Folia Parasitologica, vol. 57 (2010), issue 1

Folia Parasitologica 57[1] 62-68 (2010) | 10.14411/fp.2010.008

The effects of condensed tannins extracted from different plant species on egg hatching and larval development of Teladorsagia circumcincta (Nematoda: Trichostrongylidae)

Abdul-Lateef Molan1, Abbas Mohamed Faraj2
1 Institute of Food, Nutrition and Human Health, Massey University, Palmerston North, New Zealand
2 College of Pharmacy, Hawler Medical University, Erbil, Iraq

The effects of condensed tannins (CTs) extracted from five species of plants on egg hatching and larval development of Teladorsagia circumcincta (Stadelmann, 1894) (syn. Ostertagia circumcincta) were evaluated using in vitro bioassays. The extracts of CTs were obtained from Lotus pedunculatus (LP), Lotus corniculatus (LC), Dorycnium pentaphyllum (DP), Dorycnium rectum (DR) and Rumex obtusifolius (RO). The results of egg hatching assay showed that about 53%, 68%, 51%, 60% and 46% of the eggs hatched when in vitro incubations contained 900 mg/ml of CTs from LP, LC, DP, DR and RO, respectively (P< 0.001 relative to control incubation), while in control incubations (no CT added) 87% of the eggs hatched. In the larval development assay, development was allowed to proceed for 7 days, by which time 89% of the hatched larvae in control wells (no CTs) had reached the infective third stage (L3). In incubations containing 200 mg CT from LP, LC, DP, DR and RO/ml, about 8%, 15%, 14%, 8% and 4% of the eggs attained full development to L3 larvae, respectively (P< 0.001 relative to control incubation). Only 1% of the eggs were able to develop to L3 larvae in incubations containing 400 mg CT extracted from LC/ml, whilst in the incubations containing the same concentration of other CTs the eggs were not able to develop to L3 larvae. It seems that CTs are not only slowing down the larval development but also kill the undeveloped larvae. At 400 mg/ml, for example, CT from LP, LC, DP, DR and RO killed 67%, 48%, 68%, 93% and 91% of first-stage (L1) and second-stage (L2) larvae, respectively. This study shows that CTs are able to disrupt the life cycle of nematodes.

Keywords: Teladorsagia circumcincta, egg hatching, larval development, condensed tannins

Received: July 31, 2009; Accepted: November 11, 2009; Published: March 1, 2010


References

  1. Aerts R.J., McNabb W.C., Molan A., Brand A., Barry T.N., Peters J.S. 1999: Condensed tannins from Lotus corniculatus and Lotus pedunculatus exert different effects on the in vitro rumen degradation of ribulose-1,5-bisphosphate carboxylase/ oxygenase (Rubisco) protein. J. Sci. Food Agric. 79: 79-85 Go to original source...
  2. Athanasiadou S., Kyriazakis I., Jackson F., Coop R.L. 2000a: Consequences of long-term feeding with condensed tannins on sheep parasitised with Trichostrongylus colubriformis. Int. J. Parasitol. 30: 1025-1033 Go to original source... Go to PubMed...
  3. Athanasiadou S., Kyriazakis I., Jackson F., Coop R.L. 2000b: Effects of short-term exposure to condensed tannins on adult Trichostrongylus colubriformis. Vet. Rec. 146: 728-732 Go to original source... Go to PubMed...
  4. Athanasiadou S., Kyriazakis I., Jackson F., Coop R.L. 2001: Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: in vitro and in vivo studies. Vet. Parasitol. 99: 205-219 Go to original source... Go to PubMed...
  5. Avery L., Horvitz H.R. 1990: Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J. Exp. Zool. 64: 263-270 Go to original source... Go to PubMed...
  6. Bahuaud D., De Montellano C.M.O., Chauveau S., Prevot F., Torres -Acosta F., Fouraste I., 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 Go to original source... Go to PubMed...
  7. Barrau E., Fabre N., Fourase I., 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 Go to original source... Go to PubMed...
  8. Brunsdon R.V. 1980: Principles of helminth control. Vet. Parasitol. 6: 185-215 Go to original source...
  9. Butter N.L., Dawson J.M., Wakelin D., Buttery P.J. 2000: Effect of dietary condensed tannins on gastrointestinal nematodes. J. Agric. Sci. 137: 461-469
  10. Clausen T.P., Provenza F.D., Burritt E.A., Reichardt P.B., Bryant J.P. 1990: Ecological implications of condensed tannin structure: a case study. J. Chem. Ecol. 16: 2381-2392 Go to original source...
  11. Coop R.L., Holmes P.H. 1996: Nutrition and parasite interaction. Int. J. Parasitol. 26: 951-962 Go to original source... Go to PubMed...
  12. Foo L.Y., McNabb W.C., Waghorn G.C., Ulyatt M.J. 1997: Proanthocyanidins from Lotus pedunculatus. Phytochemistry 45: 1689-1696 Go to original source...
  13. Foo L.Y., Newman R., Waghorn G.C., McNabb W.C. 1996: Proanthocyanidins from Lotus corniculatus. Phytochemistry 41: 617-621 Go to original source...
  14. Gill J.H., Redwin J.M., Van Wyk J.A., Lacey E. 1995: Avermectin inhibition of larval development in Haemonchus contortus - effects of ivermectin resistance. Int. J. Parasitol. 25: 463-470 Go to original source... Go to PubMed...
  15. Grzywacz M. 1983: The swallowing of chemical compounds by helminths. Acta Parasitol. Pol. 28: 357-368
  16. Horigome T., Kumar R., Okamoto K . 1988: Effects of condensed tannins prepared from leaves of fodder plants on digestive enzymes in vitro and in the intestine of rats. Br. J. Nutr. 60: 275-285 Go to original source... Go to PubMed...
  17. Hoste H., Jackson F., Athanasiadou S., Thamsborg S.M., Hoskin S.O. 2006: The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends Parasitol. 22: 253-261 Go to original source... Go to PubMed...
  18. Hubert J., Kerboeuf D. 1984: A new method for culture of larvae used in diagnosis of ruminant gastrointestinal strongylosis: comparison with faecal cultures. Can. J. Comp. Med. 48: 63-71 Go to PubMed...
  19. Jackson F.S., McNabb W.C., Barry T.N., Foo Y.L., Peters J.S . 1996: The condensed tannin content of a range of subtropical and temperate forages and the reactivity of condensed tannin with ribulose-1,5-bis-phosphate carboxylase (Rubisco) protein. J. Sci. Food Agric. 72: 483-492 Go to original source...
  20. Jones W.T., Broadhurst R.B., Lyttleton J. 1976: The condensed tannins of pasture legume species. Phytochemistry 15: 1407-1409 Go to original source...
  21. Leathwick D., Pomroy W.E., Heath A. 2001: Anthelmintic resistance in New Zealand. N.Z. Vet. J. 49: 227-235 Go to original source... Go to PubMed...
  22. Marley C.L., Cook R., Keatinge R., Barrett J., Lampkin N.H. 2003: The effect of birdfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Vet. Parasitol. 112: 147-155 Go to original source... Go to PubMed...
  23. Min B.R., Hart S.P. 2003: Tannins for suppression of internal parasites. J. Anim. Sci. 81: 102-109
  24. Molan A.L., Hoskin S.O., Barry T.N., McNabb W.C. 2000a: The effect of condensed tannins extracted from four forages on deer lungworm and gastrointestinal nematode larval viability. Vet. Rec. 147: 44-48 Go to original source... Go to PubMed...
  25. Molan A.L., Meagher L.P., Spencer P.A., Sivakumaran S. 2003: Effect of flavan-3-ols on in vitro egg hatching, larval development and viability of infective larvae of Trichostrongylus colubriformis. Int. J. Parasitol. 33: 1691-1698 Go to original source... Go to PubMed...
  26. Molan A.L., Sivakumaran S., Meagher L., Lane G., Spencer P. 2004: Green tea flavan-3-ols and oligomeric proanthocyanidins inhibit the motility of infective larvae of Teladorsagia circumcincta and Trichostrongylus colubriformis in vitro. Res. Vet. Sci. 77: 239-243 Go to original source... Go to PubMed...
  27. Molan A.L., Waghorn G.C., Min B.R., McNabb W.C. 2000b: The effect of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro. Folia Parasitol. 47: 39-44 Go to original source... Go to PubMed...
  28. Molan A.L., Waghorn G.C., McNabb W.C. 2002: The impact of condensed tannins on egg hatching and larval development of Trichostrongylus colubriformis in vitro. Vet. Rec. 150: 65-69 Go to original source... Go to PubMed...
  29. Niezen J.H., Robertson H.A., Waghorn G.C., Charleston W.A.G. 1998: Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Vet. Parasitol. 80: 15-27 Go to original source... Go to PubMed...
  30. Niezen J.H., Waghorn T.S., Charleston W.A.G., Waghorn G.C. 1995: Growth and gastrointestinal nematode parasitism in lambs grazing lucerne (Medicago sativa) or sulla (Hedysarum coronarium) which contains condensed tannins. J. Agric. Sci., Camb., 125: 281-289 Go to original source...
  31. Oh H.I., Hoff J.E . 1986: Effect of condensed grape tannins on the in vitro activity of digestive proteases and activation of their zymogens. J. Food Sci. 51: 577-580 Go to original source...
  32. Paolini V., Frayssines A., De La Farge F., Dorchies P., Hoste H. 2003: Effects of condensed tannins on established populations and on incoming larvae of Trichostrongylus colubriformis and Teladorsagia circumcincta in goats. Vet. Res. 34: 331-339 Go to original source... Go to PubMed...
  33. Paolini V., Fourase I., Hoste H. 2004: In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 129: 69-77 Go to original source... Go to PubMed...
  34. Parkins J.J., Holmes P.H. 1989: Effects of gastrointestinal helminth parasites on ruminant nutrition. Nutr. Res. Rev. 2: 227-246 Go to original source... Go to PubMed...
  35. Robbins C.T., Hagerman A.E., Austin P.J., McArthur C., Hanley T.A. 1991: Variation in mammalian physiological responses to a condensed tannin and its ecological implications. J. Mammal. 72: 480-486 Go to original source...
  36. Robertson H.A., Niezen J.H., Waghorn G.C., Charleston W.A.G., Jinlong M. 1995: The effect of six herbages on liveweight gain, wool growth and faecal egg count of parasitised ewe lambs. Proc. N.Z. Soc. Anim. Prod. 55: 199-201
  37. Rogers W.P., Brooks F. 1977: The mechanism of hatching of egg of Haemonchus contortus. Int. J. Parasitol. 7: 61-65 Go to original source... Go to PubMed...
  38. Sangster N.C. 1999: Anthelmintics resistance: past, present and future. Int. J. Parasitol. 29: 115-124 Go to original source... Go to PubMed...
  39. Sommerville R.I., Rogers W.P. 1987: The nature and action of host signals. Adv. Parasitol. 26: 239-293 Go to original source... Go to PubMed...
  40. Terrill T.H., Rowan A.M., Douglas G.B., Barry T.N. 1992: Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. J. Sci. Food Agric. 58: 321-329 Go to original source...
  41. Terrill T.H., Waghorn G.C., Wooley D.J., McNabb W.C., Barry T.N. 1994: Assay and digestion of 14C-labelled condensed tannin in the gastrointestinal tract of sheep. Br. J. Nutr. 72: 467-477 Go to original source... Go to PubMed...
  42. Vlassoff A., McKenna P.B. 1994: Nematode parasites of economic importance in sheep in New Zealand. N.Z. J. Zool. 21: 1-8 Go to original source...
  43. Waghorn G.C., Molan A.L. 2001: Effect of condensed tannins in Dorycnium rectum on its nutritive value and on the development of sheep parasite larvae. Proc. N.Z. Grassl. Assoc. 63: 273-277
  44. Waghorn G.C., Shelton I.D., McNabb W.C., Mc c utecheon S.N. 1994: The effect of condensed tannins in Lotus pedunculatus on nutritive value for sheep. 2. Nitrogenous aspects. J. Agric. Sci. 123: 109-119 Go to original source...