Review

Plant Condensed Tannins: Antiparasitic Activity against Internal Parasites in Herbivores

Expand
  • 1. College of Nature Conservation, Beijing Forestry University, Beijing 100083, China;
    2. Shanxi Pien Tze Huang Musk Deer Industry Limited Liability Corporations, Baoji 721000, China

Received date: 2014-04-14

  Online published: 2014-09-10

Abstract

Plant condensed tannins are widely distributed in the plant kingdom, and have capabilities of chemical defense for ingestion of herbivores. Recent years, many studies have focused on the antiparasitic capabilities of plant condensed tannins which provide a new solution for prevention of parasites infection in herbivores. It is hopeful that condensed tannins become a substitute for anthelmintic in the future. Based on the summarization of research progress, in this paper, the mechanisms of prevention of parasites infection of plant condensed tannins for herbivores were generalized to two hypothesizes, which were nutrition immunology hypothesis and metabolic block hypothesis, and the variable factors influencing the capabilities of parasite prevention were reviewed.

Cite this article

WANG Wenxia, ZHOU Ran, LIU Baoqing, LIU Shuqiang, ZHANG Dong, LI Kai, HU Defu . Plant Condensed Tannins: Antiparasitic Activity against Internal Parasites in Herbivores[J]. Chinese Journal of Animal Nutrition, 2014 , 26(9) : 2483 -2490 . DOI: 10.3969/j.issn.1006-267x.2014.09.007

References

[1] HASLAM E.Plant polyphenols (syn.vegetable tannins) and chemical defense-A reappraisal[J].Journal of Chemical Ecology,1988,14(10):1789-1802.  

[2] SCHULTZ J C.Tannin-insect interactions[M]//HEMINGWAY R W,KARCHESY J J.Chemistry and significance of condensed tannins.New York:Plenum Press,1989:417-433.

[3] HAGERMAN A E,BUTLER L G.Tannins and lignins[M]//ROSENTAL G A,BERENBAUM M R.Herbivores:their interaction with secondary plant metabolites.2nd ed.San Diego:Academic Press,1991:355-376.

[4] MOLAN A L,WAGHORN G C,MCNABB W C.Effect of condensed tannins on egg hatching and larval development of Trichostrongylus colubriformis in vitro[J].Veterinary Parasitology,2002,150(3):65-69.

[5] MUPEYO B,BARRY T N,POMROY W E,et al.Effects of feeding willow (Salix spp.) upon death of established parasites and parasite fecundity[J].Animal Feed Science and Technology,2010,164(1/2):8-20.

[6] TIBE O,SUTHERLAND I A,LESPERANCE L,et al.The effect of purified condensed tannins of forage plants from Botswana on the free-living stages of gastrointestinal nematode parasites of livestock[J].Veterinary Parasitology,2013,197(1/2):160-167.

[7] SYKES A R.Parasitism and production in farm animals[J].Animal Production,1994,59(2):155-172.  

[8] DALTON C.Internal Parasites of sheep and their control now and in the future:background information for farmers[M].2nd ed.Hamilton:Reward Publishing,2006.

[9] 杨楠,齐萌,菅复春,等.圈养野生动物肠道寄生虫感染情况调查[J].河南农业科学,2011,40(3):154-157.

[10] PRICHARD R.Anthelmintic resistance[J].Veterinary Parasitology,1994,54(1/2/3):259-268.

[11] WALLER P J.The development of anthelmintic resistance in ruminant livestock[J].Acta Tropica,1994,56(2/3):233-243.

[12] POMROY W E,HART S P,MIN B R.Rotational grazing as a parasite management tool for goats[J].Journal of Animal Science,2002,80(2):193.

[13] JACKSON F,MILLER J.Alternative approaches to control-quo vadit?[J].Veterinary Parasitology,2006,139(4):371-384.  

[14] SUTHERLAND I A,LEATHWICK D M.Anthelmintic resistance in nematode parasites of cattle:a global issue[J].Trends in Parasitology,2011,27(4):176-181.  

[15] SANGSTER N C.Anthelmintic resistance:past,present and future[J].International Journal for Parasitology,1999,29(1):115-124.  

[16] BARRY T N,MCNEILL D,MCNABB W C.Plant secondary compounds:their impact on forage nutritive value and upon animal production//Proceedings of the 19th international grassland congress.Brazil:Fundacao Estudos Agrarios Luiz Queiroz(FEALQ)Piracicaba,2001:445-452.

[17] MIN B R,POMROY W E,HART S P,et al.The effect of short-term consumption of a forage containing condensed tannins on gastro-intestinal nematode parasite infections in grazing wether goats[J].Small Ruminant Research,2004,51(3):279-283.  

[18] NIEZEN J H,WAGHORN T S,CHARLESTON W A,et al.Growth and gastrointestinal parasitism in lamb grazing one of seven herbages and dosed with larvae for six weeks[J].Journal of the Science of Food and Agriculture,1995,125:281-289.

[19] HOSKIN S O,BARRY T N,WILSON P R,et al.Effects of reducing anthelmintic input upon growth and faecal egg and larval counts in young farmed deer grazing chicory (Cichorium intybus) and perennial ryegrass (Lolium perenne)/white clover (Trifolium repens) pasture[J].The Journal of Agricultural Science,1999,132(3):335-345.  

[20] WAGHORN G C,MCNABB W C.Consequences of plant phenolic compounds for productivity and health of ruminants[J].Proceedings of the Nutrition Society,2003,62(2):383-392.  

[21] GARRY W.Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production-Progress and challenges[J].Animal Feed Science and Technology,2008,147(1/2/3):116-139.

[22] YEAP FOO L,JONES W T,PORTER L J,et al.Proanthocyanidin polymers of fodder legumes[J].Phytochemistry,1982,21(4):933-935.  

[23] JACKSON F S,BARRY T N,LASCANO C,et al.The extractable and bound condensed tannin content of leaves from tropical tree,shrub and forage legumes[J].Journal of the Science of Food and Agriculture,1996,71(1):103-110.  

[24] FRUTOS P,HERVÁS G,RAMOS G,et al.Condensed tannin content of several shrub species from a mountain area in northern Spain,and its relationship to various indicators of nutritive value[J].Animal Feed Science and Technology,2002,95(3/4):215-226.

[25] 李元恒,金龙,韩国栋,等.植物单宁在反刍动物营养和健康养殖作用中的研究进展[J].草地学报,2013,21(6):1044-1051.

[26] BARRY T N,MCNABB W C.The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants[J].British Journal of Nutrition,1999,81(4):263-272.

[27] STEPEK G,BEHNKE J M,BUTTLE D J,et al.Natural plant cysteine proteinases as anthelmintics?[J].Trends in Parasitology,2004,20(7):322-327.  

[28] BRUNETON J.Pharmacognosie:phytochimie,plantes medicinales[Z].Paris:Technique et Documentation-Lavoisier,1999:370-404.

[29] STREIT W,FENGEL D.Purified tannins from quebrachocolorado[J].Phytochemistry,1994,36(2):481-484.  

[30] PAOLINI V,FRAYSSINES A,DE LA FARGE F,et al.Effects of condensed tannins on established populations and on incoming larvae of Trichostrongylus colubriformis and Teladorsagia circumcincta in goats[J].Veterinary Research,2003,34(3):331-339.  

[31] ATHANASIADOU S,KYRIAZAKIS I,JACKSON F,et al.Effects of short-term exposure to condensed tannins on adult Trichostrongylus colubriformis[J].Veterinary Record,2000,146(25):728-732.  

[32] ATHANASIADOU S,KYRIAZAKIS I,JACKSON F,et al.Consequences of long-term feeding with condensed tannins on sheep parasitised with Trichostrongylus colubriformis[J].International Journal for Parasitology,2000,30(9):1025-1033.  

[33] PAOLINI V,BERGEAUD J P,GRISEZ C,et al.Effects of condensed tannins on goats experimentally infected with Haemonchus contortus[J].Veterinary Parasitology,2003,113(3/4):253-261.

[34] MAKKAR H P S,BLVMMEL M,BECKER K.Formation of complexes between polyvinyl pyrrolidones or polyethylene glycols and tannins,and their implication in gas production and true digestibility in in vitro techniques[J].British Journal of Nutrition,1995,73(6):897-913.  

[35] ATHANASIADOU S,KYRIAZAKIS I,JACKSON F,et al.Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep:in vitro and in vivo studies[J].Veterinary Parasitology,2001,99(3):205-219.  

[36] MOLAN A L,ALEXANDER R A,BROOKES I M,et al.Effect of an extract from sulla (Hedysarum coronarium) containing condensed tannins on the migration of three sheep gastrointestinal nematodes in vitro[J].Proceedings of the New Zealand Society of Animal Production,2000,60:21-25.

[37] MOLAN A L,DUNCAN A J,BARRY T N,et al.Effects of condensed tannins and crude sesquiterpene lactones extracted from chicory on the motility of larvae of deer lungworm and gastrointestinal nematodes[J].Parasitology International,2003,52(3):209-218.  

[38] SCHREURS N M,MOLAN A L,LOPEZ-VILLALOBOS N,et al.Effects of grazing undrenched weaner deer on chicory or perennial ryegrass/white clover pasture on the viability of gastrointestinal nematodes and lungworms[J].Veterinary Record,2002,151(12):348-353.  

[39] PAOLINI V,FOURASTE I,HOSTE H.In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes[J].Parasitology,2004,129(1):69-77.  

[40] MOLAN A L,WAGHORN G C,MIN B R,et al.The effect of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro[J].Folia Parasitologica,2000,47(1):39-44.  

[41] MOLAN A L,SIVAKUMARAN S,SPENCER P A,et al.Green tea flavan-3-ols and oligomeric pronthicyanidins inhibit the motility of infective larvae of Teladorsagia circumcincta and Trichostrongylus colubriformis in vitro[J].Research in Veterinary Science,2004,77(3):239-243

[42] MOLAN A L,MCNABB W C,HOSKIN S O,et al.Effect of condensed tannins extracted from four forages on the viability of the larvae of deer lungworms and gastro-intestinal nematodes[J].Veterinary Record,2000,147(2):44-48.  

[43] BARRAU E,FABRE N,FOURASTE I,et al.Effect of bioactive compounds from Sainfoin (Onobrychis viciifolia Scop.) on the in vitro larval migration of Haemonchus contortus:role of tannins and flavonol glycosides[J].Parasitology,2005,131(4):531-538.  

[44] NOVOBILSK A,MUELLER-HARVEY I,THAMSBORG S M.Condensed tannins act against cattle nematodes[J].Veterinary Parasitology,2011,182(2/3/4):213-220.

[45] PAOLINI V,PREVOT F,DORCHIES P,et al.Lack of effects of quebracho and sainfoin hay on incoming third stage larvae of Haemonchus contortus in goats[J].The Veterinary Journal,2005,170(2):260-263.  

[46] KABASA J D,OPUDA-ASIBO J,TER MEULEN U.The effect of oral administration of polyethylene glycol on faecal helminth egg counts in pregnant goats grazed on browse containing condensed tannins[J].Tropical Animal Health and Production,2000,32(2):73-86.  

[47] MOLAN A L,MEAGHER L P,SPENCER P A,et al.Effect of flavan-3-ols on in vitro egg hatching,larval development and viability of infective larvae of Trichostrongylus colubriformis[J].International Journal for Parasitology,2003,33(14):1691-1698.  

[48] MIN B R,BARRY T N,ATTWOOD G T,et al.The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages:a review[J].Animal Feed Science and Technology,2003,106(1/2/3/4):3-19.

[49] COOP R L,KYRIAZAKIS I K.Influence of host nutrition on the development and consequences of nematode parasitism in ruminants[J].Trends in Parasitology,2001,17(7):325-330.  

[50] TIBE O,PERNTHANER A,SUTHERLAND I,et al.Condensed tannins from Botswanan forage plants are effective priming agents of T cells in ruminants[J].Veterinary Immunology and Immunopathology,2012,146(3/4):237-244.

[51] ATHANASIADOU S,TZAMALOUKAS O,KYRIAZAKIS I,et al.Testing for direct anthelmintic effects of bioactive forages against Trichostrongylus colubriformis different in grazing sheep[J].Veterinary Parasitology,2005,127(3/4):233-243.

[52] NIEZEN J H,CHARLESTON W A G,ROBERTSON H A,et al.The effect of feeding sulla (Hedysarum coronarium) or lucerne (Medicago sativa) on lamb parasite burdens and development of immunity to gastrointestinal nematodes[J].Veterinary Parasitology,2002,105(3):229-245.  

[53] TZAMALOUKAS O,ATHANASIADOU S,KYRIAZAKIS I,et al.The consequences of short term grazing of bioactive forages on established adult and incoming larvae populations of Teladorsagia circumcincta in lambs[J].International Journal for Parasitology,2005,35(3):329-335.  

[54] ATHANASIADOU S,KYRIAZAKIS I,JACKSON F,et al.The effects of condensed tannins supplementation of foods with different protein content on parasitism,food intake and performance of sheep infected with Trichostrongylus colubriformis[J].British Journal of Nutrition,2001,86(6):697-706.  

[55] HOSTE H,JACKSON F,ATHANASIADOU S,et al.The effects of tannin-rich plants on parasitic nematodes in ruminants[J].Trends in Parasitology,2006,22(6):253-260.  

[56] BAHUAUD D,MARTINEZ-ORTIZ DE MONTELLANO C,CHAUVEAU S,et al.Effects of four tanniferous plant extracts on the in vitro exsheathment of third-stage larvae of parasitic nematodes[J].Parasitology,2006,132(4):545-554.  

[57] MORI T,MOHAMED A S A,SATO M,et al.Ellagitannin toxicity in the free-living soil-inhabiting nematode,Caenorhabditis elegans[J].Journal of Pesticide Science,2000,25(4):405-409.  

[58] MIN B R,HART S P.Tannins for suppression of internal parasites[J].Journal of Animal Science,2003,81(14):E102-E109.

[59] WAGHORN T S,MOLAN A L,DEIGHTON M,et al.In vivo anthelmintic activity of Dorycnium rectum and grape seed extract against Ostertagia (Teladorsagia) circumcincta and Trichostrongylus colubriformis in sheep[J].New Zealand Veterinary Journal,2006,54(1):21-27.  

[60] ATHANASIADOU S,GITHIORI J,KYRIAZAKIS I.Medicinal plants for helminth parasite control:facts and fiction[J].Animal,2007,1(9):1392-1400.

[61] MEAGHER L P,LANE G,SIVAKUMARAN S,et al.Characterization of condensed tannins from Lotus species by thiolytic degradation and electrospray mass spectrometry[J].Animal Feed Science and Technology,2004,117(1/2):151-163.

[62] HOSKIN S O,POMROY W R,REIJRINK I,et al.Effect of withholding anthelmintic treatment on autumn growth and internal parasitism of weaner deer grazing perennial ryegrass-based pasture or chicory[J].Proceedings of the New Zealand Society of Animal Production,2003,63:269-273.

[63] TERRILL T H,DOUGLAS G B,FOOTE A G,et al.Effect of condensed tannins upon body growth,wool growth and rumen metabolism in sheep grazing sulla (Hedysarum cornarium) and perennial pasture[J].The Journal of Agricultural Science,1992,119(2):265-273.  

[64] NIEZEN J H,ROBERTSON H A,WAGHORN G C,et al.Production,fecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages[J].Veterinary Parasitology,1998,80(1):15-27.  

[65] NIEZEN J H,WAGHORN G C,CHARLESTON W A G.Establishment and fecundity of Ostertargia circumcincta and Tricostrongylus colubriformis in lambs fed lotus (Lotus pedunculatus) or perennial ryegrass (Lolium perenne)[J].Veterinary Parasitology,1998,78(1):13-21.  

[66] BUTTER N L,DAWSON J M,WAKELIN D,et al.Effect of dietary tannin and protein concentration on nematode infection (Trichostrongylus colubriformis) in lambs[J].The Journal of Agricultural Science,2000,134(1):89-99.  

[67] HOSTE H,JACKSON F,ATHANASIADOU S,et al.The effects of tannin-rich plants on parasitic nematodes in ruminants[J].Trends in Parasitology,2006,22(6):253-261.  

[68] 周海超,魏淑东,李敏,等.基质辅助激光解吸附飞行时间质谱方法分析山竹果皮缩合单宁[J].分析化学研究简报,2010,38(10):1492-1496.

[69] WATERMAN P G.The chemical systematics of alkaloids:a review emphasising the contribution of Robert Hegnauer[J].Biochemical Systematics and Ecology,1999,27(4):395-406.  

[70] ROBBINS C T,HAGERMAN A E,AUSTIN P J,et al.Variation in mammalian physiological responses to condensed tannins and its ecological implications[J].Journal of Mammalogy,1991,72(3):480-486.  

[71] SILANIKOVE N.The physiological basis of adaptation in goats to harsh environment[J].Small Ruminant Research,2000,35(3):181-193.  
Outlines

/