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Effect of changes in lipid classes during wilting and ensiling of red clover using two silage additives on in vitro ruminal biohydrogenation

Published online by Cambridge University Press:  14 January 2016

F. GADEYNE
Affiliation:
Laboratory for Animal Nutrition and Animal Product Quality, Faculty of Bioscience Engineering, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium
K. DE RUYCK
Affiliation:
Laboratory for Animal Nutrition and Animal Product Quality, Faculty of Bioscience Engineering, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium
G. VAN RANST
Affiliation:
Laboratory for Animal Nutrition and Animal Product Quality, Faculty of Bioscience Engineering, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium
N. DE NEVE
Affiliation:
Laboratory for Animal Nutrition and Animal Product Quality, Faculty of Bioscience Engineering, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium
V. FIEVEZ*
Affiliation:
Laboratory for Animal Nutrition and Animal Product Quality, Faculty of Bioscience Engineering, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium
*
*To whom all correspondence should be addressed. Email: Veerle.Fievez@UGent.be

Summary

Although forage lipid is generally rich in polyunsaturated fatty acids (PUFA), recovery of these fatty acids (FA) in milk and meat of ruminant origin is generally low, due to microbial biohydrogenation (BH) taking place in the rumen. Since lipolysis is a prerequisite for BH, the latter process is expected to be enhanced when (conserved) forages contain lower levels of esterified FA (particularly polar lipids; PL). However, this was not observed in former studies with red clover (Trifolium pratense L.). Furthermore, red clover inclusion in the herbivore's diet was associated with decreased rumen BH as compared with other forages. Differences in plant lipase activity during wilting and ensiling has been attributed to changes in disappearance from the PL fraction, but a potential role of microbial lipases in silo has not yet been elucidated. Therefore, the aims of the present study were to assess whether BH of red clover FA is linked with PL levels of the (conserved) starting material and to clarify the possible role of in silo microbial activity on PL disappearance. In order to obtain sufficient variation in forage PL and microbial activity, laboratory-scale silages were made by wilting and ensiling damaged or undamaged red clover using molasses or formic acid as ensiling additive, while perennial ryegrass (Lolium perenne L.) was used as a control. Distribution of lipids within three lipid fractions (PL, free FA and neutral lipids) in forages was determined and BH calculated after 24 h in vitro rumen incubation. Results indicated microbial lipases in silages did not enhance FA disappearance from the PL fraction. A gradual decrease of FA in the PL fraction upon conservation was found, both in red clover and ryegrass, irrespective of the degree of damage. In red clover PL losses started from the wilting phase, while substantial PL disappearance from ryegrass only started upon ensiling. Proportions of PUFA remaining in the PL fraction after wilting and ensiling of red clover were positively correlated with PUFA BH, while this effect was not observed for ryegrass. Red clover PUFA seemed to be partially protected against ruminal BH, while disappearance of FA from the PL fraction did not seem to be hampered. Results indicated the encapsulation mechanism as a consequence of protein-bound phenol formation induced by polyphenol oxidase is still the most probable hypothesis to explain red clover's increased flow of PUFA across the rumen.

Type
Animal Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Ackman, R. G. & Sipos, J. C. (1964). Application of specific response factors in the gas chromatographic analysis of methyl esters of fatty acids with flame ionization detectors. Journal of the American Oil Chemists’ Society 41, 377378.CrossRefGoogle Scholar
Belury, M. A. (2002). Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annual Review of Nutrition 22, 505531.CrossRefGoogle ScholarPubMed
Boufaïed, H., Chouinard, P. Y., Tremblay, G. F., Petit, H. V., Michaud, R. & Bélanger, G. (2003 a). Fatty acids in forages. I. Factors affecting concentrations. Canadian Journal of Animal Science 83, 501511.CrossRefGoogle Scholar
Boufaïed, H., Chouinard, P. Y., Tremblay, G. F., Petit, H. V., Michaud, R. & Bélanger, G. (2003 b). Fatty acids in forages. II. In vitro ruminal biohydrogenation of linolenic and linoleic acids from timothy. Canadian Journal of Animal Science 83, 513522.CrossRefGoogle Scholar
Buccioni, A., Decandia, M., Minieri, S., Molle, G. & Cabiddu, A. (2012). Lipid metabolism in the rumen: new insights on lipolysis and biohydrogenation with an emphasis on the role of endogenous plant factors. Animal Feed Science and Technology 174, 125.CrossRefGoogle Scholar
Chaney, A. L. & Marbach, E. P. (1962). Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130132.CrossRefGoogle ScholarPubMed
Chilliard, Y., Glasser, F., Ferlay, A., Bernard, L., Rouel, J. & Doreau, M. (2007). Diet, rumen biohydrogenation and nutritional quality of cow and goat milk fat. European Journal of Lipid Science and Technology 109, 828855.CrossRefGoogle Scholar
Conway, E. J. (1957). Acetaldehyde from lactic acid and threonine with bisulphite absorption. In Microdiffusion Analysis and Volumetric Error (Ed. Conway, E. J.), pp. 276280. London: Crosby Lockwood & Sons Ltd.Google Scholar
Dewhurst, R. J. & King, P. J. (1998). Effects of extended wilting, shading and chemical additives on the fatty acids in laboratory grass silages. Grass and Forage Science 53, 219224.Google Scholar
Dewhurst, R. J., Scollan, N. D., Lee, M. R. F., Ougham, H. J. & Humphreys, M. O. (2003). Forage breeding and management to increase the beneficial fatty acid content of ruminant products. Proceedings of the Nutrition Society 62, 329336.CrossRefGoogle ScholarPubMed
Ding, W. R., Long, R. J. & Guo, X. S. (2013). Effects of plant enzyme inactivation or sterilization on lipolysis and proteolysis in alfalfa silage. Journal of Dairy Science 96, 25362543.Google Scholar
Fievez, V., Vlaeminck, B., Jenkins, T., Enjalbert, F. & Doreau, M. (2007). Assessing rumen biohydrogenation and its manipulation in vivo, in vitro and in situ . European Journal of Lipid Science and Technology 109, 740756.CrossRefGoogle Scholar
Gadeyne, F., Van Ranst, G., Vlaeminck, B., Vossen, E., Van Der Meeren, P. & Fievez, V. (2015). Protection of polyunsaturated oils against ruminal biohydrogenation and oxidation during storage using a polyphenol oxidase containing extract from red clover. Food Chemistry 171, 241250.CrossRefGoogle ScholarPubMed
Glasser, F., Schmidely, P., Sauvant, D. & Doreau, M. (2008). Digestion of fatty acids in ruminants: a meta-analysis of flows and variation factors: 2. C18 fatty acids. Animal 2, 691704.CrossRefGoogle ScholarPubMed
Halmemies-Beauchet-Filleau, A., Vanhatalo, A., Toivonen, V., Heikkila, T., Lee, M. R. F. & Shingfield, K. J. (2013). Effect of replacing grass silage with red clover silage on ruminal lipid metabolism in lactating cows fed diets containing a 60:40 forage-to-concentrate ratio. Journal of Dairy Science 96, 58825900.Google Scholar
Hassim, H. A., Lourenço, M., Goel, G., Vlaeminck, B., Goh, Y. M. & Fievez, V. (2010). Effect of different inclusion levels of oil palm fronds on in vitro rumen fermentation pattern, fatty acid metabolism and apparent biohydrogenation of linoleic and linolenic acid. Animal Feed Science and Technology 162, 155158.CrossRefGoogle Scholar
Hawke, J. C. (1973). Chemistry and biochemistry in herbage. In Lipids (Eds Butler, G. W. & Bailey, R. W.), pp. 213263. London, UK: Academic Press.Google Scholar
Hoefkens, C., Verbeke, W. & Van Camp, J. (2011). European consumers’ perceived importance of qualifying and disqualifying nutrients in food choices. Food Quality and Preference 22, 550558.CrossRefGoogle Scholar
Horrocks, L. A. & Yeo, Y. K. (1999). Health benefits of docosahexaenoic acid (DHA). Pharmacological Research 40, 211225.CrossRefGoogle ScholarPubMed
Huws, S. A., Lee, M. R. F., Muetzel, S. M., Scott, M. B., Wallace, R. J. & Scollan, N. D. (2010). Forage type and fish oil cause shifts in rumen bacterial diversity. FEMS Microbiology Ecology 73, 396407.Google Scholar
Jenkins, T. C. (1993). Lipid-metabolism in the rumen. Journal of Dairy Science 76, 38513863.CrossRefGoogle ScholarPubMed
Kaniuga, Z. (2008). Chilling response of plants: importance of galactolipase, free fatty acids and free radicals. Plant Biology 10, 171184.CrossRefGoogle ScholarPubMed
Kaup, M. T., Froese, C. D. & Thompson, J. E. (2002). A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiology 129, 16161626.CrossRefGoogle ScholarPubMed
Koivunen, E., Jaakkola, S., Heikkilä, T., Lampi, A. M., Halmemies-Beauchet-Filleau, A., Lee, M. R. F., Winters, A. L., Shingfield, K. J. & Vanhatalo, A. (2015). Effects of plant species, stage of maturity, and level of formic acid addition on lipolysis, lipid content, and fatty acid composition during ensiling. Journal of Animal Science 93, 44084423.CrossRefGoogle ScholarPubMed
Lattemae, P., Ohlsson, C. & Lingvall, P. (1996). Influence of molasses or molasses-formic acid treated red clover silage on feed intake and milk yield. Swedish Journal of Agricultural Research 26, 91100.Google Scholar
Lee, M. R. F. (2014). Forage polyphenol oxidase and ruminant livestock nutrition. Frontiers in Plant Science 5, 694. doi: 10.3389/fpls.2014.00694.CrossRefGoogle ScholarPubMed
Lee, M. R. F., Harris, L. J., Dewhurst, R. J., Merry, R. J. & Scollan, N. D. (2003). The effect of clover silages on long chain fatty acid rumen transformations and digestion in beef steers. Animal Science 76, 491501.CrossRefGoogle Scholar
Lee, M. R. F., Winters, A. L., Scollan, N. D., Dewhurst, R. J., Theodorou, M. K. & Minchin, F. R. (2004). Plant-mediated lipolysis and proteolysis in red clover with different polyphenol oxidase activities. Journal of the Science of Food and Agriculture 84, 16391645.CrossRefGoogle Scholar
Lee, M. R. F., Tweed, J. K. S., Minchin, F. R. & Winters, A. L. (2009). Red clover polyphenol oxidase: activation, activity and efficacy under grazing. Animal Feed Science and Technology 149, 250264.CrossRefGoogle Scholar
Lee, M. R. F., Tweed, J. K. S., Cookson, A. & Sullivan, M. L. (2010). Immunogold labelling to localize polyphenol oxidase (PPO) during wilting of red clover leaf tissue and the effect of removing cellular matrices on PPO protection of glycerol-based lipid in the rumen. Journal of the Science of Food and Agriculture 90, 503510.CrossRefGoogle ScholarPubMed
Lee, M. R. F., Tweed, J. K. S. & Sullivan, M. L. (2013). Oxidation of ortho-diphenols in red clover with and without polyphenol oxidase (PPO) activity and their role in PPO activation and inactivation. Grass and Forage Science 68, 8392.Google Scholar
Lee, M. R. F., Theobald, V. J., Gordon, N., Leyland, M., Tweed, J. K. S., Fychan, R. & Scollan, N. D. (2014). The effect of high polyphenol oxidase grass silage on metabolism of polyunsaturated fatty acids and nitrogen across the rumen of beef steers. Journal of Animal Science 92, 50765087.CrossRefGoogle ScholarPubMed
Lourenço, M., Van Ranst, G., De Smet, S., Raes, K., & Fievez, V. (2007). Effect of grazing pastures with different botanical composition by lambs on rumen fatty acid metabolism and fatty acid pattern of longissimus muscle and subcutaneous fat. Animal 1, 537545.CrossRefGoogle ScholarPubMed
Lourenço, M., Ramos-Morales, E. & Wallace, R. J. (2010). The role of microbes in rumen lipolysis and biohydrogenation and their manipulation. Animal 4, 10081023.CrossRefGoogle ScholarPubMed
Meyers, S. A., Cuppett, S. L. & Hutkins, R. W. (1996). Lipase production by lactic acid bacteria and activity on butter oil. Food Microbiology 13, 383389.CrossRefGoogle Scholar
Munoz-Munoz, J. L., Garcia-Molina, F., Varon, R., Garcia-Ruiz, P. A., Tudela, J., Garcia-Canovas, F. & Rodriguez-Lopez, J. N. (2010). Suicide inactivation of the diphenolase and monophenolase activities of tyrosinase. IUBMB Life 62, 539547.CrossRefGoogle ScholarPubMed
Parveen, I., Threadgill, M. D., Moorby, J. M. & Winters, A. (2010). Oxidative phenols in forage crops containing polyphenol oxidase enzymes. Journal of Agricultural and Food Chemistry 58, 13711382.CrossRefGoogle ScholarPubMed
Simopoulos, A. P. (1991). Omega-3-fatty-acids in health and disease and in growth and development. American Journal of Clinical Nutrition 54, 438463.CrossRefGoogle ScholarPubMed
Van Ranst, G., Fievez, V., De Riek, J. & Van Bockstaele, E. (2009 a). Influence of ensiling forages at different dry matters and silage additives on lipid metabolism and fatty acid composition. Animal Feed Science and Technology 150, 6274.CrossRefGoogle Scholar
Van Ranst, G., Fievez, V., Vandewalle, M., De Riek, J. & Van Bockstaele, E. (2009 b). Influence of herbage species, cultivar and cutting date on fatty acid composition of herbage and lipid metabolism during ensiling. Grass and Forage Science 64, 196207.CrossRefGoogle Scholar
Van Ranst, G., Fievez, V., Vandewalle, M., De Riek, J. & Van Bockstaele, E. (2009 c). In vitro study of red clover polyphenol oxidase activity, activation, and effect on measured lipase activity and lipolysis. Journal of Agricultural and Food Chemistry 57, 66116617.CrossRefGoogle ScholarPubMed
Van Ranst, G., Fievez, V., Vandewalle, M., Van Waes, C., De Riek, J. & Van Bockstaele, E. (2010). Influence of damaging and wilting red clover on lipid metabolism during ensiling and in vitro rumen incubation. Animal 4, 15281540.CrossRefGoogle ScholarPubMed
Van Ranst, G., Lee, M. R. F. & Fievez, V. (2011). Red clover polyphenol oxidase and lipid metabolism. Animal 5, 512521.CrossRefGoogle ScholarPubMed
Van Ranst, G., Vandewalle, M., Gadeyne, F., De Riek, J. & Fievez, V. (2013). Lipid metabolism in mixtures of red clover (Trifolium repens) and perennial ryegrass (Lolium perenne) in lab scale silages and in vitro rumen incubations. Animal 7, 14541463.CrossRefGoogle ScholarPubMed
Winters, A., Minchin, F. R., Merry, R. J. & Morris, P. (2003). Comparison of polyphenol oxidase activity in red clover and perennial ryegrass. Aspects of Applied Biology 70, 121128.Google Scholar
Wolff, R. L., Bayard, C. C. & Fabien, R. J. (1995 ). Evaluation of sequential methods for the determination of butterfat fatty acid composition with emphasis on trans-18:1 acids. Application to the study of seasonal variations in French butters. Journal of the American Oil Chemists’ Society 72, 14711483.CrossRefGoogle Scholar
Wood, J. D., Enser, M., Fisher, A. V., Nute, G. R., Sheard, P. R., Richardson, R. I., Hughes, S. I. & Whittington, F. M. (2008). Fat deposition, fatty acid composition and meat quality: a review. Meat Science 78, 343358.CrossRefGoogle ScholarPubMed
Yoruk, R. & Marshall, M. R. (2003). Physicochemical properties and function of plant polyphenol oxidase: a review. Journal of Food Biochemistry 27, 361422.Google Scholar
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