Journal of Dairy Science
Volume 90, Issue 6 , Pages 2580-2595 , June 2007

Invited Review: Essential Oils as Modifiers of Rumen Microbial Fermentation

Received 4 October 2006 ,Accepted 11 January 2007.

References 

  1. Ankri S, Mirelman D. Antimicrobial properties of allicin from garlic. Microbes Infect. 1999;2:125–129
  2. Balandrin MF, Klocke JA. Natural plant chemicals: Sources of industrial and medicinal materials. Science. 1985;228:1154–1160
  3. Benchaar C, Petit HV, Berthiaume R, Whyte TD, Chouinard PY. Effects of addition of essential oils and monensin premix on digestion, ruminal fermentation, milk production, and milk composition in dairy cows. J. Dairy Sci. 2006;89:4352–4364
  4. Borchers R. Proteolytic activity of rumen fluid in vitro. J. Anim. Sci. 1965;24:1033–1038
  5. Broderick GA, Balthrop JE. Chemical inhibition of amino acid deamination by ruminal microbes in vitro. J. Anim. Sci. 1979;49:1101–1111
  6. Broudiscou LP, Papon Y, Broudiscou AF. Effects of dry plant extracts on feed degradation and the production of rumen microbial biomass in a dual outflow fermenter. Anim. Feed Sci. Technol. 2002;101:183–189
  7. Broudiscou LP, Papon Y, Broudiscou AF. Effects of dry plant extracts on fermentation and methanogenesis in continuous culture of rumen microbes. Anim. Feed Sci. Technol. 2000;87:263–277
  8. Burt S. Essential oils: Their antibacterial properties and potential applications in foods—A review. Int. J. Food Microbiol. 2004;94:223–253
  9. Busquet M, Calsamiglia S, Ferret A, Cardozo PW, Kamel C. Effects of cinnamaldehyde and garlic oil on rumen microbial fermentation in a dual flow continuous culture. J. Dairy Sci. 2005;88:2508–2516
  10. Busquet M, Calsamiglia S, Ferret A, Carro MD, Kamel C. Effect of garlic oil and four of its compounds on rumen microbial fermentation. J. Dairy Sci. 2005;88:4393–4404
  11. Busquet M, Calsamiglia S, Ferret A, Kamel C. Plant extracts affect in vitro rumen microbial fermentation. J. Dairy Sci. 2006;89:761–771
  12. Busquet M, Calsamiglia S, Ferret A, Kamel C. Screening for the effects of natural plant extracts and secondary plant metabolites on rumen microbial fermentation in continuous culture. Anim. Feed Sci. Technol. 2005;123/124:597–613
  13. Busquet M, Greathead H, Calsamiglia S, Ferret A, Kamel C. Efecto del extracto de ajo y el cinemaldehido sobre la producción, composición y residuos en leche en vacas de alta producción. ITEA. 2003;24:756–758(Vol. Extra)
  14. Calixto JB, Beirith A, Ferreira JA, Santos RS, Filho VC, Yunes RA. Naturally occurring antinociceptive substances from plants: A review. Phytother. Res. 2000;14:401–418
  15. Calsamiglia S, Castillejos L, Busquet M. Alternatives to antimicrobial growth promoters in cattle. In:  Garnsworthy PC,  Wiseman J editor. Recent Advances in Animal Nutrition. Nottingham, UK: Nottingham University Press; 2006;p. 129–167
  16. Cardozo PW, Calsamiglia S, Ferret A, Kamel C. 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. 2006;84:2801–2808
  17. Cardozo PW, Calsamiglia S, Ferret A, Kamel C. Effects of natural plant extracts on protein degradation and fermentation profiles in continuous culture. J. Anim. Sci. 2004;82:3230–3236
  18. Cardozo PW, Calsamiglia S, Ferret A, Kamel C. 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. 2005;83:2572–2579
  19. Castillejos L, Calsamiglia S, Ferret A. Effect of essential oils active compounds on rumen microbial fermentation and nutrient flow in in vitro systems. J. Dairy Sci. 2006;89:2649–2658
  20. Castillejos L, Calsamiglia S, Ferret A, Losa R. Effects of dose and adaptation time of a specific blend of essential oils compounds on rumen fermentation. Anim. Feed Sci. Technol. 2007;132:186–201
  21. Castillejos L, Calsamiglia S, Ferret A, Losa R. 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. 2005;119:29–41
  22. Chalupa W, Corbett W, Brethour JR. Effects of monensin and amicloral on rumen fermentation. J. Anim. Sci. 1980;51:170–179
  23. Chao SC, Young DG. Screening for inhibitory activity of essential oils on selected bacteria, fungi and viruses. J. Essent. Oil Res. 2000;12:639–649
  24. Chow JM, Van Kessel JAS, Russell JB. Binding of radiolabeled monensin and lasolacid to ruminal microorganisms and feed. J. Anim. Sci. 1994;72:1630–1635
  25. Cheeke PR. Actual and potential applications of Yucca schidigera and Quillaja saponaria saponins in human and animal nutrition. Proc. Am. Soc. Anim. Sci. 1999;E9:1–10
  26. Cichewicz RH, Thorpe PA. The antimicrobial properties of chile peppers (Capsicum species) and their uses in Mayan medicine. J. Ethnopharmacol. 1996;52:61–70
  27. Cimanga K, Kambu K, Tona L, Apers S, Bruyne T, Hermans N, et al. Correlation between chemical composition and antibacterial activity of essential oils of some aromatic medicinal plants growing in the Democratic Republic of Congo. J. Ethnopharmacol. 2002;79:213–220
  28. Cox SD, Mann CM, Markam JL. Interaction between components of the essential oil of Melaleuca alternifolia. J. Appl. Microbiol. 2001;91:492–497
  29. Davidson PM, Naidu AS. Phyto-phenols. In:  Naidu AS editors. Natural Food Antimicrobial Systems. Boca Raton, FL: CRC Press; 2000;p. 265–293
  30. Deans SG, Ritchie G. Antibacterial properties of plant essential oils. Int. J. Food Microbiol. 1987;5:165–180
  31. De Rosa M, Gambacorta A, Gliozzi A. Structure, biosynthesis, and physicochemical properties or archaebacterial lipids. Microbiol. Rev. 1986;50:70–80
  32. Dorman HJD, Deans SG. Antimicrobial agents from plants: Antibacterial activity of plant volatile oils. J. Appl. Microbiol. 2000;88:308–316
  33. Evans JD, Martin SA. Effects of thymol on ruminal microorganisms. Curr. Microbiol. 2000;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 RS, Chang SC, Kotik AN, Nadler M, Neuwirth Z, Sundstrom DC, et al. In vitro mechanism of inhibition of bacterial cell growth by allicin. Antimicrob. Agents Chem. 1988;32:1763–1768
  36. Ferme D, Banjac M, Calsamiglia S, Busquet M, Kamel C, Avgustin G. The effects of plant extracts on microbial community structure in a rumen-simulating continuous-culture system as revealed by molecular profiling. Folia Microbiol. (Praha). 2004;49:151–155
  37. Garcia-Lopez PM, Kung L, Odom JM. In vitro inhibition of microbial methane production by 9,10-anthraquinone. J. Anim. Sci. 1996;74:2276–2284
  38. Gebhardt R, Beck H. Differential inhibitory effects of garlic-derived organosulfur compounds on cholesterol biosynthesis in primary rat hepatocyte cultures. Lipids. 1996;31:1269–1276
  39. Gershenzon J, Croteau R. Terpenoids. In:  Rosenthal GA,  Berenbaum MR editor. Herbivores: Their Interactions with Secondary Plant Metabolites. Vol. 1:San Diego, CA: Academic Press; 1991;p. 165–219
  40. Griffin SG, Wyllie SG, Markham JL, Leach DN. The role of structure and molecular properties of terpenoids in determining their antimicrobial activity. Flavour Fragr. J. 1999;14:322–332
  41. Gustafson RH, Bowen RE. Antibiotic use in animal agriculture. J. Appl. Microbiol. 1997;83:531–541
  42. Gutiérrez ME, García AF, de Madariaga MA, Sagrista ML, Casadó FJ, Mora M. Interaction of tocopherols and phenolic compounds with membrane lipid components: Evaluation of their antioxidant activity in a liposomal model system. Life Sci. 2003;72:2337–2360
  43. Hammer KA, Carson CF, Riley TV. Antimicrobial activity of essential oils and other plant extracts. J. Appl. Microbiol. 1999;86:985–990
  44. Harborne JB, Williams CA. Advances in flavonoid research since 1992. Phytochemistry. 2000;55:481–504
  45. Helander IM, Alakomi H, Latva-Kala K, Mattila-Sandholm T, Pol I, Smid EJ, et al. Characteritzation of the action of selected essential oil components on gram-negative bacteria. J. Agric. Food Chem. 1998;46:3590–3595
  46. Hino T, Russell JB. Effect of reducing-equivalent disposal and NADH/NAD on deamination of amino acids by intact rumen microorganisms and their cell extracts. Appl. Environ. Microbiol. 1985;50:1368–1374
  47. Hoffmann C, Evans CA. The use of spices as preservatives. J. Ind. Eng. Chem. 1911;3:835–838
  48. Horton GMJ. Use of feed additives to reduce ruminal methane production and deaminase activity in steers. J. Anim. Sci. 1980;50:1160–1164
  49. Juven BJ, Kanner J, Schved F, Weisslowicz H. Factors that interact with the antibacterial action of thyme essential oil and its active constituents. J. Appl. Bacteriol. 1994;76:626–631
  50. Kamel C. Tracing modes of action and the roles of plant extracts in non-ruminants. In:  Garnsworthy PC,  Wiseman J editor. Recent Advances in Animal Nutrition. Nottingham, UK: Nottingham University Press; 2001;p. 135–150
  51. Kung L, Smith KA, Smalaga AM, Endress KM, Bessett CA, Ranjit NK, et al. Effects of 9,10 anthraquinine on ruminal fermentation, total-tract digestion, and blood metabolite concentrations in sheep. J. Anim. Sci. 2003;81:323–328
  52. Lawson L. The composition and chemistry of garlic cloves and processed garlic. In:  Koch HP,  Lawson LD editor. Garlic: The Science and Therapeutic Application of Allium sativum L. and Related Species. Baltimore, MD: Williams & Wilkins; 1996;p. 37–107
  53. Lee SE, Hwang HJ, Ha JS, Jeong HS, Kim JH. Screening of medicinal plant extracts for antioxidant activity. Life Sci. 2003;73:167–179
  54. Mahmoud ALE. Antifungal action and antiaflatoxigenic properties of some essential oil constituents. Lett. Appl. Microbiol. 1994;19:110–113
  55. Marino M, Bersani C, Comi G. Impedance measurements to study the antimicrobial activity of essential oils from Lamiacea and Compositae. Int. J. Food Microbiol. 2001;67:187–195
  56. Martin SA, Macy JM. Effects of monensin, pyromellitic diimide and 2-bromoethanesulfonic acid on rumen fermentation in vitro. J. Anim. Sci. 1985;60:544–550
  57. McIntosh FM, Newbold CJ, Losa R, Williams P, Wallace RJ. Effects of essential oils on rumen fermentation. Reprod. Nutr. Dev. 2000;40:221–222
  58. McIntosh FM, Williams P, Losa R, Wallace RJ, Beever DA, Newbold CJ. Effects of essential oils on ruminal microorganisms and their protein metabolism. Appl. Environ. Microbiol. 2003;69:5011–5014
  59. Miller TL, Wolin MJ. Inhibition of growth of methane-producing bacteria of the ruminant forestomach by hydroxymethylglutaryl∼SCoA reductase inhibitors. J. Dairy Sci. 2001;84:1445–1448
  60. Min BR, Barry TN, Attwood GT, McNabb WC. The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperature forages: A review. Anim. Feed Sci. Technol. 2003;106:3–19
  61. Mohammed N, Ajisaka N, Lila ZA, Mikuni K, Hara K, Kanda S, et al. Effect of Japanese horseradish oil on methane production and ruminal fermentation in vitro and in steers. J. Anim. Sci. 2004;82:1839–1846
  62. Molero R, Ibars M, Calsamiglia S, Ferret A, Losa R. 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. 2004;114:91–104
  63. Nagy JG, Tengerdy RP. 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. 1968;16:441–444
  64. Newbold CJ, McIntosch FM, Williams P, Losa R, Wallace RJ. Effects of a specific blend of essential oil compounds on rumen fermentation. Anim. Feed Sci. Technol. 2004;114:105–112
  65. Nikaido H. Prevention of drug access to bacterial targets: Permeability barriers and active efflux. Science. 1994;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 EA, Hill DJ, Maslin DJ. Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Appl. Environ. Microbiol. 2000;66:2269–2273
  68. Oh HK, Jones MB, Longhurst WM. Comparison of rumen microbial inhibition resulting from various essential oils isolated from relatively unpalatable plant species. Appl. Microbiol. 1968;16:39–44
  69. Oh HK, Sakai T, Jones MB, Longhurst WM. Effect of various essential oils isolated from Douglas fir needles upon sheep and deer rumen microbial activity. Appl. Microbiol. 1967;15:777–784
  70. Ouattara B, Simard RE, Holley RA, Piette G J-P, Bégin A. Antibacterial activity of selected fatty acids and essential oils against six meat spoilage organisms. Int. J. Food Microbiol. 1997;37:155–162
  71. Pentz R, Siegers CP. Methods for qualitative and quantitative assessment of their ingredients. In:  Koch HP,  Lawson LD editor. Garlic: The Science and Therapeutic Application of Allium sativum L. and Related Species. Baltimore, MD: Williams & Wilkins; 1996;p. 109–134
  72. Piacente S, Pizza C, Oleszek W. Saponins and phenolics of Yucca schidigera Roezl: Chemistry and bioactivity. Phytochem. Rev. 2005;4:177–190
  73. Piva G, Rossi F. Possible alternatives to the use of antibiotics as growth promoters. New additives. In Feed Manufacturing in the Mediterranean Region. Opt. Mediter. 1999;37:83–106
  74. Prescott LM, Harley JP, Klein DA. Control de microorganismos por agentes físicos y químicos. Microbiología. Madrid, Spain: McGraw-Hill-Interamericana de España; 2004;Pages 145–162
  75. Reddy L, Odhav B, Bhoola KD. Natural products for cancer prevention: A global perspective. Pharmacol. Therap. 2003;99:1–13
  76. Reuter HD, Koch JP, Lawson L. Therapeutic effects and applications of garlic and its preparations. In:  Koch HP,  Lawson LD editor. Garlic: The Science and Therapeutic Application of Allium sativum L. and Related Species. Baltimore, MD: Williams & Wilkins; 1996;p. 135–212
  77. Ross ZM, O’Gara EA, Hill DJ, Sleightholme HV, Maslin DJ. Antimicrobial properties of garlic oil against human enteric bacteria: Evaluation of methodologies and comparisons with garlic oil sulfides and garlic powder. Appl. Environ. Microbiol. 2001;67:475–480
  78. Rossi, J. 1999. Additives for animal nutrition and technique for their preparation. European Patent EP 0646321 B1.
  79. Sangwan NS, Farooqi AHA, Shabih F, Sangwan RS. Regulation of essential oil production in plants. Plant Growth Reg. 2001;34:3–21
  80. Sikkema J, Bont JAM, Poolman B. Interactions of cyclic hydrocarbons with biological membranes. J. Biol. Chem. 1994;269:8022–8028
  81. Sivropoulou A, Papanikolaou E, Nikolaou C, Kokkini S, Lanaras T, Arsenakis M. Antimicrobial and cytotoxic activities of Origanum essential oils. J. Agric. Food Chem. 1996;44:1202–1205
  82. Skandamis PN, Nychas GJ. 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. 2000;66:1646–1653
  83. Smith-Palmer A, Stewart J, Fyfe L. Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Lett. Appl. Microbiol. 1998;26:118–122
  84. Tamminga S. A review on environmental impacts of nutritional strategies in ruminants. J. Anim. Sci. 1996;74:3112–3124
  85. Trouillas P, Calliste CA, Allais DP, Simon A, Marfak A, Delage C, et al. Antioxidant, anti-inflammatory and antiproliferative properties of sixteen water plant extracts used in the Limousin countryside as herbal teas. Food Chem. 2003;80:399–407
  86. Ultee A, Bennik MHJ, Moezelaar R. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl. Environ. Microbiol. 2002;68:1561–1568
  87. Ultee A, Kets EP, Smid EJ. Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl. Environ. Microbiol. 1999;65:4606–4610
  88. Van Nevel CJ, Demeyer DI. Manipulation of rumen fermentation. In:  Hobson PN editors. The Rumen Microbial Ecosystem. New York, NY: Elsevier Applied Science; 1988;p. 387–443
  89. Wallace RJ, McEwan NR, McIntosh FM, Teferedegne B, Newbold CJ. Natural products as manipulators of rumen fermentation. Asian-australas. J. Anim. Sci. 2002;10:1458–1468
  90. Wendakoon CN, Sakaguchi M. Inhibition of amino acid decarboxylase activity of Enterobacter aerogenes by active components in spices. J. Food Prot. 1995;58:280–283
  91. Zafra MA, Molina F, Puerto A. Effects of perivagal administration of capsaicin on post-surgical food intake. Auto. Neurosci.: Basic and Clin. 2003;107:37–44

PII: S0022-0302(07)70069-3

doi: 10.3168/jds.2006-644

Journal of Dairy Science
Volume 90, Issue 6 , Pages 2580-2595 , June 2007

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