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The Effects of Thyme and Cinnamon Essential Oils on Performance, Rumen Fermentation and Blood Metabolites in Holstein Calves Consuming High Concentrate Diet

  • Vakili, A.R. (Department of Animal Science, Ferdowsi University of Mashhad) ;
  • Khorrami, Behzad (Department of Animal Science, Ferdowsi University of Mashhad) ;
  • Mesgaran, M. Danesh (Department of Animal Science, Ferdowsi University of Mashhad) ;
  • Parand, E. (Department of Animal Science, Ferdowsi University of Mashhad)
  • 투고 : 2012.11.13
  • 심사 : 2013.01.31
  • 발행 : 2013.07.01

초록

Essential oils have been shown to favorably effect in vitro ruminal fermentation, but there are few in vivo studies that have examined animal responses. The objective of this study was to evaluate the effects of thyme (THY) and cinnamon (CIN) essential oils on feed intake, growth performance, ruminal fermentation and blood metabolites in feedlot calves fed high-concentrate diets. Twelve growing Holstein calves ($213{\pm}17kg$ initial BW) were used in a completely randomized design and received their respective dietary treatments for 45 d. Treatments were: 1-control (no additive), 2-THY (5 g/d/calf) and 3-CIN (5 g/d/calf). Calves were fed ad libitum diets consisting of 15% forage and 85% concentrate, and adapted to the finishing diet by gradually increasing the concentrate ratio with feeding a series of transition diets 5 wk before the experiment started. Supplementation of THY or CIN did not affect DMI and ADG, and feed efficiency was similar between treatment groups. There were no effects of additives on ruminal pH and rumen concentrations of ammonia nitrogen and total VFA; whereas molar proportion of acetate and ratio of acetate to propionate decreased, and the molar proportion of propionate increased with THY and CIN supplementation. Rumen molar concentration of butyrate was significantly increased by adding CIN compared to control; but no change was observed with THY compared with control group. No effects of THY, or CIN were observed on valerate, isobutyrate or isovalerate proportions. Plasma concentrations of glucose, cholesterol, triglyceride, urea-N, ${\beta}$-hydroxybutyrate, alanine aminotransferase and aspartate aminotransferase were not changed by feeding THY or CIN. Results from this study suggest that supplementing a feedlot finishing diet with THY or CIN essential oil might be useful as ruminal fermentation modifiers in beef production systems, but has minor impacts on blood metabolites.

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참고문헌

  1. Allen, M. S. 1997. Relationship between fermentation acid production in the rumen and the requirement for physically effective fiber. J. Dairy Sci. 80:1447-1462. https://doi.org/10.3168/jds.S0022-0302(97)76074-0
  2. Allen, M. S. 2000. Effects of diet on short-term regulation of feed intake by lactating dairy cattle. J. Dairy Sci. 83:1598-1624. https://doi.org/10.3168/jds.S0022-0302(00)75030-2
  3. Beauchemin, K. A., and S. M. McGinn. 2005. Methane emissions from feedlot cattle fed barley or corn diets. J. Anim. Sci. 83:653-661.
  4. Benchaar, C., and H. Greathead. 2011. Essential oils and opportunities to mitigate enteric methane emissions from ruminants. Anim. Feed. Sci. Technol. 166-167:338-355. https://doi.org/10.1016/j.anifeedsci.2011.04.024
  5. Benchaar, C., J. L. Duynisveld, and E. Charmley. 2006a. Effects of monensin and increasing dose levels of a mixture of essential oil compounds on intake, digestion and growth performance of beef cattle. Can. J. Anim. Sci. 86:91-96.
  6. Benchaar, C., H. V. Petit, R. Berthiaume, D. R. Ouellet, J. Chiquette, and P. Y. Chouinard. 2007. Effects of essential oils on digestion, ruminal fermentation, rumen microbial populations, milk production, and milk composition in dairy cows fed alfalfa silage or corn silage. J. Dairy Sci. 90:886-897. https://doi.org/10.3168/jds.S0022-0302(07)71572-2
  7. Benchaar, C., H. V. Petit, R. Berthiaume, T. D. Whyte, and P. Y. Chouinard. 2006b. Effects of addition of essential oils and monensin premix on digestion, ruminal fermentation, milk production and milk composition in dairy cows. J. Dairy Sci. 89:4352-4364. https://doi.org/10.3168/jds.S0022-0302(06)72482-1
  8. Benchaar, C., S. Calsamiglia, A. V. Chaves, G. R. Fraser, D. Colombatto, T. A. McAllister, and K. A. Beauchemin. 2008. A review of plant-derived essential oils in ruminant nutrition and production. Anim. Feed Sci. Technol. 145:209-228. https://doi.org/10.1016/j.anifeedsci.2007.04.014
  9. Bergen, W. G., and D. B. Bates. 1984. Ionophores: their effect on production efficiency and mode of action. J. Anim. Sci. 58:1465-1483.
  10. Burt, S. 2004. Essential oils: their antibacterial properties and potential applications in foods-A review. Int. J. Food Microbiol. 94:223-253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
  11. Busquet, M., S. Calsamiglia, A. Ferret, and C. Kamel. 2006. Plant extracts affect in vitro rumen microbial fermentation. J. Dairy Sci. 89:761-771. https://doi.org/10.3168/jds.S0022-0302(06)72137-3
  12. Busquet, M., S. Calsamiglia, A. Ferret, P. W. Cardozo, and C. Kamel. 2005. Effects of cinnamaldehyde and garlic oil on rumen microbial fermentation in a dual flow continuous culture. J. Dairy Sci. 88:2508-2516. https://doi.org/10.3168/jds.S0022-0302(05)72928-3
  13. Calsamiglia, S., M. Busquet, P. Cardozo, L. Castillejos, and A. Ferret. 2007. Essential oils as modifiers of rumen microbial fermentation: a review. J. Dairy Sci. 90:2580-2595. https://doi.org/10.3168/jds.2006-644
  14. Cardozo, P. W., S. Calsamiglia, A. Ferret, and C. Kamel. 2004. Effects of plant extracts on ruminal protein degradation and fermentation profiles in continuous culture. J. Anim. Sci. 82:3230-3236.
  15. Cardozo, P. W., S. Calsamiglia, A. Ferret, and C. Kamel. 2005. Screening for the effects of natural plant extracts at different pH on in vitro rumen microbial fermentation of a high-concentrate diet for beef cattle. J. Anim. Sci. 83:2572-2579.
  16. Cardozo, P. W., S. Calsamiglia, A. Ferret, and C. Kamel. 2006. Effects of alfalfa extract, anise, capsicum, and a mixture of cinnamaldehyde and eugenol on ruminal fermentation and protein degradation in beef heifers fed a high-concentrate diet. J. Anim. Sci. 84:2801-2808. https://doi.org/10.2527/jas.2005-593
  17. Castillejos, L., S. Calsamiglia, and A. Ferret. 2006. Effect of essential oils active compounds on rumen microbial fermentation and nutrient flow in in vitro systems. J. Dairy Sci. 89:2649-2658. https://doi.org/10.3168/jds.S0022-0302(06)72341-4
  18. Castillejos, L., S. Calsamiglia, A. Ferret, and R. Losa. 2005. Effects of a specific blend of essential oil compounds and the type of diet on rumen microbial fermentation and nutrient flow from a continuous culture system. Anim. Feed Sci. Technol. 119:29-41. https://doi.org/10.1016/j.anifeedsci.2004.12.008
  19. Castillejos, L., S. Calsamiglia, J. Martin-Ereso, and H. Ter Wijlen. 2008. In vitro evaluation of effects of ten essential oils at three doses on ruminal fermentation of high concentrate feedlot-type diets. Anim. Feed Sci. Technol. 145:259-270. https://doi.org/10.1016/j.anifeedsci.2007.05.037
  20. Chaves, A. V., K. Stanford, M. E. R. Dugan, L. L. Gibson, T. A. McAllister, F. Van Herk, and C. Benchaar. 2008a. Effects of cinnamaldehyde, garlic and juniper berry essential oils on rumen fermentation, blood metabolites, growth performance, and carcass characteristics of growing lambs. Livest. Sci. 117:215-224. https://doi.org/10.1016/j.livsci.2007.12.013
  21. Chaves, A. V., K. Stanford, L. L. Gibson, T. A. McAllister, and C. Benchaar. 2008b. Effects of carvacrol and cinnamaldehyde on intake, rumen fermentation, growth performance, and carcass characteristics of growing lambs. Anim. Feed Sci. Technol. 145:396-408. https://doi.org/10.1016/j.anifeedsci.2007.04.016
  22. Davidson, S., B. A. Hopkins, D. E. Diaz, S. M. Bolt, C. Brownie, V. Fellner, and L. W. Whitlow. 2003. Effects of amounts and degradability of dietary protein on lactation, nitrogen utilization, and excretion in early lactation Holstein cows. J. Dairy Sci. 86:1681-1689. https://doi.org/10.3168/jds.S0022-0302(03)73754-0
  23. Devant, M., A. Anglada, and A. Bach. 2007. Effects of plant extract supplementation on rumen fermentation and metabolism in young Holstein bulls consuming high levels of concentrate. Anim. Feed Sci. Technol. 137:46-57. https://doi.org/10.1016/j.anifeedsci.2006.10.003
  24. Evans, J. D., and S. A. Martin. 2000. Effects of thymol on ruminal microorganisms. Curr. Microbiol. 41:336-340. https://doi.org/10.1007/s002840010145
  25. Fandino, I., S. Calsamiglia, A. Ferret, and M. Blanch. 2008. Anise and capsicum as alternatives to monensin to modify rumen fermentation in beef heifers fed a high concentrate diet. Anim. Feed Sci. Technol. 145:409-417. https://doi.org/10.1016/j.anifeedsci.2007.04.018
  26. Fraser, G. R., A. V. Chaves, Y. Wang, T. A. McAllister, K. A. Beauchemin, and C. Benchaar. 2007. Assessment of the effects of cinnamon leaf oil on rumen microbial fermentation using two continuous culture systems. J. Dairy Sci. 90:2315-2328. https://doi.org/10.3168/jds.2006-688
  27. Geraci, J. I., A. D. Garciarena, G. A. Gagliostro, K. A. Beauchemin, and D. Colombatto. 2012. Plant extracts containing cinnamaldehyde, eugenol and capsicum oleoresin added to feedlot cattle diets: Ruminal environment, short term intake pattern and animal performance. Anim. Feed Sci. Technol. 176:123-130. https://doi.org/10.1016/j.anifeedsci.2012.07.015
  28. Grigore, A., I. Paraschiv, S. Colceru-Mihul, C. Bubueanu, E. Draghichi, and M. Ichim. 2010. Chemical composition and antioxidant activity of Thymus vulgaris L. volatile oil obtained by two different methods. Romanian Biotechnol. Lett. 15:5436-5443.
  29. Hino, T., and J. B. Russell. 1985. Effect of reducing-equivalent disposal and NADH/NAD on deamination of amino acids by intact rumen microorganisms and their cell extracts. Appl. Environ. Microbiol. 50:1368-1374.
  30. Hristov, A. N., T. A. McAllister, F. H. Van Herk, K. J. Cheng, C. J. Newbold, and P. R. Cheeke. 1999. Effect of Yucca schidigera on ruminal fermentation and nutrient digestion in heifers. J. Anim. Sci. 77:2554-2563.
  31. Hristov, A. N., J. K. Ropp, S. Zaman, and A. Melgar. 2008. Effects of essential oils on in vitro ruminal fermentation and ammonia release. Anim. Feed. Sci. Technol. 144:55-64. https://doi.org/10.1016/j.anifeedsci.2007.09.034
  32. Jahani-Azizabadi, H., M. Danesh Mesgaran, A. R. Vakili, K. Rezayazdi, and M. Hashemi. 2011. Effect of various medicinal plant essential oils obtained from semi-arid climate on rumen fermentation characteristics of a high forage diet using in vitro batch culture. Afr. J. Microbiol. Res. 5:4812-4819.
  33. Jakhetia, V., R. Patel, P. Khatri, N. Pahuja, S. Garg, A. Pandey, and S. Sharma. 2010. Cinnamon: a parmacological review. J. Adv. Sci. Res. 1:19-23.
  34. Juven, B. J., J. Kanner, F. Schved, and H. Weisslowicz. 1994. Factors that interact with the antibacterial action of thyme essential oil and its active constituents. J. Appl. Bacteriol. 76:626-631. https://doi.org/10.1111/j.1365-2672.1994.tb01661.x
  35. Kung-Jr, L., P. Williams, R. J. Schmidt, and W. Hu. 2008. A blend of essential plant oils used as an additive to alter silage fermentation or used as a feed additive for lactating dairy cows. J. Dairy Sci. 91:4793-4800. https://doi.org/10.3168/jds.2008-1402
  36. Lana, R. P., J. B. Russell, and M. E. Van Amburgh. 1998. The role of pH in regulating methane and ammonia production. J. Anim. Sci. 76:2190-2196.
  37. Martinez, S., J. Madrid, F. Hernandez, M. D. Megias, J. A. Sotomayor, and M. J. Jordan. 2006. Effect of thyme essential oils (Thymus hyemalis and Thymus zygis) and monensin on in vitro ruminal degradation and volatile fatty acid production. J. Agric. Food Chem. 54:6598-6602. https://doi.org/10.1021/jf060985p
  38. McIntosh, F. M., P. Williams, R. Losa, R. J. Wallace, D. A. Beever, and C. J. Newbold. 2003. Effects of essential oils on ruminal microorganisms and their protein metabolism. Appl. Environ. Microbiol. 69:5011-5014. https://doi.org/10.1128/AEM.69.8.5011-5014.2003
  39. Meyer, N. F., G. E. Erickson, T. J. Klopfenstein, M. A. Greenquist, M. K. Luebbe, P. Williams, and M. A. Engstrom. 2009. Effect of essential oils, tylosin and monensin on finishing steer performance, carcass characteristics, liver abscesses, ruminal fermentation and digestibility. J. Anim. Sci. 87:2346-2354. https://doi.org/10.2527/jas.2008-1493
  40. Moss, A. R., J. P. Jouany, and J. Newbold. 2000. Methane production by ruminants: its contribution to global warming. Review article. Ann. Zootech. 49:231-253. https://doi.org/10.1051/animres:2000119
  41. National Research Council. 1996. Nutrient requirements of beef cattle. 7th rev. ed. Nat. Acad. Press, Washington, DC.
  42. Newbold, C. J., F. M. McIntosh, P. Williams, R. Losa, and R. J. Wallace. 2004. Effects of a specific blend of essential oil compounds on rumen fermentation. Anim. Feed Sci. Technol. 114:105-112. https://doi.org/10.1016/j.anifeedsci.2003.12.006
  43. Nikaido, H. 1994. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science. 264:382-388. https://doi.org/10.1126/science.8153625
  44. Nocek, J. E. 1997. Bovine acidosis: implications on laminitis. J. Dairy Sci. 80:1005-1028. https://doi.org/10.3168/jds.S0022-0302(97)76026-0
  45. Ozdogan, M., S. S. Onenx, and A. Onenc. 2011. Fattening performance, blood parameters and slaughter traits of Karya lambs consuming blend of essential oil compounds. Afr. J. Biotechnol. 10:6663-6669.
  46. Petit, H. V., and P. M. Flipot. 1992. Feed utilization of beef steers fed grass as hay or silage with or without nitrogen supplementation. J. Anim. Sci. 70:876-883.
  47. SAS Institute Inc. 2004. SAS/SAT user's guide: Version 9.2th edn. SAS Institute Inc., Cary, North Carolina.
  48. Russell, J. B. 1998. The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. J. Dairy Sci. 81:3222-3230. https://doi.org/10.3168/jds.S0022-0302(98)75886-2
  49. Skandamis, P. N., and G. J. Nychas. 2000. Development and evaluation of a model predicting the survival of Escherichia coli O157:H17 NCTC 12900 in homemade eggplant salad at various temperatures, pHs, and oregano essential oil concentration. Appl. Environ. Microbiol. 66:1646-1653. https://doi.org/10.1128/AEM.66.4.1646-1653.2000
  50. Stewart, C. S. 1991. The rumen bacteria. In: Rumen Microbial Metabolism and Ruminant Digestion (Ed. J. P. Jouany). INRA Editions, Paris, France. pp. 15-26.
  51. Tager, L. R., and K. M. Krause. 2011. Effects of essential oils on rumen fermentation, milk production, and feeding behavior in lactating dairy cows. J. Dairy Sci. 94:2455-2464. https://doi.org/10.3168/jds.2010-3505
  52. Tassoul, M. D., and R. D. Shaver. 2009. Effect of a mixture of supplemental dietary plant essential oils on performance of periparturient and early lactation dairy cows. J. Dairy Sci. 92:1734-1740. https://doi.org/10.3168/jds.2008-1760
  53. Wallace, R. J. 2005. Symposium: Plants as animal foods: A case of catch 22? Antimicrobial properties of plant secondary metabolites. Proc. Nutr. Soc. 63:621-629.
  54. Wallace, R. J., L. Arthaud and C. J. Newbold. 1994. Influence of Yucca schidigera extract on ruminal ammonia concentrations and ruminal microorganisms. Appl. Environ. Microbiol. 60:1762-1767.
  55. Wolin, M. J. 1975. Interactions between the bacterial species of the rumen. In: Digestion & Metabolism in the Ruminant (Ed. I. W. McDonald and A. C. I. Warner). University of New England Publ. Unit, Armidale, Australia. pp. 134-148.
  56. Yang, W. Z., B. N. Ametaj, C. Benchaar, and K. A. Beauchemin. 2010a. Dose response to cinnamaldehyde supplementation in growing beef heifers: ruminal and intestinal digestion. J. Anim. Sci. 88:680-688. https://doi.org/10.2527/jas.2008-1652
  57. Yang, W. Z., B. N. Ametaj, M. L. He, C. Benchaar, and K. A. Beauchemin. 2010b. Cinnamaldehyde in feedlot cattle diets: intake, growth performance, carcass characteristics, and blood metabolites. J. Anim. Sci. 88:1082-1092. https://doi.org/10.2527/jas.2008-1608
  58. Yang, W. Z., C. Benchaar, B. N. Ametaj, A. V. Chaves, M. L. He, and T. A. McAllister. 2007. Effects of garlic and juniper berry essential oils on ruminal fermentation and on the site and extent of digestion in lactating cows. J. Dairy Sci. 90:5671-5681. https://doi.org/10.3168/jds.2007-0369
  59. Yang, W. Z., C. Benchaar, B. N. Ametaj, and K.A. Beauchemin. 2010c. Dose response to eugenol supplementation in growing beef cattle: ruminal fermentationand intestinal digestion. Anim. Feed Sci. Technol. 158:57-64. https://doi.org/10.1016/j.anifeedsci.2010.03.019

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