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Plant secondary metabolites: antiparasitic effects and their role in ruminant production systems

Published online by Cambridge University Press:  07 March 2007

Spiridoula Athanasiadou  and
Ilias Kyriazakis
Spiridoula Athanasiadou*
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK
Ilias Kyriazakis
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK
*
*Corresponding author: Dr Spiridoula Athanasiadou, fax +44 131 535 3221, email s.athanasiadou@ed.sac.ac.uk
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Abstract

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The purported antiparasitic properties of plant secondary metabolites (PSM) have been the cause of controversy amongst the scientific community. Despite long-standing knowledge of the prophylactic and therapeutic properties of PSM-rich extracts, which comes mainly from ethnoveterinary sources, the scientific evidence of the antiparasitic effects of PSM is inconsistent. In the first part of the present paper the causes of this controversy are addressed, and the evidence available on the antiparasitic effects of PSM is critically examined. The focus is on examples of the antiparasitic activity of PSM against helminth nematodes. The conclusion is that PSM can have antiparasitic properties, which depend on their structure, level of ingestion and availability within the gastrointestinal tract of the animal. The second part is an appraisal of the potential role of PSM for parasite control in ruminant production systems. Despite their antiparasitic properties, PSM consumption does not necessarily have positive consequences in parasitised herbivores, as excessive consumption of PSM can adversely affect herbivore fitness and survival, through their anti-nutritional properties. For this reason it is suggested that the antiparasitic properties of PSM should be assessed at the same time as their anti-nutritional effects. The same measure, e.g. the performance of parasitised hosts, should be used when assessing these properties. The assessment of the costs and benefits suggests that parasitised herbivores can benefit from the long-term consumption of PSM only if the antiparasitic benefits outweigh the anti-nutritional costs of PSM. In addition, it is proposed that parasitised animals might be able to benefit from PSM consumption even if their performance is impaired, as long as the latter is a short-term compromise that leads to long-term benefits.

Keywords

Bioactive plantsGastrointestinal parasitesHelminthsPlant secondary metabolites
Type
Symposium on ‘Plants as animal foods: a case of catch 22?’
Information
Proceedings of the Nutrition Society , Volume 63 , Issue 4 , November 2004 , pp. 631 - 639
Copyright
Copyright © The Nutrition Society 2004

References

Akhtar, MS & Ahmad, I (1992) Comparative efficacy of Mallotus philippinensis fruit (Kamala) or Nilzan drug against gastrointestinal cestodes in Beetal goats. Small Ruminants Research 8, 121–128.CrossRefGoogle Scholar
Applebaum, SW & Birk, Y (1979) Saponins Herbivores. Their Interactions with Secondary Plant Metabolites, pp. 539–566 [Rosental, GA and Janzen, TH, editors] London: Academic Press.Google Scholar
Athanasiadou, S, Kyriazakis, I, Jackson, F & Coop, RL (2000) Consequences of long-term feeding with condensed tannins on sheep parasitised with Trichostrongylus colubriformis. International Journal for Parasitology 30, 1025–1033.CrossRefGoogle ScholarPubMed
Athanasiadou, S, Kyriazakis, I, Jackson, F & Coop, RL (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
Athanasiadou, S, Tzamaloukas, O, Kyriazakis, I, Jackson, F & Coop, RL (2004) Direct effects of bioactive forages in sheep infected with Trichostrongylus colubriformis Proceedings of the British Society of Animal Science 52.Google ScholarPubMed
Barry, TN (1998) The feeding value of chicory ( Cichorium intybus ) for ruminant livestock. Journal of Agricultural Science, Cambridge 131, 251–257.CrossRefGoogle Scholar
Barry, TN & Duncan, SJ (1984) The role of condensed tannins in the nutritional value of Lotus pedunculatus 1. Voluntary intake. British Journal of Nutrition 51, 485–491.CrossRefGoogle ScholarPubMed
Barry, TN & McNabb, WC (1999) The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. British Journal of Nutrition 81, 263–272.CrossRefGoogle ScholarPubMed
Bernays, EA, Driver, GC & Bilgener, M (1989) Herbivores and plant tannins. Advances in Ecological Research 19, 263–302.CrossRefGoogle Scholar
Butter, NL, Dawson, JM, Wakelin, D & Buttery, PJ (2000)Effect of dietary tannin and protein concentration on nematode infection ( Trichostrongylus colubriformis ) in lambs. Journal of Agricultural Science, Cambridge 134, 89–99.CrossRefGoogle Scholar
Butter, NL, Dawson, JM, Wakelin, D & Buttery, PJ (2001) Effect of dietary condensed tannins on gastrointestinal nematodes. Journal of Agricultural Science, Cambridge 137, 461–469.CrossRefGoogle Scholar
Clark, AM (1996) Natural products as a resource for new drugs. Pharmaceutical Research 13, 1133–1141.CrossRefGoogle ScholarPubMed
Conn, EE (1979) Cyanide and cyanogenic glycosides Herbivores. Their Interactions with Secondary Plant Metabolites pp. 387–412 [Rosental, GA and Janzen, TH, editors]. London: Academic Press.Google Scholar
Coop, RL & Kyriazakis, I (1999) Nutrition-parasite interaction. Veterinary Parasitology 84, 187–204.CrossRefGoogle ScholarPubMed
Coop, RL & Kyriazakis, I (2001) Influence of host nutrition on the development and consequences of nematode parasitism in livestock. Trends in Parasitology 17, 325–330.CrossRefGoogle Scholar
Coop, RL, Sykes, AR & Angus, KW (1982) The effect of three levels of intake of Ostertagia circumcincta larvae on growth rate, food intake and body composition of growing lambs. Journal of Agricultural Science, Cambridge 98, 247–255.CrossRefGoogle Scholar
Dawson, JM, Buttery, PJ, Jenkins, D, Wood, CD & Gill, M (1999) Effects of dietary Quebracho tannin on nutrient utilisation and tissue metabolism in sheep and rats. Journal of the Science of Food and Agriculture 79, 1423–1430.3.0.CO;2-8>CrossRefGoogle Scholar
Githiori, JB, Hoglund, J, Waller, PJ & Baker, RL (2002) Anthelmintic activity of preparations derived from Myrsine africana and Rapanea melanophloeos against the nematode parasite, Haemonchus contortus of sheep. Journal of Ethnopharmacology 80, 187–191.CrossRefGoogle ScholarPubMed
Gray, GD (1997) The use of genetically resistant sheep to control nematode parasitism. Veterinary Parasitology 72, 345–366.CrossRefGoogle ScholarPubMed
Guarrera, PM (1999) Traditional antihelmintic, antiparasitic and repellent uses of plants in Central Italy. Journal of Ethnopharmacology 68, 183–192.CrossRefGoogle ScholarPubMed
Hagerman, AE (1989) Chemistry of tannin-protein complexation. In Chemistry and Significance of Condensed Tannins, pp. 323–333 [Hemingway, RW and Karchesy, JJ, editors] New York and London: Plenum Press.CrossRefGoogle Scholar
Hagerman, AE & Butler, LG (1991) Tannins and lignins In Herbivores: Their Interaction with Secondary Plant Metabolites, pp. 355–376 [Rosental, GA and Berenbaum, MR, editors] San Diego, CA: Academic Press.CrossRefGoogle Scholar
Harborne, JB (1999) An overview of antinutritional factors in higher plants Secondary Plant Products. Antinutritional and Beneficial Actions in Animal Feeding, pp. 7–16 Caygill, JC and Mueller-Harvey, I, editors] Nottingham: Nottingham University Press.Google Scholar
Hoskin, SO, Barry, TN, Wilson, PR, Charleston, WAG & Hodgson, J (1999) Effects of reducing anthelmintic input upon growth and faecal egg and larval counts in young farmed deer grazing chicory ( Chicorium intybus ) and perennial ryegrass ( Lolium perenne )/white clover ( Trifolium repens ) pasture. Journal of Agricultural Science, Cambridge 132, 335–345.CrossRefGoogle Scholar
Houdijk, JGM & Athanasiadou, S (2003) Direct and indirect effects of host nutrition on ruminant gastrointestinal nematodes. In Matching Herbivore Nutrition to Ecosystems Biodiversity, pp. 213–236 [Mannetje, Lt', Ramirez-Aviles, L, Sandoval-Castro, and Ku-Vera, JC, editors]. Yucatan, Mexico: Universita Autonoma de Yucatan.Google Scholar
Houdijk, JGM, Jessop, NS & Kyriazakis, I (2001) Nutrient partitioning between reproductive and immune functions in animals. Proceedings of the Nutrition Society 60, 515–525.CrossRefGoogle ScholarPubMed
Huffman, MA (2003) Animal self-medication and ethno-medicine: exploration and exploitation of the medicinal properties of plants. Proceedings of the Nutrition Society 62, 371–381.CrossRefGoogle ScholarPubMed
Hutchings, MR, Athanasiadou, S, Kyriazakis, I & Gordon, IJ (2003) Can animals use foraging behaviour to combat parasites. Proceedings of the Nutrition Society 62, 361–370.CrossRefGoogle ScholarPubMed
Ibrahim, AM (1992) Anthelmintic activity of some Sudanese anthelmintic plants. Phytotherapy Research 6, 155–157.CrossRefGoogle Scholar
International Institute of Rural Reconstruction (1994) Ethnoveterinary Medicine in Asia. An Information Kit on Traditional Animal Health and Care Practices, 2, Ruminants Silang, Cavite, The Phillippines International Institute of Rural Reconstruction.Google Scholar
Jackson, F & Coop, RL (2000) The development of anthelmintic resistance in sheep nematodes. Parasitology 120, S95–S107.CrossRefGoogle ScholarPubMed
Julien, J, Gasquet, M, Maillard, C, Balansard, G, Timon-David, P (1985) Extracts of the ivy plant, Hedera helix, and their anthelminthic activity on liver flukes. Plant Medica 3, 205–208.CrossRefGoogle Scholar
Karban, R, Agrawal, AA, Thaler, JS & Adler, LS (1999) Induced plant responses and information content about risk of herbivory. Trends in Ecology and Evolution 14, 443–447.CrossRefGoogle ScholarPubMed
Ketzis, JK, Taylor, A, Bowman, DD, Brown, DL, Warnick, LD & Erb, HN (2002) Chenopodium ambrosioides and its essential oil as treatments for Haemonchus contortus and mixed adult-nematode infections in goats. Small Ruminant Research 44, 193–200.CrossRefGoogle Scholar
Larsen, M (1999) Biological control of helminths. International Journal for Parasitology 29, 139–146.CrossRefGoogle ScholarPubMed
Lorimer, SD, Perry, NB, Foster, LM & Burgess, EJ (1996) A nematode larval motility inhibition assay for screening plant extracts and natural products. Journal of Agriculture and Food Chemistry 44, 2842–2845.CrossRefGoogle Scholar
Mabry, TJ & Gill, JE (1979) Sesquiterpenes lactones and other terpenoids. In Herbivores. Their Interactions with Secondary Plant Metabolites, 501–537 [Rosental, GA and Janzen, TH, editors] London: Academic Press.Google Scholar
Marley, CL, Cook, R, Keatinge, R, Barrett, J & Lampkin, NH (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, 147–155.CrossRefGoogle ScholarPubMed
Milgate, J & Roberts, DCK (1995) The nutritional and biological significance of saponins. Nutrition Research 15, 1223–1249.CrossRefGoogle Scholar
Min, BR, Barry, TN, Attwood, GT & McNabb, WC (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, 3–19.CrossRefGoogle Scholar
Min, BR, Pomroy, WE, Hart, SP & 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, 279–283.CrossRefGoogle Scholar
Mohamed, ASA, Mori, T, Islam, SQ, Sato, M & Yamasaki, T (2000) Lethal activity of gallo- and condensed tannins against the free-living soil-inhabiting nematode Caenorhabditis elegans. Journal of Pesticide Science 25, 410–415.CrossRefGoogle Scholar
Molan, A, Waghorn, GC, Min, BR & McNabb, WC (2000) The effects of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro. Folia Parasitologica 47, 39–44.CrossRefGoogle ScholarPubMed
Molan, AP, Duncan, A, Barry, TN & McNabb, WC (2003) Effects of condensed tannins and sesquiterpene lactones extracted from chicory on the viability of deer lungworm larvae. Proceedings of the New Zealand Society of Animal Production 60, 26–29.Google Scholar
Mueller-Harvey, I & McAllan, AB (1992) Tannins: their biochemistry and nutritional properties. Advances in Plant Cell Biochemistry and Biotechnology 1, 151–217.Google Scholar
Niezen, JH, Charleston, WAG, Hodgson, J & Waghorn, TS (1993) Effect of four grass species on lamb parasitism and growth. Proceedings of the New Zealand Grassland Association 55, 203–206.CrossRefGoogle Scholar
Niezen, JH, Charleston, WAG, Robertson, HA, Shelton, D, Waghorn, GC & 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, 229–245.CrossRefGoogle ScholarPubMed
Niezen, JH, Robertson, HA, Waghorn, GC & Charleston, WAG (1998 a) Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Veterinary Parasitology 80, 15–27.CrossRefGoogle ScholarPubMed
Niezen, JH, Waghorn, GC & Charleston, WAG (1998 b) Establishment and fecundity of Ostertagia circumcincta and Trichostrongylus colubriformis in lambs fed lotus ( Lotus pedunculatus ) or perennial ryegrass ( Lolium perenne ). Veterinary Parasitology 78, 13–21.CrossRefGoogle ScholarPubMed
Niezen, JH, Waghorn, TS, Charleston, WAG & Waghorn, GC (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, 281–289.CrossRefGoogle Scholar
Niezen, JH, Waghorn, TS, Raufautk, K, Robertson, HA & McFarlane, RG (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, 15–18.Google Scholar
Paolini, V, Dorchies, P & Hoste, H (2003) Effects of sainfoin hay on gastrointestinal nematode infections in goats. Veterinary Record 152, 600–601.CrossRefGoogle ScholarPubMed
Provenza, FD, Burritt, EA, Clausen, TP, Bryant, JP, Reichardt, PB & Distel, RA (1990) Conditioned flavour aversion: a mechanism for goats to avoid condensed tannins in blackbrush. American Naturalist 136, 810–828.CrossRefGoogle Scholar
Reed, JD (1995) Nutritional toxicology of tannins and related polyphenols in forage legumes. Journal of Animal Science 73, 1516–1528.CrossRefGoogle ScholarPubMed
Robertson, HA, Niezen, JH, Waghorn, GC, Charleston, WAG & Jinlong, M (1995) The effect of six herbages on liveweight gain, wool growth and faecal egg count of parasitised ewe lambs. Proceedings of the New Zealand Society of Animal Production 55, 199–201.Google Scholar
Satou, T, Akao, N, Matsuhashi, R, Koike, K, Fujita, K & Nikaido, T (2002) Inhibitory effect of isoquinoline alkaloids on movement of second-stage larvae of Toxocara canis. Biological & Pharmaceutical Bulletin 25, 1651–1654.CrossRefGoogle ScholarPubMed
Satrija, F, Nansen, P, Bjorn, H, Murtini, S & He, S (1994) Effects of papaya latex against Ascaris suum naturally infected pigs. Journal of Helminthology 68, 343–346.CrossRefGoogle ScholarPubMed
Silanikove, N, Perevolotsky, A & Provenza, FD (2001) Use of tannin-binding chemicals to assay for tannins and their negative post-ingestive effects in ruminants. Animal Feed Science and Technology 91, 69–81.CrossRefGoogle Scholar
Smith, WD (1999) Prospects for vaccines of helminth parasites of grazing ruminants. International Journal for Parasitology 29, 17–24.CrossRefGoogle ScholarPubMed
Sykes, AR (1994) Parasitism and production in farm animals. Animal Production 59, 155–172.Google Scholar
Terrill, TH, Waghorn, GC, Wooley, DJ, McNabb, WC & Barry, TN (1994) Assay and digestion of 14 C-labelled condensed tannins in the gastrointestinal tract of sheep. British Journal of Nutrition 72, 467–477.CrossRefGoogle Scholar
Tzamaloukas, O, Athanasiadou, S, Kyriazakis, I, Jackson, F & Coop, RL (2004) Effects of short-term grazing on bioactive forages on lambs artificially infected with Teladorsagia circumicncta Proceedings of the British Society of Animal Science, 6.Google Scholar
Urquart, GM, Armour, J, Duncan, JL, Dunn, AM & Jennings, FW (1996) Veterinary Helminthology Parasitology 10–26 Urquart GM Oxford Blackwell.Google Scholar
Villalba, JJ & Provenza, FD (2002) Polyethylene glycol influences selection of foraging location by sheep consuming quebracho tannin. Journal of Animal Science 80, 1846–1851.CrossRefGoogle ScholarPubMed
Waghorn, GC & McNabb, WC (2003) Consequences of plant phenolic compounds for productivity and health of ruminants. Proceedings of the Nutrition Society 62, 383–392.CrossRefGoogle ScholarPubMed