Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T15:35:12.231Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of fish oil on ruminal biohydrogenation of C18 unsaturated fatty acids

Published online by Cambridge University Press:  08 March 2007

I. Wąsowska ,
M. R. G. Maia ,
K. M. Niedźwiedzka ,
M. Czauderna ,
J. M. C. Ramalho Ribeiro ,
E. Devillard ,
K. J. Shingfield  and
R. J. Wallace
I. Wąsowska
Affiliation:
Rowett Research InstituteGreenburn RoadBucksburnAberdeen AB21 9SBUK Kielanowski Institute of Animal Physiology and NutritionPolish Academy of Sciences05-110 JablonnaPoland
M. R. G. Maia
Affiliation:
Rowett Research InstituteGreenburn RoadBucksburnAberdeen AB21 9SBUK Estaça˜o Zootécnica NacionalFonte Boa2005-048 Vale de SantarémPortugal
K. M. Niedźwiedzka
Affiliation:
Rowett Research InstituteGreenburn RoadBucksburnAberdeen AB21 9SBUK Kielanowski Institute of Animal Physiology and NutritionPolish Academy of Sciences05-110 JablonnaPoland
M. Czauderna
Affiliation:
Kielanowski Institute of Animal Physiology and NutritionPolish Academy of Sciences05-110 JablonnaPoland
J. M. C. Ramalho Ribeiro
Affiliation:
Estaça˜o Zootécnica NacionalFonte Boa2005-048 Vale de SantarémPortugal
E. Devillard
Affiliation:
Rowett Research InstituteGreenburn RoadBucksburnAberdeen AB21 9SBUK
K. J. Shingfield
Affiliation:
Animal Production ResearchMTT Agrifood Research Finland31600JokioinenFinland
R. J. Wallace*
Affiliation:
Rowett Research InstituteGreenburn RoadBucksburnAberdeen AB21 9SBUK
*
*Corresponding author: Dr R. John Wallace, fax +44 1224 716687, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Dietary cis-9, trans-11-conjugated linoleic acid (CLA) is generally thought to be beneficial for human health. Fish oil added to ruminant diets increases the CLA concentration of milk and meat, an increase thought to arise from alterations in ruminal biohydrogenation of unsaturated fatty acids. To investigate the mechanism for this effect, in vitro incubations were carried out with ruminal digesta and the main biohydrogenating ruminal bacterium, Butyrivibrio fibrisolvens. Linoleic acid (LA) or α-linolenic acid (LNA) was incubated (1·67g/l) with strained ruminal digesta from sheep receiving a 50:50 grass hay–concentrate ration. Adding fish oil (up to 4·17g/l) tended to decrease the initial rate of LA (P=0·025) and LNA (P=0·137) disappearance, decreased (P<0·05) the transient accumulation of conjugated isomers of both fatty acids, and increased (P<0·05) the accumulation of trans-11-18:1. Concentrations of EPA (20:5 n-3) or DHA (22:6 n-3), the major fatty acids in fish oil, were low (100mg/l or less) after incubation of fish oil with ruminal digesta. Addition of EPA or DHA (50mg/l) to pure cultures inhibited the growth and isomerase activity of B. fibrisolvens, while fish oil had no effect. In contrast, similar concentrations of EPA and DHA had no effect on biohydrogenation of LA by mixed digesta, while the addition of LA prevented metabolism of EPA and DHA. Neither EPA nor DHA was metabolised by B. fibrisolvens in pure culture. Thus, fish oil inhibits ruminal biohydrogenation by a mechanism which can be interpreted partly, but not entirely, in terms of its effects on B. fibrisolvens.

Keywords

BiohydrogenationConjugated linoleic acidFish oilTrans fatty acids
Type
Research Article
Information
British Journal of Nutrition , Volume 95 , Issue 6 , June 2006 , pp. 1199 - 1211
Copyright
Copyright © The Nutrition Society 2006

References

AbuGhazaleh, AA & Jenkins, TCDisappearance of docosahexaenoic and eicosapentaenoic acids from cultures of mixed ruminal microorganisms. J Dairy Sci 2004a 87, 645–651.CrossRefGoogle ScholarPubMed
AbuGhazaleh, AA & Jenkins, TCShort communication: Docosahexaenoic acid promotes vaccenic acid accumulation in mixed ruminal cultures when incubated with linoleic acid. J Dairy Sci 2004b 87, 1047–1050..CrossRefGoogle ScholarPubMed
Beam, TM, Jenkins, TC, Moate, PJ, Kohn, RA, Palmquist, DLEffects of amount and source of fat on the rates of lipolysis and biohydrogenation of fatty acids in ruminal contents. J Dairy Sci 2000 83, 2564–2573.CrossRefGoogle ScholarPubMed
Chaudhary, LC, McKain, N, Richardson, AJ, Barbier, M, Charbonnier, J & Wallace, RJScreening for Fusocillus: factors that affect the detection of ruminal bacteria which form stearic acid from linoleic acid. Repr Nutr Develop 44 Suppl. 2004 1, S65.Google Scholar
Chow, TT, Fievez, V, Moloney, AP, Raes, K, Demeyer, D & De Smet, SEffect of fish oil on in vitro rumen lipolysis, apparent biohydrogenation of linoleic and linolenic acids and accumulation of biohydrogenation intermediates. Anim Feed Sci Technol 2004 117, 1–12.CrossRefGoogle Scholar
Christie, WWGas chromatography-mass spectrometry methods for structural analysis of fatty acids. Lipids 1998 33, 343–353.CrossRefGoogle ScholarPubMed
Christie, WWLipid analysis. Isolation, separation, identifi-cation and structural analysis of lipids. Bridgwater, UK:. The Oily Press. 2003.Google Scholar
Dohme, F, Fievez, V, Raes, K & Demeyer, DIIncreasing levels of two different fish oils lower ruminal biohydrogenation of eicosapentaenoic and docosahexaenoic acid in vitro. Anim Res 2003 52, 309–320.CrossRefGoogle Scholar
Donovan, DC, Schingoethe, DJ, Baer, RJ, Ryali, J, Hippen, AR & Franklin, STInfluence of dietary fish oil on conjugated linoleic acid and other fatty acids in milk fat from lactating dairy cows. J Dairy Sci 2000 83, 2620–2628.CrossRefGoogle ScholarPubMed
Fay, L, Richli, ULocation of double bonds in polyunsaturated fatty acids by gas chromatography-mass spectrometry after 4,4-dimethyloxazoline derivatization. J Chromatog 1991 541, 89–98.CrossRefGoogle Scholar
Fellner, V, Sauer, FD & Kramer, JKSteady-state rates of linoleic acid biohydrogenation by ruminal bacteria in continuous culture. J Dairy Sci 1995 78, 1815–1823.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GHA simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957 226, 497–509.CrossRefGoogle ScholarPubMed
Fujimoto, K, Kimoto, H, Shishikura, M, Endo, Y & Ogimoto, KBiohydrogenation of linoleic acid by anaerobic bacteria isolated from the rumen. Biosci Biotech Biochem 1993 57, 1026–1027.CrossRefGoogle Scholar
Givens, DI & Shingfield, KJFood derived from animals: the impact of animal nutrition on their nutritive value and ability to sustain long-term health. Nutr Bull 2004 29, 325–332.CrossRefGoogle Scholar
Griinari, JM, Corl, BA, Lacy, SH, Chouinard, PY, Nurmela, KV & Bauman, DEonjugated linoleic acid is synthesized endogenously in lactating dairy cows by delta(9)-desaturase. C. J NutrC. J Nutr 2000 130, 2285–2291.Google Scholar
Gulati, SK, Ashes, JR, Scott, TWHydrogenation of eicosapentaenoic and decahexaenoic acids and their incorporation into milk fat. Anim Feed Sci Technol 1999 79, 57–64.CrossRefGoogle Scholar
Harfoot, CGLipid metabolism in the rumen. In Lipid Metabolism in Ruminant Animals, pp (Christie, WWOxford:. Pergamon Press. 1981. 21–55.CrossRefGoogle Scholar
Harfoot, CG, Crouchman, ML, Noble, RC & Moore, JHCompetition between food particles and rumen bacteria in the uptake of long-chain fatty acids and triglycerides. J Appl Bacteriol 1974 37, 633–641.CrossRefGoogle ScholarPubMed
Harfoot, CG & Hazlewood, GPLipid metabolism in the rumen. In The Rumen Microbial Ecosystem, pp (Hobson, PN & CS, Stewart) London:. Chapman & Hall. 1997. 382–426.CrossRefGoogle Scholar
Herbert, D, Phipps, PJ & Strange, REChemical analysis of microbial cells. In Methods in Microbiology, vol 5B. pp (Norris, JR & Ribbons, DW) London:. Academic Press. 1971. 209–344.Google Scholar
Hobson, PNRumen bacteria. In Methods in Microbiology, vol.3B. (Norris, JR & Ribbons, DW) London:. Academic Press 1969. 133–149.Google Scholar
Kaluzny, MA, Duncan, LA, Merritt, MV & Epps, DERapid separation of lipid classes in high yield and purity using bonded phase columns. J Lipid Res 1985 26, 135–140.CrossRefGoogle ScholarPubMed
Kepler, CR, Tove, SBBiohydrogenation of unsaturated fatty acids. 3. Purification and properties of a linoleate delta-12-cis,- delta-11-trans-isomerase fromButyrivibrio fibrisolvens. J Biol Chem 1967 242, 5686–5692.CrossRefGoogle ScholarPubMed
Kepler, CR, Tucker, WP & Tove, SBBiohydrogenation of unsaturated fatty acids. IV. Substrate specificity and inhibition of linoleate delta-12-cis, delta-11-trans-isomerase from Butyrivibrio fibrisolvens. J Biol Chem 1970 245, 3612–3620.CrossRefGoogle ScholarPubMed
Kritchevsky, DAntimutagenic and some other effects of conjugated linoleic acid. Br J Nutr 2000 83, 459–465.CrossRefGoogle ScholarPubMed
Lawson, RE, Moss, AR, Givens, DIThe role of dairy products in supplying conjugated linoleic acid to man's diet: a review. Nutr Res Rev 2001 14, 153–172.CrossRefGoogle ScholarPubMed
Lee, MRF, Tweed, JKS, Moloney, AP & Scollan, NDThe effects of fish oil supplementation on rumen metabolism and the biohydrogenation of unsaturated fatty acids in beef steers given diets containing sunflower oil. Anim Sci 2005 80, 361–367.CrossRefGoogle Scholar
Legay-Carmier, F, Bauchart, D & Doreau, MDistribution of bacteria in the rumen contents of dairy cows given a diet supplemented with soyabean oil. Br J Nutr 1989 61, 725–740.CrossRefGoogle Scholar
Loor, JJ, Ueda, K, Ferlay, A, Chilliard, Y & Doreau, MIntestinal flow and digestibility of trans fatty acids and conjugated linoleic acids (CLA) in dairy cows fed a high-concentrate diet supplemented with fish oil, linseed oil, or sunflower oil. Anim Feed Sci Technol 2005 119, 203–225.CrossRefGoogle Scholar
McKain, N, Chaudhary, LC, Walker, ND, Pizette, F, Koppova, I, McEwan, NR, Kopecny, J, Vercoe, PE & Wallace, RJRelation between phylogenetic position and fatty acid metabolism of different Butyrivibrio isolates from the rumen. Repr Nutr Develop 44, Suppl 2004 1, S64.Google Scholar
Martin, SA & Jenkins, TCFactors affecting conjugated linoleic acid and trans-C18:1 fatty acid production by mixed ruminal bacteria. J Anim Sci 2002 80, 3347–3352.CrossRefGoogle ScholarPubMed
Noble, RC, Noble, JH, Harfoot, CGObservations on the pattern of biohydrogenation of esterified and unesterified linoleic acid in the rumen. Br J Nutr 1974 31, 99–108.CrossRefGoogle ScholarPubMed
Offer, NW, Marsden, M, Dixon, J, Speake, BK & Thacker, FEEffect of dietary fat supplements on levels of n-3 poly-unsaturated fatty acids, trans acids and conjugated linoleic acid in bovine milk. Anim Sci 1999 69, 613–625.CrossRefGoogle Scholar
Parodi, PWConjugated linoleic acid and other anticarcinogenic agents of bovine milk fat. J Dairy Sci 1999 82, 1339–1349.CrossRefGoogle ScholarPubMed
Polan, CE & McNeill, JJ, Tove, SBBiohydrogenation of unsaturated fatty acids by rumen bacteria. J Bacteriol 1964 88, 1056–1064.CrossRefGoogle ScholarPubMed
Scollan, ND, Choi, NJ, Kurt, E, Fisher, AV, Enser, M & Wood, JDManipulating the fatty acid composition of muscle and adipose tissue in beef cattle. Br J Nutr 2001a 85, 115–124.CrossRefGoogle ScholarPubMed
Scollan, ND, Dhanoa, MS, Choi, NJ, Maeng, WJ, Enser, M & Wood, JDBiohydrogenation and digestion of long chain fatty acids in steers fed on different sources of lipid. J Agric Sci (Camb) 2001b 136, 345–355.CrossRefGoogle Scholar
Shingfield, KJ, Ahvenjarvi, S, Toivonen, V, Arola, A, Nurmela, KVV, Huhtanen, P & Griinari, JMEffect of dietary fish oil on biohydrogenation of fatty acids and milk fatty acid content in cows. Anim Sci 2003 77, 165–179.CrossRefGoogle Scholar
Stewart, CS, Flint, HJ & Bryant, MPThe rumen bacteria. In The Rumen Microbial Ecosystem, pp (Hobson, PN & Stewart, CS) London:. Chapman & Hall. 1997. 10–72.CrossRefGoogle Scholar
Troegeler-Meynadier, A, Nicot, MC, Bayourthe, C, Moncoulon, R & Enjalbert, FEffects of pH and concentrations of linoleic and linolenic acids on extent and intermediates of ruminal biohydrogenation in vitro. J Dairy Sci 2003 86, 4054–4063.CrossRefGoogle ScholarPubMed
van, de, Vossenberg, JL & Joblin, KNBiohydrogenation of C18 unsaturated fatty acids to stearic acid by a strain of Butyrivibrio hungatei from the bovine rumen. Lett Appl Microbiol 2003 37, 424–428.Google Scholar
Wachira, AM, Sinclair, LA, Wilkinson, RG, Enser, M, Wood, JD & Fisher, AVEffects 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 2002 88, 697–709.CrossRefGoogle ScholarPubMed
Wachira, AM, Sinclair, LA, Wilkinson, RG, Hallett, K, Enser, M & Wood, JDRumen biohydrogenation of n-3 polyunsaturated fatty acids and their effects on microbial efficiency and nutrient digestibility in sheep. J Agric Sci (Camb) 135 2000, 419–428.CrossRefGoogle Scholar
Wallace, RJ, Brammall, MLThe role of different species of rumen bacteria in the hydrolysis of protein in the rumen. J Gen Microbiol 1985 131, 821–832.Google Scholar
Wąsowska, I, Maia, M, Czauderna, M, Ramalho-Ribeiro, JMC & Wallace, RJInhibition of ruminal biohydrogenation of linoleic acid by fish oil. Reprod Nutr Develop 44, Suppl 2004 1, S64–S65.Google Scholar
Wilde, PF & Dawson, RMCThe biohydrogenation of a-linolenic and oleic acid by rumen micro-organisms. Biochem J 1966 98, 469–475.CrossRefGoogle Scholar
Williams, CMDietary fatty acids and human health. Ann Zootech 2000 49, 165–180.CrossRefGoogle Scholar
Wonsil, BJ, Herbein, JH & Watkins, BADietary and ruminally derived trans-18:1 fatty acids alter bovine milk lipids. J Nutr 1994 124, 556–565.Google Scholar
Zoetendal, EG, Collier, CT, Koike, S, Mackie, RI & Gaskins, HRMolecular ecological analysis of the gastrointestinal microbiota: a review. J Nutr 2004 134, 465–472.CrossRefGoogle ScholarPubMed