Effect of essential oils and aqueous extracts of plants on in vitro rumen fermentation and methane production
Aaron Alejandro Molho-Ortiz, Atmir Romero-Pérez, Efrén Ramírez-Bribiesca, Claudia Cecilia Márquez-Mota, Francisco Alejandro Castrejón-Pineda, Luis Corona
Abstract
The objective of this study was to evaluate in vitro rumen fermentation and methane production under the influence of two sources of phytochemicals: essential oils (EOs) and aqueous extracts (AEs). Treatments were set up in a completely randomized block design, with 4×2+1 factorial arrangement of four species, S (garlic, G; cinnamon, C; rosemary, R; eucalyptus; EU) × two types of presentation, P (essential oil, EO; aqueous extract, AE) and a basal diet, BD (50% concentrate, 20% alfalfa and 30% corn silage). Rumen fermentation was evaluated using the in vitro gas production technique. All experimental units were incubated with 500 mg of BD for 72 hours. Treatments were added at a single dose of 900 mg/L of rumen inoculum. Gas pressure was recorded at 0, 2, 4, 6, 8, 10, 14, 18, 24, 30, 36, 42, 48, 60 and 72 h post-incubation. There was an interaction effect (P × S) between plant extract presentation (P) and plant species (S) for all variables. Treatments GEO, CEO, REO decreased volatile fatty acids (mmol/200 mg), microbial mass production (mg/g), CH4 production (mL/g), in vitro dry matter digestibility (P < 0.05), and total gas production at 24 and 72 h post-incubation (P < 0.05; mL/g DM, mL/g OM). No differences (P > 0.05) were observed between AEs and BD. In conclusion, the use of EOs negatively affected rumen fermentation parameters and the production of CH4. Garlic and cinnamon EOs effectively reduced methane emissions; however, they also reduced in vitro dry matter digestibility.
Keywords
References
Aggoun M, Boussaada A, Rabah A, Serine A, Malika B (2017) Effect of natural bioflavonoid on in vitro ruminal microbiota activity in sheep rumen liquor. Journal of bioscience and Biotechnology 6:31–35.
Alemu AW, Romero-Pérez A, Araujo RC, Beauchemin KA (2019) Effect of encapsulated nitrate and microencapsulated blend of essential oils on growth performance and methane emissions from beef steers fed backgrounding diets. Animals 9:1–19. doi: 10.3390/ani9010021.
Amanzougarene Z, Fondevila M (2020) Fitting of the in vitro gas production technique to the study of high concentrate diets. Animals 10:1910- 1935. doi: 10.3390/ani10101935.
Amin N, Tagliapietra F, Arango S, Guzzo N, Bailoni L (2021) Free and microencapsulated essential oils incubated in vitro: ruminal stability and fermentation parameters. Animals 11:180. doi: 10.3390/ani11010180.
Anassori E, Dalir-Naghadeh B, Pirmohammadi R, Taghizadeh A, Asri-Rezaei S, Maham M, Farahmand-Azar S, Farhoomand P (2011) Garlic: a potential alternative for monensin as a rumen modifier. Livestock Science 142:276–287. doi: 10.1016/j.livsci.2011.08.003.
Ankri S, Mirelman D (1999) Antimicrobial properties of allicin from garlic. Microbes and infection 1: 125-129. doi: 10.1016/S1286-4579(99)80003-3.
AOAC (2016) AOAC official methods of analysis. Assoc. Off. Agric. Chem. Washington, D.C. 20th, 136–138.
Apori SO, Castro FB, Shand WJ, Ørskov ER (1998) Chemical composition, in sacco degradation and in vitro gas production of some ghanaian browse plants. Animal Feed Science Technology 76:129–137. doi: 10.1016/S0377-8401(98)00205-3.
Benchaar C, McAllister TA, Chouinard PY (2008) Digestion, ruminal fermentation, ciliate protozoal populations, and milk production from dairy cows fed cinnamaldehyde, quebracho condensed tannin, or Yucca schidigera saponin extracts. Journal of Dairy Science 91:4765–4777. doi: 10.3168/jds.2008-1338.
Blanch M, Carro MD, Ranilla MJ, Viso A, Vázquez-Añón M, Bach A (2016) Influence of a mixture of cinnamaldehyde and garlic oil on rumen fermentation, feeding behavior and performance of lactating dairy cows. Animal Feed Science abd Technology 219:313–323. doi: 10.1016/j.anifeedsci.2016.07.002.
Blümmel M, Ørskov ER (1993) Comparison of in vitro gas production and nylon bag degradability of roughages in predicting feed intake in cattle. Animal Feed Science and Technology 40:109–119. doi: 10.1016/0377-8401(93)90150-I.
Blümmel M, Steingaβ H, Becker K (1997) The relationship between in vitro gas production, in vitro microbial biomass yield and N incorporation and its implications for the prediction of voluntary feed intake of roughages. British Journal of Nutrition 77:911–921. doi:10.1079/BJN19970089.
Busquet M, Calsamiglia S, Ferret A, Carro MD, Kamel C (2005) Effect of garlic oil and four of its compounds on rumen microbial fermentation. Journal of Dairy Science 88:4393–4404. doi: 10.3168/jds.S0022-0302(05)73126-X.
Cardozo PW, Kamel C (2008) Plant extract as rumen modifiers. International Dairy Topics. Volume 7:7-9.
Castillejos L, Calsamiglia S, Martín-Tereso J, Ter Wijlen H (2008) In vitro evaluation of effects of ten essential oils at three doses on ruminal fermentation of high concentrate feedlot-type diets. Animal Feed Science and Technology 145:259–270. doi: 10.1016/j.anifeedsci.2007.05.037.
Chaves AV, Stanford K, Dugan MER., Gibson LL, McAllister TA, Van Herk F, Benchaar C (2008) Effects of cinnamaldehyde, garlic and juniper berry essential oils on rumen fermentation, blood metabolites, growth performance, and carcass characteristics of growing lambs. Livestock Science 117:215–224. doi: 10.1016/j.livsci.2007.12.013.
Cobellis G, Acuti G, Forte C, Menghini L, De Vincenzi S, Orrú, M., Valiani, A., Pacetti, D., Trabalza-Marinucci, M., 2015. Use of Rosmarinus officinalis in sheep diet formulations: Effects on ruminal fermentation, microbial numbers and in situ degradability. Small Ruminant Research 126:10–18. doi: 10.1016/j.smallrumres.2015.01.018.
Cobellis G, Trabalza-Marinucci M, Marcotullio MC, Yu Z, (2016a) Evaluation of different essential oils in modulating methane and ammonia production, rumen fermentation, and rumen bacteria in vitro. Animal Feed Science and Technology 215:25–36. doi: 10.1016/j.anifeedsci.2016.02.008.
Cobellis G., Trabalza-Marinucci M, Yu Z (2016b) Critical evaluation of essential oils as rumen modifiers in ruminant nutrition: A review. Science of the Total Environment 545–546: 556–568. doi: 10.1016/j.scitotenv.2015.12.103.
Cochran WG, William G, Cox GM (1992) Experimental designs. Wiley.
De Rosa M, Gambacorta A, Gliozzi A (1986) Structure, biosynthesis, and physicochemical properties of archaebacterial lipids. Microbiological Reviews 50:70–80.
Dey A, Paul SS, Lailer PC, Dahiya SS (2021) Reducing enteric methane production from buffalo (Bubalus bubalis) by garlic oil supplementation in in vitro rumen fermentation system. SN Applied Sciences 3:187. doi: 10.1007/s42452-021-04264-6.
Diario Oficial de la Federación (2001) Norma oficial mexicana NOM-062-ZOO-1999 Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. CDMX. Available at: https://www.gob.mx/cms/uploads/attachment/file/203498/NOM-062-ZOO-1999_220801.pdf
Doreau M, Arturo-Schaan M, Laverroux S (2017) Garlic oil reduces ruminal fatty acid biohydrogenation in vitro. European Journal of Lipid Science and Technology 119:1-21. doi: 10.1002/ejlt.201500388.
European parliament (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 (Text with EEA relevance). Official Journal of the European Union 268:29–43.
FAO (2016) El estado mundial de la agricultura y la alimentación 2016: Cambio climático, agricultura y seguridad alimentaria. 49-75.
Ferme D, Banjac M, Calsamiglia S, Busquet M, Kamel C, Avgustin G (2004) The effects of plant extracts on microbial community structure in a rumen-simulating continuous-culture system as revealed by molecular profiling. Folia Microbiologica. 49:151–165.
Fernández-Agulló A, Freire MS, González-Álvarez J (2015) Effect of the extraction technique on the recovery of bioactive compounds from eucalyptus (Eucalyptus globulus) wood industrial wastes. Industrial Crops and Products 64:105–113. . doi: 10.1016/j.indcrop.2014.11.031.
Fondevila M, Pérez-Espés B (2008) A new in vitro system to study the effect of liquid phase turnover and pH on microbial fermentation of concentrate diets for ruminants. Animal Feed Science and Technology 144:196–211. doi: 10.1016/j.anifeedsci.2007.10.013.
Foskolos A, Siurana A, Rodriquez-Prado M, Ferret A, Bravo D, Calsamiglia S (2015) The effects of a garlic oil chemical compound, propyl-propane thiosulfonate, on ruminal fermentation and fatty acid outflow in a dual-flow continuous culture system. Journal of Dairy Science 98:5482–5491. doi: 10.3168/jds.2014-8674.
France J, Dhanoa MS, Theodorou MK, Lister SJ, Davies DR, Isac D, Williams BA, Dhanoa MS, Mcallan AB, France J (1993) A model to interpret gas accumulation profiles associated with in vitro degradation of ruminant feeds. Journal of Theoretical Biology 163:99–111. doi: 10.1006/jtbi.1993.1109.
García-González R, López S, Fernández M, Bodas R, González JS (2008) Screening the activity of plants and spices for decreasing ruminal methane production in vitro. Animal Feed Science and Technology 147:36–52. doi: 10.1016/J.ANIFEEDSCI.2007.09.008.
Gerber PJ, Steinfeld H, Henderson B, Mottet A, Opio C, Dijkman J, Falcucci A, Tempio, G (2013) Tackling climate change through livestock - A global assessment of emissions and mitigation opportunities, Food and Agriculture Organization of the United Nations 14:12-16.
Getachew, G., Makkar, H.P.S., Becker, K., 2002. Tropical browses: contents of phenolic compound and stoichiometric relationship between short chain fatty acid and in vitro gas production. J Agr Sci Camb 139:341–352. doi: 10.1017/S0021859602002393.
Getachew G, Robinson PH, DePeters EJ, Taylor SJ (2004) Relationships between chemical composition, dry matter degradation and in vitro gas production of several ruminant feeds. Animal Feed Science Technology 111:57–71. doi: 10.1016/S0377-8401(03)00217-7.
Gopu CL, Aher S, Mehta H, Paradkar AR, Mahadik KR (2008) Simultaneous determination of cinnamaldehyde, eugenol and piperine by HPTLC densitometric method. Phytochemicl Analysis 19:116–121. doi: 10.1002/pca.1022.
Grant RH, Mertens DR (1992) Influence of buffer ph and raw corn starch addition on in vitro fiber digestion kinetics. Journal of Dairy Science 75:2762–2768. doi: 10.3168/jds.S0022-0302(92)78039-4.
Griffin SG, Wyllie SG, Markham JL, Leach DN (1999) The role of structure and molecular properties of terpenoids in determining their antimicrobial activity. Flavour and Fragrance Journal 14:322–332.
Hart KJ, Yáñez-Ruiz DR, Duval SM, McEwan NR, Newbold CJ (2008) Plant extracts to manipulate rumen fermentation. Animal Feed Science and Technology 147:8–35. doi: 10.1016/j.anifeedsci.2007.09.007.
Hiltner P, Dehority BA (1983) Effect of soluble carbohydrates on digestion of cellulose by pure cultures of rumen bacteria. Applied and Environmental Microbiology 46:642-648.
Hoover WH (1986) Chemical factors involved in ruminal fiber digestion. Journal of Dairy Science 69:2755–2766.
Intergovernmental Panel on Climate Change IPCC (2014a) Climate change. Mitigation of climate change: 150-211. doi: 10.1017/CBO9781107415416.
Intergovernmental Panel on Climate Change IPCC (2014b) Informe de síntesis. contribución de los grupos de trabajo I, II y III al quinto informe de evaluación del grupo intergubernamental de expertos sobre el cambio climático: 170-200.
Jafari S, Goh YM, Rajion MA, Faseleh Jahromi M, Ebrahimi M (2016) Ruminal methanogenesis and biohydrogenation reduction potential of papaya (Carica papaya) leaf: an in vitro study. Italian Journal of Animal Science 15:157–165. doi: 10.1080/1828051X.2016.1141031.
Jahani-Azizabadi H, Mesgaran MD, Vakili AR, Rezayazdi K, Hashemi M (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. African Journal of Microbiology Research 5:4812–4819. doi: 10.5897/ajmr11.575.
Jiang Y, Wu N, Fu YJ, Wang W, Luo M, Zhao CJ, Zu YG, Liu XL (2011) Chemical composition and antimicrobial activity of the essential oil of Rosemary. Environmental Toxicology and Pharmacology 32:63–68. doi: 10.1016/j.etap.2011.03.011.
Joch M, Kudrna V, Hučko B (2017) Effects of geraniol and camphene on in vitro rumen fermentation and methane production. Scientia Agriculturae Bohemica 48:63–69. doi: 10.1515/sab-2017-0012.
Kamel C, Greathead HMR, Tejido ML, Ranilla MJ, Carro MD (2008) Effects of allicin and diallyl disulfide on in vitro rumen fermentation of a mixed diet. Animal Feed Science Technology 145:351–363.
Kamel C, Greathead MJ, Ranilla ML, Tejido S, Ramos M, Carro D (2009) Effects of garlic oil on in vitro rumen fermentation and methane production are influenced by the basal diet. Dairy Cattle: 110-15. Available at: https://en.engormix.com/dairy-cattle/forums/forum-effects-garlic-oil-t28442/
Kobayashi Y (2010) Abatement of methane production from ruminants: trends in the manipulation of rumen fermentation. Asian-Australasian Journal of Animal Sciences 23:410–416. doi: 10.5713/ajas.2010.r.01.
Lawson LD, Gardner CD (2005) Composition, stability, and bioavailability of garlic products used in a clinical trial. Journal of Agricultural and Food Chemistry 53:6254–6261. doi: 10.1021/jf050536+.
Macheboeuf D, Morgavi DP, Papon Y, Mousset JL, Arturo-Schaan M (2008) Dose-response effects of essential oils on in vitro fermentation activity of the rumen microbial population. Animal Feed Science and Technology 145:335–350. doi: 10.1016/j.anifeedsci.2007.05.044.
Mateos I, Ranilla MJ, Tejido ML, Saro C, Kamel C, Carro MD (2013) The influence of diet type (dairy versus intensive fattening) on the effectiveness of garlic oil and cinnamaldehyde to manipulate in vitro ruminal fermentation and methane production. Animal Production Science 53:299 -307. doi: 10.1071/AN12167.
Menke KH, Raab L, Steingass H (1979) The estimation of the digestibility and metabolizable content of ruminant feedingstudds from the gas production when they are incubated with rumen liquor in vitro. Journal of Agricultural Science 93:217–222.
Meyer NF, Erickson GE, Klopfenstein TJ, Greenquist MA, Luebbe MK, Williams P, Engstrom MA (2009) Effect of essential oils, tylosin, and monensin on finishing steer performance, carcass characteristics, liver abscesses, ruminal fermentation, and digestibility. Journal of Animal Science 87:2346–2354. doi: 10.2527/JAS.2008-1493.
National Research Council (U.S.). Subcommittee on Dairy Cattle Nutrition (2001) Nutrient Requirements of Dairy Cattle. National Academies Press.
O’Grady MN, Maher M, Troy DJ, Moloney AP, Kerry JP (2006) An assessment of dietary supplementation with tea catechins and rosemary extract on the quality of fresh beef. Meat Science 73:132–143.
O’Mara FP (2011) The significance of livestock as a contributor to global greenhouse gas emissions today and in the near future. Animal Feed Science and Technology 166–167:7–15. doi: 10.1016/J.ANIFEEDSCI.2011.04.074.
Ørskov E (1994) Recent advances in understanding of microbial transformation in ruminants. Livestock Production Science 39:53–60. doi: 10.1016/0301-6226(94)90153-8.
Patra AK (2012) Dietary phytochemicals and microbes. Springer.
Patra AK, Kamra DN, Agarwal N (2009) Effects of extracts of spices on rumen methanogenesis, enzyme activities and fermentation of feeds in vitro. JJournal of the Science of Food and Agriculture 90:511-520. doi: 10.1002/jsfa.3849.
Patra AK, Kamra DN, Agarwal N (2006a) Effect of plant extracts on in vitro methanogenesis, enzyme activities and fermentation of feed in rumen liquor of buffalo. Animal Feed Science and Technology 128:276–291. doi: 10.1016/j.anifeedsci.2005.11.001.
Patra AK, Kamra DN, Agarwal N (2006b) Effect of spices on rumen fermentation, methanogenesis and protozoa counts in in vitro gas production test. International Congress Series 1293:176–179. doi: 10.1016/j.ics.2006.01.025.
Patra AK, Saxena J (2009) Dietary phytochemicals as rumen modifiers: A review of the effects on microbial populations. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology 96:363–375. doi: 10.1007/s10482-009-9364-1.
Patra, Amlan K, Saxena, J. (2010). A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. In Phytochemistry (Vol. 71, Issues 11–12, pp. 1198–1222). Elsevier Ltd. https://doi.org/10.1016/j.phytochem.2010.05.010
Patra AK, Yu Z (2015) Effects of adaptation of in vitro rumen culture to garlic oil, nitrate, and saponin and their combinations on methanogenesis, fermentation, and abundances and diversity of microbial populations. Frontiers in Microbiology 6:1–11. doi: 10.3389/fmicb.2015.01434.
Patra AK, Yu Z (2012a) Effects of essential oils on methane production and fermentation by, and abundance and diversity of, rumen microbial populations. Applied and Environmental Microbiology 78:4271–4280. doi: 10.1128/AEM.00309-12.
Poornachandra KT, Malik PK, Dhali A, Kolte AP, Bhatta R (2019) Effect of combined supplementation of tamarind seed husk and soapnut on enteric methane emission in crossbred cattle. Carbon Management: 1–11. doi: 10.1080/17583004.2019.1640136.
Righi F, Simoni M, Foskolos A, Beretti V, Sabbioni A, Quarantelli A (2017) In vitro ruminal dry matter and neutral detergent fibre digestibility of common feedstuffs as affected by the addition of essential oils and their active compounds. Journal Animal Feed Science 26:204–212. doi: 10.22358/jafs/76754/2017.
Roy D, Tomar SK, Sirohi SK, Kumar V, Kumar M (2014) Efficacy of different essential oils in modulating rumen fermentation in vitro using buffalo rumen liquor. Veterinary World 7:213–218. doi: 10.14202/vetworld.2014.213-218.
Sahli F, Darej C, Moujahed N (2018) Potential of white garlic powder (Allium sativum L.) to modify in vitro ruminal fermentation. South African Journal of Animal Sciences 48 253–260. doi: 10.4314/SAJAS.V48I2.6.
Salem AZM (2012) Oral administration of leaf extracts to rumen liquid donor lambs modifies in vitro gas production of other tree leaves. Animal Feed Science and Technology 176: 94–101. doi: 10.1016/j.anifeedsci.2012.07.011.
Salzer UJ, Furia TE (1977) The Analysis of Essential Oils and Extracts (Oleoresins) from Seasonings - A Critical Review. Critical Reviews in Food Science and Nutrition 9:345-373. doi: 10.1080/10408397709527239.
Sharma V, McNeill JH (2009) To scale or not to scale: The principles of dose extrapolation. British Journal of Pharmacology 157:907-921. doi: 10.1111/j.1476-5381.2009.00267.x.
Sirohi SK, Pandey N, Goel N, Singh B, Mohini M, Pandey P, Chaudhry PP (2009) Microbial activity and ruminal methanogenesis as affected by plant secondary metabolites in different plant extracts. Environmental Engineering 1:52–58.
Theodorou MK, Williams BA, Dhanoa MS, McAllan AB, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology 48:185–197. doi: 10.1016/0377-8401(94)90171-6.
Tocmo R, Wu Y, Liang D, Fogliano V, Huang D (2016) Boiling enriches the linear polysulfides and the hydrogen sulfide-releasing activity of garlic. Food Chemistry 221:1867–1873. doi: 10.1016/j.foodchem.2016.10.076.
Torres-Salado N, Sánchez-Santillán P, Rojas-García AR, Herrera-Pérez J, Hernández-Morales J (2017) Producción de gases efecto invernadero in vitro de leguminosas arbóreas del trópico seco mexicano. Archivos de Zootecnia 67:55–59. doi: 10.21071/az.v67i257.3491.
Ultee A, Bennik MHJ, Moezelaar R (2002) The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Applied and Environmental Microbiology 68:1561–1568. doi: 10.1128/AEM.68.4.1561-1568.2002.
Ungerfeld EM (2018) Inhibition of rumen methanogenesis and ruminant productivity: A meta-analysis. Frontiers in Veterinary Science 5:1–13. doi: 10.3389/fvets.2018.00113.
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for Dietary Fiber, Neutral Detergent Fiber, and Nonstarch Polysaccharides in Relation to Animal Nutrition. Journal of Dairy Science 74:3583–3597. doi: 10.3168/jds.S0022-0302(91)78551-2.
Wencelová M, Váradyová Z, Mihaliková K, Čobanová K, Plachá I, Pristaš P, Jalč D, Kišidayová S (2015) Rumen fermentation pattern, lipid metabolism and the microbial community of sheep fed a high-concentrate diet supplemented with a mix of medicinal plants. Small Ruminant Research 125:64–72. doi: 10.1016/j.smallrumres.2015.01.028.
Williams WL, Tedeschi LO, Kononoff PJ, Callaway TR, Dowd SE, Karges K, Gibson ML (2010) Evaluation of in vitro gas production and rumen bacterial populations fermenting corn milling (co)products. Jornual of Dairy Science 93:4735–4743. doi: 10.3168/jds.2009-2920.
Yang WZ, Benchaar C, Ametaj BN, Chaves AV, He ML, McAllister TA (2007) Effects of garlic and juniper berry essential oils on ruminal fermentation and on the site and extent of digestion in lactating cows. Journal of Dairy Science 90:5671–5681. doi: 10.3168/jds.2007-0369.
Submitted date:
11/16/2021
Reviewed date:
12/27/2021
Accepted date:
12/27/2021
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email