., Athanasiadou, S., Kyriazakis, I., Jackson, F. and Coop, R. L. ( 2005). The consequences of short-term grazing of bioactive forages on established adult and incoming larvae populations of Teladorsagia circumcincta in lambs. International Journal for Parasitology 35, 329335. DOI: 10.1016/j.ijpara.2004.11.013.
van Houtert, M. F. J., Barger, I. A., Steel, J. W., Windon, R. G. and Emery, D. L. ( 1995). Effects of dietary protein intake on responses of young sheep to infection with Trichostrongylus colubriformis. Veterinary Parasitology 56, 163180.
van Soest, P. J. ( 1982). Nutritional Ecology of the Ruminant. O & B Books Inc., Corvallis, USA.
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