Czech J. Anim. Sci., 2018, 63(8):293-304 | DOI: 10.17221/118/2017-CJAS

In vitro bioactivity of various pure flavonoids in ruminal fermentation, with special reference to methane formationOriginal Paper

Susanne Sinz1, Carmen Kunz1, Annette Liesegang2, Ueli Braun3, Svenja Marquardt1, Carla R. Soliva1, †, Michael Kreuzer*,1
1 ETH Zürich, Institute of Agricultural Sciences, Zürich, Switzerland
2 Institute of Animal Nutrition, Vetsuisse Faculty, University of Zürich, Zürich, Switzerland
3 Department of Farm Animals, Vetsuisse Faculty, University of Zürich, Zürich, Switzerland

Polyphenols, like flavonoids, have been investigated when present in intact plants or in extracts as methane mitigating dietary supplements in ruminants. The aim of the present study was to examine pure compounds in a short-term in vitro experiment using the Hohenheim Gas Test method. We focused on the group of the flavonoids and tested which of them had the potential to mitigate methane without negatively affecting ruminal fermentation. Eight flavonoids were tested: epicatechin, luteolin-7-glucoside, quercetin, and isoquercetin in Experiment 1; catechin, gallocatechin, epigallocatechin, and epigallocatechin gallate in Experiment 2. Tannic acid, no flavonoid but a phenolic acid with known methane mitigating properties, served as positive control, and the unsupplemented basal diet as negative control. In both experiments, each of these compounds (including tannic acid) was tested at dosages of 0.5, 5.0, and 50.0 mg/g basal diet dry matter (DM) in four runs each. Gallocatechin, tannic acid, and epigallocatechin gallate (50 mg/g DM) lowered fermentation gas formation and in vitro organic matter digestibility relative to the negative control (Experiment 2). Apart from tannic acid, epicatechin, quercetin, isoquercetin, and luteolin-7-glucoside (5 and 50 mg/g DM) reduced the amount of CH4 produced in relation to total gas produced (Experiment 1). The incubation fluid ammonia concentration was decreased with luteolin-7-glucoside and tannic acid (50 mg/g DM). From the flavonoids tested especially luteolin-7-glucoside seems to have a similar potential as tannic acid to mitigate methane and ammonia formation during ruminal fermentation in vitro, both favourable in environmental respect. These results need to be confirmed in live animals.

Keywords: rumen; ammonia; Hohenheim Gas Test; epicatechin; isoquercetin; luteolin-7-glucoside; quercetin; catechin; tannic acid

Published: August 31, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Sinz S, Kunz C, Liesegang A, Braun U, Marquardt S, Soliva CR, Kreuzer M. In vitro bioactivity of various pure flavonoids in ruminal fermentation, with special reference to methane formation. Czech J. Anim. Sci. 2018;63(8):293-304. doi: 10.17221/118/2017-CJAS.
Download citation

References

  1. Aerts R.J., Barry T.N., McNabb W.C. (1999): Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agriculture, Ecosystems and Environment, 75, 1-12. Go to original source...
  2. AOAC (1997): Official Methods of Analysis. 16 th Ed. Association of Official Analytical Chemists, Arlington, USA.
  3. Beauchemin K.A., Kreuzer M., O'Mara F., McAllister T.A. (2008): Nutritional management for enteric methane abatement: a review. Australian Journal of Experimental Agriculture, 48, 21-27. Go to original source...
  4. Becker P.M., van Wikselaar P.G., Franssen M.C.R., de Vos R.C.H., Hall R.D., Beekwilder J. (2014): Evidence for a hydrogen-sink mechanism of (+)catechin-mediated emission reduction of the ruminant greenhouse gas methane. Metabolomics, 10, 179-189. Go to original source...
  5. Berger L.M., Blank R., Zorn F., Wein S., Metges C.C., Wolffram S. (2015): Ruminal degradation of quercetin and its influence on fermentation in ruminants. Journal of Dairy Science, 98, 5688-5698. Go to original source... Go to PubMed...
  6. Bhagwat S., Haytowitz D.B., Holden J.M. (2014): USDA Database for the Flavonoid Content of Selected Foods, Release 3.1. US Department of Agriculture, Agricultural Research Service, Beltsville, USA. Available from https://www.ars.usda.gov/ARSUserFiles/80400525/Data/Flav/Flav_R03-1.pdf (accessed July 17, 2018).
  7. Bjorklund G., Chirumbolo S. (2017): Role of oxidative stress and antioxidants in daily nutrition and human health. Nutrition, 33, 311-321. Go to original source... Go to PubMed...
  8. Cieslak A., Szumacher-Strabel M., Stochmal A., Oleszek W. (2013): Plant components with specific activities against rumen methanogens. Animal, 7 (Suppl. 2), 253-265. Go to original source... Go to PubMed...
  9. Cieslak A., Zmora P., Stochmal A., Pecio L., Oleszek W., Pers-Kamczyc E., Szczechowiak J., Nowak A., SzumacherStrabel M. (2014): Rumen antimethanogenic effect of Saponaria officinalis L. phytochemicals in vitro. The Journal of Agricultural Science, 152, 981-993. Go to original source...
  10. Cieslak A., Zmora P., Matkowski A., Nawrot-Hadzik I., PersKamczyc E., El-Sherbiny M., Bryszak M., SzumacherStrabel M. (2016): Tannins from Sanguisorba officinalis affect in vitro rumen methane production and fermentation. Journal of Animal and Plant Sciences, 26, 54-62.
  11. Cortes J.E., Moreno B., Pabon M.L., Avila P., Kreuzer M., Hess H.D., Carulla J.E. (2009): Effects of purified condensed tannins extracted from Calliandra, Flemingia and Leucaena on ruminal and postruminal degradation of soybean meal as estimated in vitro. Animal Feed Science and Technology, 151, 194-204. Go to original source...
  12. Crozier A., Clifford M.N., Ashihara H. (2006): Phenols, polyphenols and tannins: an overview. In: Crozier A., Clifford M.N., Ashihara H. (eds): Plant Secondary Metabolites: Occurrence, Structure and Role in the Human Diet. Blackwell Publishing, 1-24. Go to original source...
  13. Ehrlich G.G., Goerlitz D.F., Bourell J.H., Eisen G.V., Godsy E.M. (1981): Liquid chromatographic procedure for fermentation product analysis in the identification of anaerobic bacteria. Applied and Environmental Microbiology, 42, 878-885. Go to original source... Go to PubMed...
  14. Erlund I. (2004): Review of the flavonoids quercetin, hesperetin, and naringenin. Dietary sources, bioactivities, bioavailability, and epidemiology. Nutrition Research, 24, 851-874. Go to original source...
  15. Fabjan N., Rode J., Kosir I.J., Wang Z., Zhang Z., Kreft I. (2003): Tartar y buckwheat (Fagopyrum tataricum Gaertn.) as a source of dietary rutin and quercitrin. Journal of Agricultural and Food Chemistry, 51, 6452-6455. Go to original source... Go to PubMed...
  16. Field J.A., Lettinga G. (1987): The methanogenic toxicity and anaerobic degradability of a hydrolyzable tannin. Water Research, 21, 367-374. Go to original source...
  17. Gorosito A.R., Russell J.B., Van Soest P.J. (1985): Effect of carbon-4 and carbon-5 volatile fatty acids on digestion of plant cell wall in vitro. Journal of Dairy Science, 68, 840-847. Go to original source...
  18. Hatahet T., Morille M., Hommoss A., Devoisselle J.M., Muller R.H., Begu S. (2016): Quercetin topical application, from conventional dosage forms to nanodosage forms. European Journal of Pharmaceutics and Biopharmaceutics, 108, 41-53. Go to original source... Go to PubMed...
  19. Jayanegara A., Wina E., Soliva C.R., Marquardt S., Kreuzer M., Leiber F. (2011): Dependence of forage quality and methanogenic potential of tropical plants on their phenolic fractions as determined by principal component analysis. Animal Feed Science and Technology, 163, 231-243. Go to original source...
  20. Jayanegara A., Leiber F., Kreuzer M. (2012): Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. Journal of Animal Physiology and Animal Nutrition, 96, 365-375. Go to original source... Go to PubMed...
  21. Leiber F., Kunz C., Kreuzer M. (2012): Influence of different morphological parts of buckwheat (Fagopyrum esculentum) and its major secondary metabolite rutin on rumen fermentation in vitro. Czech Journal of Animal Science, 57, 10-18. Go to original source...
  22. Makkar H.P.S., Becker K., Abel H., Szegletti C. (1995): Degradation of condensed tannins by rumen microbes exposed to quebracho tannins (QT) in rumen simulation technique (RUSITEC) and effects of QT on fermentative processes in the RUSITEC. Journal of the Science of Food and Agriculture, 69, 495-500. Go to original source...
  23. Manach C., Scalbert A., Morand C., Remesy C., Jimenez L. (2004): Polyphenols: food sources and bioavailability. American Society for Clinical Nutrition, 79, 727-747. Go to original source... Go to PubMed...
  24. McSweeney C.S., Palmer B., McNeill D.M., Krause D.O. (2001): Microbial interactions with tannins: nutritional consequences for ruminants. Animal Feed Science and Technology, 91, 83-93. Go to original source...
  25. Menke K.H., Steingass H. (1988): Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Animal Research and Development, 28, 7-55.
  26. Nelson K.E., Pell A.N., Schofield P., Zinder S. (1995): Isolation and characterization of an anaerobic ruminal bacterium capable of degrading hydrolyzable tannins. Applied and Environmental Microbiology, 61, 3293-3298. Go to original source... Go to PubMed...
  27. Patra A.K., Min B.R., Saxena J. (2011): Dietary tannins on microbial ecology of the gastrointestinal tract in ruminants. In Patra A.K. (ed.): Dietary Phytochemicals and Microbes. Springer, Dordrecht, the Netherlands, 237-262. Go to original source...
  28. Scola G., Conte D., Spada P.W., Dani C., Vanderlinde R., Funchal C., Salvador M. (2010): Flavan-3-ol compounds from wine wastes with in vitro and in vivo antioxidant activity. Nutrients, 2, 1048-1059. Go to original source... Go to PubMed...
  29. Soliva C.R., Hess H.D. (2007): Measuring methane emission of ruminants by in vitro and in vivo techniques. In: Makkar H.P.S., Vercoe P.E. (eds): Measuring Methane Production from Ruminants. Springer, Dordrecht, the Netherlands, 15-31. Go to original source...
  30. Terrill T.H., Rowan A.M., Douglas G.B., Barry T.N. (1992): Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. Journal of the Science of Food and Agriculture, 58, 321-329. Go to original source...
  31. Wang D., Huang J., Zhang Z., Tian X., Huang H., Yu Y., Zhang G., Ding J., Huang R. (2013): Influences of Portulaca oleracea extracts on in vitro methane emissions and rumen fermentation of forage. Journal of Food, Agriculture and Environment, 11, 483-488.
  32. Wischer G., Boguhn J., Steingass H., Schollenberger M., Rodehutscord M. (2013): Effects of different tannin-rich extracts and rapeseed tannin monomers on methane formation and microbial protein synthesis in vitro. Animal, 7, 1796-1805. Go to original source... Go to PubMed...
  33. Yang K., Wei C., Zhao G.Y., Xu Z.W., Lin S.X. (2017): Effects of dietary supplementing tannic acid in the ration of beef cattle on rumen fermentation, methane emission, microbial flora and nutrient digestibility. Journal of Animal Physiology and Animal Nutrition, 101, 302-310. Go to original source... Go to PubMed...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.