The Effects of Phenolic Compounds in Iranian Propolis Extracts on in vitro Rumen Fermentation, Methane Production and Microbial Population
الموضوعات :ش. احتشام 1 , ع.ر. وکیلی 2 , م. دانش مسگران 3 , و. بانکوا 4
1 - Department of Animal Science, Ferdowsi University of Mashhad, International Campus, Mashhad, Iran
2 - Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran
3 - Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran
4 - Institute of Organic Chemistry with Centre of Phytochemistry, Bulgarian Academy of Science, Acad. G. Bonchev Str., bl. 9, 1113 Sofia, Bulgaria
الکلمات المفتاحية: gas production, methane production, microbial, Iranian propolis extracts, rumen fer-mentation,
ملخص المقالة :
The objective of this study was to determine the chemical compounds of Iranian propolis (IP) extracts and to show flavonoids and phenol effects on methane production, fermentation characteristics and rumen microbial population (in vitro). In this study two diets with different concentrate: forage ratios as (HC: high concentrate) and (MC: middle concentrate), respectively as non-supplemented or supplemented with different Iranian propolis (IP) extracts were used. The treatments were HC (control), HC + IP 25%, HC + IP 50%, HC + IP 75%, MC (control), MC + IP 25%, MC + IP 50% and MC + IP 75%, which means 25, 50 and 75 g of propolis in 100 mL ethanol 70%, respectively. The results showed that IP significantly increased gas production in IP 75% with different concentrate: forage ratios. Adding IP caused a decrease in pH, however this decrease was not significant in all treatments. There was a significant difference between the effect of HC + IP 50% on NH3-N compared to the HC + IP 25% and HC. Adding IP 75% significantly decreased CH4 production compared to the other treatments. In HC diet, there was no significant difference in total populations of protozoa and Ruminococcus albus between the individual IP 25%, 50%, 75% treatments, however when they were considered as the group, a significant difference was observed between them and the control group. The highest decrease and the highest increase in total populations of Prevotella bryantii was observed in IP 75% and in IP25%, respectively. In MC diet, methanogens were significantly reduced in IP 25%, 50% and 75%, compared to control treatment. The propolis extract caused improvement in fermentation and decreased methane and nitrogen ammonia. This may help the nitrogen retain longer in ruminants.
Aguiar S.C., Cottica S.M., Boeing J.S., Samensari R.B., Santos G.T., Visentainer J.V. and Zeoula L.M. (2014). Effect of feeding phenolic compounds from propolis extracts to dairy cows on milk production, milk fatty acid composition, and the antioxidant capacity of milk. Anim. Feed Sci. Technol. 193, 148-154.
Aguiar S.C., Zeoula L.M., Franco S.L., Peres L.P., Arcuri P.B. and Forano E. (2013). Antimicrobial activity of Brazilian propolis extracts against rumen bacteria in vitro. World J. Microbiol. Biotechnol. 29, 1951-1959.
Amoros M., Lurton E., Boustie J., Girre L., Sauvager F. and Cormier M. (1994). Comparison of the anti-herpes simplex virus activities of propolis and 3-methyl-but-2-enyl caffeate. J. Nat. Prod. 57, 644-647.
AOAC. (2005). Official Methods of Analysis. Vol. I. 18th Ed. Association of Official Analytical Chemists, Arlington, VA, USA.
Balcells J., Aris A., Serrano A., Seradj A.R., Crespo J. and Devant M. (2012). Effects of an extract of plant flavonoids (Bioflavex) on rumen fermentation and performance in heifers fed high-concentrate diets. J. Anim. Sci. 90, 4975-4984.
Bankova V., Castro S.L. and Marcucci M.C. (2000). Propolis: recent advances in chemistry and plant origin. Apidologie. 31, 3-15.
Bankova V., Dyulgerov A., Popov S. and Marekov V. (1992). Propolis produced in Bulgaria and Mongolia: Phenolic compounds and plant origin. Apidologie. 23, 79-85.
Bodas R., Prieto N., García-González R., Andrés S., Giráldez F.J. and López S. (2012). Manipulation of rumen fermentation and methane production with plant secondary metabolites. Anim. Feed Sci. Technol. 176, 78-93.
Castaldo S. and Capasso F. (2002). Propolis, an old remedy used in modern medicine. Fitoterapia. 73(1), 1-6.
Cottica S.M., Sawaya A.C.H.E., Eberlin M.N., Franco S.L., Zeoula L.M. and Visentainer J.V. (2011). Antioxidant activity and composition of propolis obtained by different methods of extraction. J. Brazilian Chem. Soc. 22, 929-935.
Denman S.E. and McSweeney C.S. (2006). Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiol. Ecol. 58, 572-582.
Denman S.E., Tomkins N.W. and McSweeney C.S. (2007). Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiol. Ecol. 62, 313-322.
Dimov V., Ivanovska N., Manolova N., Bankova V., Nikolov N. and Popov S. (1991). Immunomodulatory action of propolis: Influence on anti-infectious protection and macrophage function. Pidologie. 22, 155-162.
El-Bassuony A.A. (2009). New prenilated compound from Egyptian propolis with antimicrobial activity. Rev. Latinoam. Quím. 39, 85-90.
Isla M.I., Nieva Moreno M.I., Sampietro A.R. and Vattuone M.A. (2001). Antioxidant activity of Argentine propolis extracts. J. Ethnopharmacol. 76, 165-170.
Koike S. and Kobayashi Y. (2001). Development and use of competitive PCR assays for the rumen cellulolytic bacteria: Fibrobacter succinogenes, Ruminococcus albus and Ruminococcus flavefaciens. FEMS Microbiol. Lett. 204, 361-366.
Krause D.O., Bunch B.R., Smith W.J.M. and McSweeney C.S. (1999). Diversity of Ruminococcus strains: A survey of genetic polymorphisms and plant digestibility. J. Appl. Microbiol. 86, 487-495.
Kreuzer M., Kirchgessner M. and Müller H.L. (1986). Effect of defaunation on the loss of energy in wethers fed different quantities of cellulose and normal or steamflaked maize star-ch. Anim. Feed Sci. Technol. 16, 233-241.
Maeda H., Fujimoto C., Haruki Y., Maeda T., Kokeguchi S., Petelin M., Arai H., Tanimoto I., Nishimura F. and Takashiba S. (2003). Quantitative real-time PCR using TaqMan and SYBR green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria. FEMS Immunol. Med. Microbiol. 39, 81-86.
Makkar H.P.S. and Vercoe P.E. (2007). Measuring Methane Production from Ruminants. Publications of Springer, Berlin, Germany.
Marcucci M.C. (1995). Propolis: Chemical composition, biological properties and therapeutic activity. Apidologie. 26, 83-89.
McGuffey R.K., Richardson L.F. and Wilkinson J.I.D. (2001). Ionophores for dairy cattle: Current status and future outlook. J. Dairy Sci. 84, 194-203.
Menke H.H. and Steingass H. (1988). Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Dev. 28, 7-55.
Mirzoeva O.K., Grishanin R.N. and Calder P.C. (1997). Antimicrobial action of propolis and some of its components: The effects on growth, membrane potential and motility of bacteria. Microbiol. Res. 152, 239-246.
Miyataka H., Nishiki M., Matsumoto H., Fujimoto T., Matsuka M. and Satoh T. (1997). Evaluation of propolis: Evaluation of Brazilian and Chinese propolis by enzymatic and physico-chemical methods. Biol. Pharm. Bull. 20, 496-501.
Murad J.M., Calvi S.A., Soares A.M.V.C., Bankova V. and Sforcin J.M. (2002). Effects of propolis from Brazil and Bulgaria on fungicidal activity of macrophages against Paracoccidioides brasiliensis. J. Ethnopharmacol. 79, 331-334.
Nisbet D.J., Edrington T.S., Anderson R.C. and Krueger N. (2009). Effects of the dicarboxylic acids malate and fumarate on E. coli O157:H7 and Salmonella enteric typhimurium populations in pure culture and in mixed ruminal microorganism fermentations. Curr. Microbiol. 58, 488-492.
Oliveira J.S., Borges L.R., Queiroz A.C. and Almeida I.C.C. (2004). Effect of monensin and propolis extract on ammonia production and in vitro degradability of crude protein of different nitrogen sources. Rev. Brasileira Zootec. 33, 504-510.
Oliveira J.S., Queiroz A.C., Lana R.P., Mantovani H.C. and Generoso R.A.R. (2006). Effect of monensin and bee propolis on in vitro fermentation of amino acids by mixed ruminal bacteria. Rev. Brasileira Zootec. 35, 275-281.
Orskov E.R. and McDonald I. (1979). The estimation of protein degradability in the rumen from incubation measurements weighed according to rate of passage. J. Agric. Sci. 92, 499-503.
Oskoueian E., Abdullah N. and Oskoueian A. (2013). Effects of flavonoids on rumen fermentation activity, methane production, and microbial population. BioMed Res. Int. 2013, 1-8.
Ozturk H., Pekcan M., Sireli M. and Fidanci U.R. (2010). Effects of propolis on in vitro rumen microbial fermentation. Ankara Üniv. Vet. Fak. Derg. 57, 217-221.
Padmavati M., Sakthivel N., Thara K.V. and Reddy A.R. (1997). Differential sensitivity of rice pathogens to growth inhibition by flavonoids. Phytochemistry. 46, 499-502.
Paint Z.M. and Metzner J. (1979). On the local anaesthetic action of propolis and some of its constituents. Biol. Pharm. Bull. 34, 839.
Patra A.K., Kamra D.N. and Agarwal N. (2006). Effect of plant extracts on in vitro methanogenesis, enzyme activities and fermentation of feed in rumen liquor of buffalo. Anim. Feed Sci. Technol. 128, 276-291.
Rispoli T.B., Rodrigues I.L., Martins Neto R.G., Kazama R., Prado O.P.P., Zeoula L.M. and Arcuri P.B. (2009). Ruminal ciliate protozoa of cattle and buffalo fed on diet supplemented with monensin or extracts from propolis. Pes. Agrop. Brasileira. 44, 92-97.
Santos N.W., Yoshimura E.H., Machado E., Matumoto-Pintro P.T., Montanher P.F., Visentainer J.V., dos Santos G.T. and Zeoula L.M. (2016). Antioxidant effects of a propolis extract and vitamin E in blood and milk of dairy cows fed diet containing flaxseed oil. Livest. Sci. 191, 132-138.
SAS Institute. (2001). SAS®/STAT Software, Release 9.1. SAS Institute, Inc., Cary, NC. USA.
Sforcin J.M. and Bankova V. (2011). Propolis: Is there a potential for the development of new drugs? J. Ethnopharmacol. 133, 253-260.
Sforcin J.M., Fernandes Jr A., Lopes C.A.M., Bankova V. and Funari S.R.C. (2000). Seasonal effect on Brazilian propolis antibacterial activity. J. Ethnopharmacol. 73, 243-249.
Swain T. and Hillis W.E. (1959). The phenolic constituents of Prunus domestica. I.-The quantitative analysis of phenolic constituents. J. Sci. Food. Agric. 10(1), 63-68.
Tavendale M.H., Meagher L.P., Pacheco D., Walker N., Attwood G.T. and Sivakumaran S. (2005). Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Anim. Feed Sci. Technol. 123(1), 403-419.
Valizadeh R., Behgar M., Mirzaee M., Naserian A.A., Vakili A.R. and Ghovvati S. (2010). The effect of physically effective fiber and soy hull on the ruminal cellulolytic bacteria population and milk production of dairy cows. Asian-Australasian J. Anim. Sci. 23, 1325-1332.
Van Soest P.J., Robertson J.B. and Lewis B.A. (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583-3597.
Velikova M., Bankova V., Tsvetkova I., Kujumgiev A. and Marcucci M.C. (2000). Antibacterial ent-kaurene from Brazilian propolis of native stingless bees. Fitoterapia. 71, 693-696.
Wallace R.J. (2004). Antimicrobial properties of plant secondary metabolites. Proc. Nutr. Soc. 63, 621-629.
Ware C.E., Banehop T. and Gregg K. (1989). The isolation and comparison of ellulose genes from two strains of Ruminococcus albus. J. Gen. Microbiol. 135, 921-930.
Weatherburn M.W. (1967). Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. 39, 971-974.
Zia M., Mannani R., Mahmoodi M., Bayat M. and Mohaghegh F. (2009). The Effects of alcoholic extract of propolis obtained from Iran bee hives on the growth of trichophyton mentagrophytis, trichophyton rubrum and trichophyton verrucosum. J. Isfahan Med. Sch. 27, 232-241.
