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Biohydrogenation of dietary n-3 PUFA and stability of ingested vitamin E in the rumen, and their effects on microbial activity in sheep

Published online by Cambridge University Press:  09 March 2007

S. Chikunya ,
G. Demirel ,
M. Enser ,
J. D. Wood ,
R. G. Wilkinson  and
L. A. Sinclair
S. Chikunya*
Affiliation:
ASRC, Harper Adams University College, School of Agriculture, Edgmond, Newport, Shropshire TF10 8NB, UK
G. Demirel
Affiliation:
Division of Food Animal Science, School of Veterinary Science, University of Bristol, Bristol BS40 5DU, UK
M. Enser
Affiliation:
Division of Food Animal Science, School of Veterinary Science, University of Bristol, Bristol BS40 5DU, UK
J. D. Wood
Affiliation:
Division of Food Animal Science, School of Veterinary Science, University of Bristol, Bristol BS40 5DU, UK
R. G. Wilkinson
Affiliation:
ASRC, Harper Adams University College, School of Agriculture, Edgmond, Newport, Shropshire TF10 8NB, UK
L. A. Sinclair
Affiliation:
ASRC, Harper Adams University College, School of Agriculture, Edgmond, Newport, Shropshire TF10 8NB, UK
*
*Corresponding author: Dr Sifelani Chikunya, present address: Faculty of Applied Science and Technology, Writtle College, Chelmsford, Essex CM1 3RR, UK, fax +44 1952 420456, email [email protected]
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Abstract

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The present study investigated the susceptibility of dietary n-3 PUFA to ruminal biohydrogenation, the stability of ingested vitamin E in the rumen and the subsequent uptake of PUFA and vitamin E into plasma. Six cannulated sheep were assigned to six diets over five 33d periods, in an incomplete 6×5 Latin square. The diets, based on dried grass, were formulated to supply 50g fatty acids/kg DM using three lipid sources: Megalac® (calcium soap of palm fatty acid distillate; Volac Ltd, Royston, Herts., UK), linseed (formaldehyde-treated; Trouw Nutrition, Northwich, Ches., UK) and linseed–fish oil (formaldehyde-treated linseed+fish oil). The diets were supplemented with 100 or 500mg α-tocopheryl acetate/kg DM. Fat source or level of vitamin E in the diet did not alter microbial activity in the rumen. Biohydrogenation of linoleic acid (18:3n-6; 85–90%), linolenic acid (18:3n-3; 88–93%), docosahexaenoic acid (22:6n-3; 91%) and EPA (20:5n-3; 92%) was extensive. Feeding formaldehyde-treated linseed elevated concentrations of 18:3n-3 in plasma, whilst 22:6n-3 and 20:5n-3 were only increased by feeding the linseed–fish oil blend. Duodenal recovery of ingested vitamin E was high (range 0·79–0·92mg/mg fed). High dietary vitamin E was associated with increased plasma α-tocopherol (2·57 v. 1·46μg/ml for 500 and 100mg α-tocopheryl acetate/kg DM respectively), although all concentrations were low. Plasma vitamin E levels, however, tended to decrease as the type and quantity of PUFA in the diet increased. The present study illustrates that nutritionally beneficial PUFA in both fish and linseed oils are highly susceptible to biohydrogenation in the rumen. Although α-tocopheryl acetate resisted degradation in the rumen, plasma vitamin E status remained deficient to borderline, suggesting either that uptake may have been impaired or metabolism post-absorption increased.

Keywords

Polyunsaturated fatty acidsVitamin EMicrobial protein synthesis
Type
Research Article
Information
British Journal of Nutrition , Volume 91 , Issue 4 , April 2004 , pp. 539 - 550
Copyright
Copyright © The Nutrition Society 2004

References

Agricultural Research Council (1980) The Nutrient Requirements of Ruminant Livestock. (Slough, Bucks.: Commonwealth Agricultural Bureaux).Google Scholar
Alderson, NE, Mitchell, JR, Little, GE, Warner, RE & Tucker, RE (1971) Pre-intestinal disappearance of vitamin E in ruminants. J Nutr 101, 655–660.CrossRefGoogle Scholar
Ashes, JR, Siebert, BD, Gulati, SK, Cuthbertson, AZ & Scott, TW (1992) Incorporation of n-3 fatty acids of fish oil into tissue and serum lipids. Lipids 27, 629–631.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists (1995) Official Methods of Analysis, 16th ed., Arlington, VA: AOAC.Google Scholar
Astrup, HN, Mills, SC, Cook, LJ 7 Scott, TW (1974) Stability of α-tocopherol in rumen liquor of sheep. Acta Vet Scand 15, 451–453.CrossRefGoogle Scholar
Bessa, RJB, Santos-Silva, J, Ribeiro, JMR & Portugal, AV (2000) Reticulo-rumen biohydrogenation and the enrichment of ruminant edible products with linoleic acid conjugated isomers. Livest Prod Sci 63, 201–211.CrossRefGoogle Scholar
Binnerts, WT, van't Klooster, ATh & Frens, AM (1968) Soluble chromium indicator by atomic absorption in digestion experiments. Vet Rec 82, 470.Google Scholar
Broudiscou, L, Pochet, S & Poncet, C (1994) Effect of linseed oil supplementation on feed degradation and microbial synthesis in the rumen of ciliate-free and refaunated sheep. Anim Feed Sci Technol 49, 189–202.CrossRefGoogle Scholar
Chalupa, W, Rickabaugh, B, Kronfeld, DS 7 Sklan, D (1984) Rumen fermentation in vitro as influenced by long chain fatty acids. J Dairy Sci 67, 1439–1444.CrossRefGoogle ScholarPubMed
Chilliard, Y, Ferlay, A & Doreau, M (2001) Effect of different types of forages, animal fat or marine oils in cow's diet on milk fat secretion and composition, especially conjugated linoleic acid (CLA) and polyunsaturated fatty acids. Livest Prod Sci 70, 31–48.CrossRefGoogle Scholar
Choi, NJ, Kim, EJ, Maeng, WJ, Neville, MA, Enser, M, Wood, JD & Scollan, ND (1997) Rumen biohydrogenation of fatty acids from different sources of fat. Proc Br Soc Anim Sci 1997, 19 Abstr.CrossRefGoogle Scholar
Chow, JM & Russell, JB (1992) Effect of pH and monensin on glucose transport by Fibrobacter succinogenes, a cellulolytic ruminal bacterium. Appl Environ Microbiol 58, 1115–1120.CrossRefGoogle ScholarPubMed
Cook, DA, McGilliard, AD & Richard, M (1967) In vitro conversion of long-chain fatty acids to ketones by bovine rumen mucosa. J Dairy Sci 51, 715–720.CrossRefGoogle Scholar
Demeyer, DI, Henderson, C & Prins, RA (1978) Relative significance of exogenous and de novo synthesised fatty acids in the formation of rumen microbial lipids in vitro. Appl Environ Microbiol 35, 24–31.CrossRefGoogle ScholarPubMed
Demeyer, DI & Van Nevel, CJ (1995) Transformations and effects of lipids in the rumen: Three decades of research at Ghent University. Arch Anim Nutr 48, 119–134.Google Scholar
Demirel, G, Wachira, A, Sinclair, LA, Wilkinson, RG, Wood, JD & Enser, M (2004) Effects of dietary n-3 polyunsaturated fatty acids, breed and dietary vitamin E on the fatty acids of lamb muscle, liver and adipose tissue. Br Nutr 91, 000–000.Google ScholarPubMed
Department of Health (1994) Nutritional Aspects of Cardiovascular Disease. Report on Health Social Subjects no. 46. London: H. M. Stationery Office.Google Scholar
Doreau, M & Chilliard, Y (1997a) Digestion and metabolism of dietary fat in farm animals. Br J Nutr 78, S15–S35.CrossRefGoogle ScholarPubMed
Doreau, M & Chilliard, Y (1997 b) Effects of ruminal or post-ruminal fish oil supplementation on intake and digestion in dairy cows. Reprod Nutr Dev 37, 113–124.CrossRefGoogle ScholarPubMed
Doreau, M & Ferlay, A (1994) Digestion and utilisation of fatty acids by ruminants. Anim Feed Sci Technol 45, 379–396.CrossRefGoogle Scholar
Enser, M, Demirel, G, Wood, JD, Nute, GR, Wachira, AM, Sinclair, LA & Wilkinson, RG (1999a) Impaired deposition of vitamin E in lambs of two breeds fed a dry pelleted complete diet and its effects on meat quality. Proc Br Soc Anim Sci 1999, 40 Abstr.CrossRefGoogle Scholar
Enser, M, Hallett, K, Hewitt, B, Fursey, GAJ & Wood, JD (1996) Fatty acids content and composition of English beef, lamb and pork at retail. J Meat Sci 42, 443–456.CrossRefGoogle Scholar
Enser, M, Scollan, ND, Choi, NJ, Kurt, E, Hallet, K & Wood, JD (1999 b) Effect of dietary lipid on the content of conjugated linoleic acid (CLA) in beef muscle. Anim Sci 69, 143–146.CrossRefGoogle Scholar
Faichney, GJ (1975) The use of markers to partition digestion within the gastro-intestinal tract of ruminants. In Digestion Metabolism in the Ruminant. Proceedings of the IV International Symposium on Ruminant Physiology, pp.277–291 [McDonald, IW and, Warner, ACI, editors]. Armidale, New South Wales: The University of New England Publishing Unit.Google Scholar
Fievez, VI, Van Nevel, CJ & Demeyer, DI (2000) Lipolysis and biohydrogenation of PUFAs from fish oil during in vitro incubations with rumen contents. Proc Nutr Soc 59, 193A.Google Scholar
Firkins, JL, Weiss, WP & Piwonka, EJ (1992) Quantification of intra-ruminal recycling of microbial nitrogen using nitrogen-15. J Anim Sci 70, 3223–3233.CrossRefGoogle Scholar
Griinari, JM, Corl, BA, Lacy, SH, Chouinard, PY, Nurmela, KVV & Bauman, DE (2000) Conjugated linoleic acid is synthesised endogenously in lactating dairy cows by Δ9-desaturase. J Nutr 130, 2285–2291.CrossRefGoogle Scholar
Harfoot, CG 7 Hazzlewood, GP (1997) Lipid metabolism in the rumen. In The Rumen Microbial Ecosystem, pp. 383–426 [Hobson, PN and Stewart, CS, editors]. London: Chapman and Hall.Google Scholar
Harfoot, CG, Noble, RC & Moore, JH (1973) Food particles as a site for biohydrogenation of unsaturated fatty acids in the rumen. Biochem J 132, 829–832.CrossRefGoogle ScholarPubMed
Hidiroglou, N, Cave, N, Atwal, AS, Farnworth, ER & McDowell, LR (1992) Comparative vitamin E requirements and metabolism in livestock. Ann Rech Vet 23, 337–359.Google ScholarPubMed
Hidoroglou, M & Charmley, E (1990) Response of plasma and tissue d -α-tocopherol in sheep to graded dietary levels of dl -α-tocopheryl acetate. Res Vet Sci 49, 122–124.CrossRefGoogle Scholar
Hidiroglou, M & Jenkins, KL (1974) Fate of radiotocopherol adminstered into the gastric system of sheep. Ann Biol Anim Biochim Biophys 14, 667–677.CrossRefGoogle Scholar
Hino, T 7 Nagatake, Y (1993) The effect of grass lipids on fibre digestion by mixed rumen micro-organisms in vitro. Anim Sci Technol 64, 121–128.Google Scholar
Hird, FJR, Jackson, RB & Weidemann, MJ (1966) Transport and metabolism of fatty acids by isolated rumen epithelium. Biochem J 98, 394–400.CrossRefGoogle ScholarPubMed
Hoover, WH (1986) Chemical factors involved in fibre digestion. J Dairy Sci 69, 2755–2766.CrossRefGoogle Scholar
Ikwuegbu, OA & Sutton, JD (1982) The effect of varying the amount of linseed oil supplementation on rumen metabolism in sheep. Br J Nutr 48, 365–375.CrossRefGoogle ScholarPubMed
Jenkins, TC (1993) Lipid metabolism in the rumen. J Dairy Sci 76, 3851–3863.CrossRefGoogle ScholarPubMed
Kasapidou, E, Wood, JD, Sinclair, LA, Wilkinson, RG & Enser, M (2001) Vitamin E supplementation and meat quality in lambs. Proc Br Soc Anim Sci 2001. 56 Abstr.CrossRefGoogle Scholar
Leedle, RA, Leedle, JAZ & Butine, MD (1993) Vitamin E is not degraded by ruminal micro-organisms: Assessment with ruminal contents from a steer fed a high concentrate diet. J Anim Sci 71, 3442–3450.CrossRefGoogle ScholarPubMed
Mathers, JC & Miller, EL (1980) A simple procedure using 35 S incorporation for the measurement of microbial and undegraded food protein in ruminant digesta. Br J Nutr 43, 503–514.CrossRefGoogle Scholar
Moore, JH & Christie, WW (1984) Digestion, absorption and transport of fats in ruminant animals. In Fats in Animal Nutrition, pp. 123–149 [Wiseman, J, editor]. London: Butterworth.CrossRefGoogle Scholar
Mosley, EE, Powell, GL, Riley, MB & Jenkins, TC (2002) Microbial biohydrogenation of oleic acid to trans isomers in vitro. J Lipid Res 43, 290–296.CrossRefGoogle ScholarPubMed
Murray, CH & Rice, DA (1982) Vitamin E and selenium deficiency diseases. Ir Vet J 36, 57–67.Google Scholar
Newbold, CJ, Williams, AG & Chamberlain, DG (1987) The in vitro metabolism of D, l -lactic acid by rumen micro-organisms. J Sci Food Agric 38, 9–19.CrossRefGoogle Scholar
Nicholson, JWG & Sutton, JD (1971) Some effects of unsaturated oils given to dairy cows with rations of different roughage content. J Dairy Res 38, 363–372.CrossRefGoogle ScholarPubMed
Offer, NW, Marsden, M, Dixon, J, Speake, BK & Thacker, FE (1999) Effect of dietary fat supplements on levels of n-3 poly-unsaturated fatty acids, trans acids and conjugated linoleic acid in bovine milk. Anim Sci 69, 613–625.CrossRefGoogle Scholar
Palmquist, DL 7 Kinsey, DJ (1994) Lipolysis and biohydrogenation of fish oil by ruminal micro-organisms. J Anim Sci 72 Suppl. 1, 350 Abstr.Google Scholar
Pocklington, WD & Dieffenbacher, A (1988) Determination of tocopherols and tocotrienals in vegetable oils and fats by high performance liquid chromatography: results of a collaborative study and the standardised method. Pure Appl Chem 60, 877–892.CrossRefGoogle Scholar
Putnam, ME & Comben, N (1987) Vitamin E. Vet Rec 121, 541–545.Google ScholarPubMed
Raes, K, Ansorena, D, Chow, TT, Fievez, V, Demeyer, D & De Smet, S (2001) Introduction of n-3 fatty acids and conjugated linoleic acid into the intramuscular fat of Belgian Blue double-muscled bulls. In Proceedings of the 47th International Congress of Meat Science Technology, pp. 114–115. Savoy, IL, USA: American Meat Science Association.Google Scholar
Rule, DC, Wu, WH, Busboom, JR, Hinds, FC & Kercher, CJ (1989) Dietary canola seeds alter fatty acid composition of bovine subcutaneous adipose tissue. Nutr Rep Int 39, 781–786.Google Scholar
Russell, JB & Wilson, DB (1996) Why are ruminal cellulolytic bacteria unable to digest cellulose at low pH? J Dairy Sci 79, 1503–1509.CrossRefGoogle ScholarPubMed
Santora, JE, Palmquist, DL & Roehrig, KL (2000) Trans-vaccenic acid is desaturated to conjugated linolenic acid in mice. J Nutr 130, 208–215.CrossRefGoogle Scholar
Scott, TW, Cook, LJ & Mills, SC (1971) Protection of dietary polyunsaturated fatty acids against microbial hydrogenation in ruminants. J Am Oil Chem Soc 48, 358–364.CrossRefGoogle Scholar
Shi, Y & Weimer, PJ (1992) Response surface analysis of the effects of pH and dilution rate on Ruminococcus flavefaciens FD-1 in cellulose fed continuous culture. Appl Environ Microbiol 58, 2583–2591.CrossRefGoogle ScholarPubMed
Shin, IS & Owens, FN (1990) Ruminal and intestinal disappearance of several sources of vitamin E. J Anim Sci 68, Suppl.1, 544 Abstr.Google Scholar
Siddons, RC, Paradine, J, Beever, DE & Cornell, PR (1985) Ytterbium acetate as a particulate-phase digesta-flow marker. Br J Nutr 54, 509–519.CrossRefGoogle ScholarPubMed
Van Soest, PJ, Robertson, JB & Lewis, BA (1991) Methods for dietary fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74, 3025–3034.CrossRefGoogle ScholarPubMed
Wachira, AM, Sinclair, LA, Wilkinson, RG, Enser, M, Wood, JD & Fisher, AV (2002) Effects of dietary fat source and breed on the carcass composition, n-3 polyunsaturated fatty acid and conjugated linoleic acid content of sheep meat and adipose tissue. Br J Nutr 88, 697–709.CrossRefGoogle ScholarPubMed
Wachira, AM, Sinclair, LA, Wilkinson, RG, Hallett, K, Enser, M & Wood, JD (2000) Rumen biohydrogenation of n-3 polyunsaturated fatty acids and their effects on microbial efficiency and nutrient digestibility in sheep. J Agric Sci Camb 135, 419–428.CrossRefGoogle Scholar
Weimer, PJ (1993) Effects of dilution rate and pH on the ruminal cellulolytic bacterium Fibrobacter succinogens S85 in the cellulose fed continuous culture. Arch Microbiol 160, 288–294.CrossRefGoogle ScholarPubMed
Wonsil, BJ, Herbein, JH & Watkins, BA (1994) Dietary and ruminally derived trans-18:1 fatty acids alter bovine milk lipids. J Nutr 79, 62–68.Google Scholar
Wood, JD & Enser, MB (1997) Factors influencing fatty acids in meat and the role of antioxidants in improving meat quality. Br J Nutr 78, Suppl. 1, S49–S60.CrossRefGoogle ScholarPubMed
Wu, Z, Ohajuruka, OA & Palmiquist, DL (1991) Ruminal synthesis, biohydrogenation and digestibility of fatty acids by dairy cows. J Dairy Sci 74, 3025–3034.CrossRefGoogle ScholarPubMed
Wulf, DM, Morgan, JB, Sanders, SK, Tatum, JD, Smith, GC & Williams, S (1995) Effects of dietary supplementation of vitamin E on storage and case life properties of lamb retail cuts. J Anim Sci 73, 399–405.CrossRefGoogle Scholar
Zinn, RA & Owens, FN (1986) A rapid procedure for purine measurement and its use for estimating for net ruminal protein synthesis. Can J Anim Sci 66, 157–166.CrossRefGoogle Scholar