Invited review: Essential oils as modifiers of rumen microbial fermentation

Journal of Dairy Science

Volumn 90, Issue 6, 2007, Pages 2580-2595

  Calsamiglia, S ^a   Busquet, M ^a   Cardozo, P W ^a   Castillejos, L ^a   Ferret, A ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Plant extract; Rumen fermentation

Indexed keywords

ALLIUM SATIVUM; ANIMALIA; BOVIDAE; CAPSICUM FRUTESCENS; CINNAMOMUM VERUM; MYRRHIS ODORATA; NEGIBACTERIA; POSIBACTERIA; SYZYGIUM AROMATICUM;

AMMONIA; ESSENTIAL OIL; METHANE; PLANT EXTRACT;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; BACTERIUM; DIET; DRUG EFFECT; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; REVIEW; RUMINANT STOMACH;

AMMONIA; ANIMAL FEED; ANIMAL NUTRITION PHYSIOLOGY; ANIMALS; BACTERIA; DIET; FERMENTATION; METHANE; OILS, VOLATILE; PLANT EXTRACTS; RUMEN;

EID: 34547669315     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2006-644     Document Type: Review

References (91)

1. Ankri, S., and D. Mirelman. 1999. Antimicrobial properties of allicin from garlic. Microbes Infect. 2:125-129.
2. Balandrin, M. F., and J. A. Klocke. 1985. Natural plant chemicals: Sources of industrial and medicinal materials. Science 228:1154-1160.
3. Benchaar, C., H. V. Petit, R. Berthiaume, T. D. Whyte, and P. Y. Chouinard. 2006. Effects of addition of essential oils and monensin premix on digestion, ruminal fermentation, milk production, and milk composition in dairy cows. J. Dairy Sxi. 89:4352-4364.
4. Borchers, R. 1965. Proteolytic activity of rumen fluid in vitro. J. Anim. Sci. 24:1033-1038.
5. Broderick, G. A., and J. E. Balthrop. 1979. Chemical inhibition of amino acid deamination by ruminal microbes in vitro. J. Anim. Sci. 49:1101-1111.
6. Broudiscou, L. P., Y. Papon, and A. F. Broudiscou. 2002. Effects of dry plant extracts on feed degradation and the production of rumen microbial biomass in a dual outflow fermenter. Anim. Feed Sci. Technol. 101:183-189.
7. Broudiscou, L. P., Y. Papon, and A. F. Broudiscou. 2000. Effects of dry plant extracts on fermentation and methanogenesis in continuous culture of rumen microbes. Anim. Feed Sci. Technol. 87:263-277.
8. Burt, S. 2004. Essential oils: Their antibacterial properties and potential applications in foods - A review. Int. J. Food Microbiol. 94:223-253.
9. Busquet, M., S. Calsamiglia, A. Ferret, P. W. Cardozo, and C. Kamel. 2005a. Effects of cinnamaldehyde and garlic oil on rumen microbial fermentation in a dual flow continuous culture. J. Dairy Sci. 88:2508-2516.
10. Busquet, M., S. Calsamiglia, A. Ferret, M. D. Carro, and C. Kamel. 2005b. Effect of garlic oil and four of its compounds on rumen microbial fermentation. J. Dairy Sci. 88:4393-4404.
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.
12. Busquet, M., S. Calsamiglia, A. Ferret, and C. Kamel. 2005c. Screening for the effects of natural plant extracts and secondary plant metabolites on rumen microbial fermentation in continuous culture. Anim. Feed Sci. Technol. 123/124:597-613.
13. Busquet, M., H. Greathead, S. Calsamiglia, A. Ferret, and C. Kamel. 2003. Efecto del extracto de ajo y el cinemaldehido sobre la producción, composición y residuos en leche en vacas de alta producción. ITEA 24 (Vol. Extra):756-758.
14. Calixto, J. B., A. Beirith, J. Ferreira, A. R. S. Santos, V. C. Filho, and R. A. Yunes. 2000. Naturally occurring antinociceptive substances from plants: A review. Phytother. Res. 14:401-418.
15. Calsamiglia, S., L. Castillejos, and M. Busquet. 2006. Alternatives to antimicrobial growth promoters in cattle. Pages 129-167 in Recent Advances in Animal Nutrition. P. C. Garnsworthy, and J. Wiseman, ed. Nottingham University Press, Nottingham, UK.
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 ruminai fermentation and protein degradation in beef heifers fed a high concentrate diet. J. Anim. Sci. 84:2801-2808.
17. Cardozo, P. W., S. Calsamiglia, A. Ferret, and C. Kamel. 2004. Effects of natural plant extracts on protein degradation and fermentation profiles in continuous culture. J. Anim. Sci. 82:3230-3236.
18. 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.
19. 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.
20. Castillejos, L., S. Calsamiglia, A. Ferret, and R. Losa. 2007. Effects of dose and adaptation time of a specific blend of essential oils compounds on rumen fermentation. Anim. Feed Sci. Technol. 132:186-201.
21. 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.
22. Chalupa, W., W. Corbett, and J. R. Brethour. 1980. Effects of monensin and amicloral on rumen fermentation. J. Anim. Sci. 51:170-179.
23. Chao, S. C., and D. G. Young. 2000. Screening for inhibitory activity of essential oils on selected bacteria, fungi and viruses. J. Essent. Oil Res. 12:639-649.
24. Chow, J. M., J. A. S. Van Kessel, and J. B. Russell. 1994. Binding of radiolabeled monensin and lasolacid to ruminal microorganisms and feed. J. Anim. Sci. 72:1630-1635.
25. Cheeke, P. R. 1999. Actual and potential applications of Yucca schidigera and Quillaja saponaria saponins in human and animal nutrition. Proc. Am. Soc. Anim. Sci. E9:1-10.
26. Cichewicz, R. H., and P. A. Thorpe. 1996. The antimicrobial properties of chile peppers (Capsicum species) and their uses in Mayan medicine. J. Ethnopharmacol. 52:61-70.
27. Cimanga, K., K. Kambu, L. Tona, S. Apers, T. Bruyne, N. Hermans, J. Totté, L. Pieters, and A. J. Vlietinck. 2002. Correlation between chemical composition and antibacterial activity of essential oils of some aromatic medicinal plants growing in the Democratic Republic of Congo. J. Ethnopharmacol. 79:213-220.
28. Cox, S. D., C. M. Mann, and J. L. Markam. 2001. Interaction between components of the essential oil of Melaleuca alternifolia. J. Appl. Microbiol. 91:492-497.
29. Davidson, P. M., and A. S. Naidu. 2000. Phyto-phenols. Pages 265-293 in Natural Food Antimicrobial Systems. A. S. Naidu, ed. CRC Press, Boca Raton, FL.
30. Deans, S. G., and G. Ritchie. 1987. Antibacterial properties of plant essential oils. Int. J. Food Microbiol. 5:165-180.
31. De Rosa, M., A. Gambacorta, and A. Gliozzi. 1986. Structure, biosynthesis, and physicochemical properties or archaebacterial lipids. Microbiol. Rev. 50:70-80.
32. Dorman, H. J. D., and S. G. Deans. 2000. Antimicrobial agents from plants: Antibacterial activity of plant volatile oils. J. Appl. Microbiol. 88:308-316.
33. Evans, J. D., and S. A. Martin. 2000. Effects of thymol on ruminal microorganisms. Curr. Microbiol. 41:336-340.
34. FDA (US Food and Drug Administration). 2005. Freedom of information summary. Supplemental new animal drug application. NADA 095-735. Monensin Sodium (Rumensin 80): Type A Medicated Article for Dairy Cattle. http://www.fda.gov/ cvm/FOI/095-735s121505.pdf Accessed Oct. 1, 2006.
35. Feldberg, R. S., S. C. Chang, A. N. Kotik, M. Nadler, Z. Neuwirth, D. C. Sundstrom, and N. H. Thompson. 1988. In vitro mechanism of inhibition of bacterial cell growth by allicin. Antimicrob. Agents Chem. 32:1763-1768.
36. Ferme, D., M. Banjac, S. Calsamiglia, M. Busquet, C. Kamel, and G. Avgustin. 2004. The effects of plant extracts on microbial community structure in a rumen-simulating continuous-culture system as revealed by molecular profiling. Folia Microbiol. (Praha) 49:151-155.
37. Garcia-Lopez, P. M., L. Kung, Jr., and J. M. Odom. 1996. In vitro inhibition of microbial methane production by 9,10-anthraquinone. J. Anim. Sci. 74:2276-2284.
38. Gebhardt, R., and H. Beck. 1996. Differential inhibitory effects of garlic-derived organosulfur compounds on cholesterol biosynthesis in primary rat hepatocyte cultures. Lipids 31:1269-1276.
39. Gershenzon, J., and R. Croteau. 1991. Terpenoids. Pages 165-219 in Herbivores: Their Interactions with Secondary Plant Metabolites. Vol. 1. G. A. Rosenthal, and M. R. Berenbaum, ed. Academic Press, San Diego, CA.
40. Griffin, S. G., S. G. Wyllie, J. L. Markham, and D. N. Leach. 1999. The role of structure and molecular properties of terpenoids in determining their antimicrobial activity. Flavour Fragr. J. 14:322-332.
41. Gustafson, R. H., and R. E. Bowen. 1997. Antibiotic use in animal agriculture. J. Appl. Microbiol. 83:531-541.
42. Gutiérrez, M. E., A. F. García, M. A. de Madariaga, M. L. Sagrista, F. J. Casadó, and M. Mora. 2003. Interaction of tocopherols and phenolic compounds with membrane lipid components: Evaluation of their antioxidant activity in a liposomal model system. Life Sci. 72:2337-2360.
43. Hammer, K. A., C. F. Carson, and T. V. Riley. 1999. Antimicrobial activity of essential oils and other plant extracts. J. Appl. Microbiol. 86:985-990.
44. Harborne, J. B., and C. A. Williams. 2000. Advances in flavonoid research since 1992. Phytochemistry 55:481-504.
45. Helander, I. M., H. Alakomi, K. Latva-Kala, T. Mattila-Sandholm, I. Pol, E. J. Smid, L. G. M. Gorris, and A. Wright. 1998. Characterization of the action of selected essential oil components on gram-negative bacteria. J. Agric. Food Chem. 46:3590-3595.
46. 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.
47. Hoffmann, C., and C. A. Evans. 1911. The use of spices as preservatives. J. Ind. Eng. Chem. 3:835-838.
48. Horton, G. M. J. 1980. Use of feed additives to reduce ruminal methane production and deaminase activity in steers. J. Anim. Sci. 50:1160-1164.
49. 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.
50. Kamel, C. 2001. Tracing modes of action and the roles of plant extracts in non-ruminants. Pages 135-150 in Recent Advances in Animal Nutrition. P. C. Garnsworthy, and J. Wiseman, ed. Nottingham University Press, Nottingham, UK.
51. Kung, L., Jr., K. A. Smith, A. M. Smalaga, K. M. Endress, C. A. Bessett, N. K. Ranjit, and J. Yaissle. 2003. Effects of 9,10 anthraquinine on ruminal fermentation, total-tract digestion, and blood metabolite concentrations in sheep. J. Anim. Sci. 81:323-328.
52. Lawson, L. 1996. The composition and chemistry of garlic cloves and processed garlic. Pages 37-107 in Garlic: The Science and Therapeutic Application of Allium sativum L. and Related Species. H. P. Koch, and L. D. Lawson, ed. Williams & Wilkins, Baltimore, MD.
53. Lee, S. E., H. J. Hwang, J. S. Ha, H. S. Jeong, and J. H. Kim. 2003. Screening of medicinal plant extracts for antioxidant activity. Life Sci. 73:167-179.
54. Mahmoud, A. L. E. 1994. Antifungal action and antiaflatoxigenic properties of some essential oil constituents. Lett. Appl. Microbiol. 19:110-113.
55. Marino, M., C. Bersani, and G. Comi. 2001. Impedance measurements to study the antimicrobial activity of essential oils from Lamiacea and Compositae. Int. J. Food Microbiol. 67:187-195.
56. Martin, S. A., and J. M. Macy. 1985. Effects of monensin, pyromellitic diimide and 2-bromoethanesulfonic acid on rumen fermentation in vitro. J. Anim. Sci. 60:544-550.
57. McIntosh, F. M., C. J. Newbold, R. Losa, P. Williams, and R. J. Wallace. 2000. Effects of essential oils on rumen fermentation. Reprod. Nutr. Dev. 40:221-222.
58. 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.
59. Miller, T. L., and M. J. Wolin. 2001. Inhibition of growth of methaneproducing bacteria of the ruminant forestomach by hydroxymethylglutaryl- SCoAreductase inhibitors. J. Dairy Sci. 84:1445-1448.
60. Min, B. R., T. N. Barry, G. T. Attwood, and W. C. McNabb. 2003. The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperature forages: A review. Anim. Feed Sci. Technol. 106:3-19.
61. Mohammed, N., N. Ajisaka, Z. A. Lila, K. Mikuni, K. Hara, S. Kanda, and H. Itabashi. 2004. Effect of Japanese horseradish oil on methane production and ruminal fermentation in vitro and in steers. J. Anim. Sci. 82:1839-1846.
62. Molero, R., M. Ibars, S. Calsamiglia, A. Ferret, and R. Losa. 2004. Effect of a specific blend of essential oil compounds on dry matter and crude protein degradability in heifers fed diets with different forage to concentrate rations. Anim. Feed Sci. Technol. 114:91-104.
63. Nagy, J. G., and R. P. Tengerdy. 1968. Antibacterial action of essential oils of Artemisia as an ecological factor. II. Antibacterial action of the volatile oils of Artemisia tridentata (big sagebrush) on bacteria from the rumen of mule deer. Appl. Microbiol. 16:441-444.
64. Newbold, C. J., F. M. McIntosch, 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.
65. Nikaido, H. 1994. Prevention of drug access to bacterial targets: Permeability barriers and active efflux. Science 264:382-388.
66. European Commission. 2003. Regulation (EC) No. 1831/2003 of the European Parliament and of the Council of 22 September 2003 on Additives for Use in Animal Nutrition. Off. J. Eur. Union L:L268/29-L268/43.
67. O'Gara, E. A., D. J. Hill, and D. J. Maslin. 2000. Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Appl. Environ. Microbiol. 66:2269-2273.
68. Oh, H. K., M. B. Jones, and W. M. Longhurst. 1968. Comparison of rumen microbial inhibition resulting from various essential oils isolated from relatively unpalatable plant species. Appl. Microbiol. 16:39-44.
69. Oh, H. K., T. Sakai, M. B. Jones, and W. M. Longhurst. 1967. Effect of various essential oils isolated from Douglas fir needles upon sheep and deer rumen microbial activity. Appl. Microbiol. 15:777-784.
70. Ouattara, B., R. E. Simard, R. A. Holley, G. J.-P. Piette, and A. Begin. 1997. Antibacterial activity of selected fatty acids and essential oils against six meat spoilage organisms. Int. J. Food Microbiol. 37:155-162.
71. Pentz, R., and C. P. Siegers. 1996. Methods for qualitative and quantitative assessment of their ingredients. Pages 109-134 in Garlic: The Science and Therapeutic Application of Allium sativum L. and Related Species. H. P. Koch, and L. D. Lawson, ed. Williams & Wilkins, Baltimore, MD.
72. Piacente, S., C. Pizza, and W. Oleszek. 2005. Saponins and phenolics of Yucca schidigera Roezl: Chemistry and bioactivity. Phytochem. Rev. 4:177-190.
73. Piva, G., and F. Rossi. 1999. Possible alternatives to the use of antibiotics as growth promoters. New additives. In Feed Manufacturing in the Mediterranean Region. Opt. Mediter. 37:83-106.
74. Prescott, L. M., J. P. Harley, and D. A. Klein. 2004. Control de microorganismos por agentes físicos y químicos. Pages 145-162 in Microbiología. McGraw-Hill-Interamericana de España, Madrid, Spain.
75. Reddy, L., B. Odhav, and K. D. Bhoola. 2003. Natural products for cancer prevention: A global perspective. Pharmacol. Therap. 99:1-13.
76. Reuter, H. D., J. P. Koch, and L. Lawson. 1996. Therapeutic effects and applications of garlic and its preparations. Pages 135-212 in Garlic: The Science and Therapeutic Application of Allium sativum L. and Related Species. H. P. Koch, and L. D. Lawson. ed. Williams & Wilkins, Baltimore, MD.
77. Ross, Z. M., E. A. O'Gara, D. J. Hill, H. V. Sleightholme, and D. J. Maslin. 2001. Antimicrobial properties of garlic oil against human enteric bacteria: Evaluation of methodologies and comparisons with garlic oil sulfides and garlic powder. Appl. Environ. Microbiol. 67:475-480.
78. Rossi, J. 1999. Additives for animal nutrition and technique for their preparation. European Patent EP 0646321 B1.
79. Sangwan, N. S., A. H. A. Farooqi, F. Shabih, and R. S. Sangwan. 2001. Regulation of essential oil production in plants. Plant Growth Reg. 34:3-21.
80. Sikkema, J., J. A. M. Bont, and B. Poolman. 1994. Interactions of cyclic hydrocarbons with biological membranes. J. Biol. Chem. 269:8022-8028.
81. Sivropoulou, A., E. Papanikolaou, C. Nikolaou, S. Kokkini, T. Lanaras, and M. Arsenakis. 1996. Antimicrobial and cytotoxic activities of Origanum essential oils. J. Agrie. Food Chem. 44:1202-1205.
82. Skandamis, P. N., and G. J. Nychas. 2000. Development and evaluation of a model predicting the survival of Escherichia coli 0157:H17 NCTC 12900 in homemade eggplant salad at various temperatures, pHs, and oregano essential oil concentration. Appl. Environ. Microbiol. 66:1646-1653.
83. Smith-Palmer, A., J. Stewart, and L. Fyfe. 1998. Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Lett. Appl. Microbiol. 26:118-122.
84. Tamminga, S. 1996. A review on environmental impacts of nutritional strategies in ruminants. J. Anim. Sci. 74:3112-3124.
85. Trouillas, P., C. A. Calliste, D. P. Allais, A. Simon, A. Marfak, C. Delage, and J. L. Duroux. 2003. Antioxidant, anti-inflammatory and antiproliferative properties of sixteen water plant extracts used in the Limousin countryside as herbal teas. Food Chem. 80:399-407.
86. Ultee, A., M. H. J. Bennik, and R. Moezelaar. 2002. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl. Environ. Microbiol. 68:1561-1568.
87. Ultee, A., E. P. Kets, and E. J. Smid. 1999. Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl. Environ. Microbiol. 65:4606-4610.
88. Van Nevel, C. J., and D. I. Demeyer. 1988. Manipulation of rumen fermentation. Pages 387-443 in The Rumen Microbial Ecosystem. P. N. Hobson, ed. Elsevier Applied Science, New York, NY.
89. Wallace, R. J., N. R. McEwan, F. M. McIntosh, B. Teferedegne, and C. J. Newbold. 2002. Natural products as manipulators of rumen fermentation. Asian-australas. J. Anim. Sci. 10:1458-1468.
90. Wendakoon, C. N., and M. Sakaguchi. 1995. Inhibition of amino acid decarboxylase activity of Enterobacter aerogenes by active components in spices. J. Food Prot. 58:280-283.
91. Zafra, M. A., F. Molina, and A. Puerto. 2003. Effects of perivagal administration of capsaicin on post-surgical food intake. Auto. Neurosci.: Basic and Clin. 107:37-44.