Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Is ruminal trans-11-18:1 accumulation a prerequisite for trans-10-18:1 production?

B. Vlaeminck A , W. Khattab B and V. Fievez A C
+ Author Affiliations
- Author Affiliations

A Laboratory for Animal Nutrition and Animal Product Quality, Department of Animal Production, Faculty of Bioscience Engineering, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium.

B Department of Nutrition and Clinical Nutrition, Faculty of Veterinary Medicine, Benha University, Moshtohor, Tukh, Qalubia 13736, Egypt.

C Corresponding author. Email: veerle.fievez@ugent.be

Animal Production Science 55(2) 225-230 https://doi.org/10.1071/AN14331
Submitted: 13 March 2014  Accepted: 1 September 2014   Published: 18 December 2014

Abstract

Understanding ruminal biohydrogenation of linoleic and linolenic acid is important in relation to physiological responses in the animal and the fatty acid profile of ruminant meat and milk. Alterations in ruminal biohydrogenation pathways leading to an increased formation of trans-10-18:1 are known to occur with high-concentrate diets and marine supplements. We hypothesised that accumulation of trans-11-18:1 is a prerequisite for trans-10-18:1 production. To evaluate this hypothesis, a batch-culture method, using rumen fluid from wethers, was used which consisted of two periods. Period 1 (10 h) was used to induce changes in trans-11-18:1 accumulation using a 2 × 2 factorial design, with 18:2n-6 (0 vs 6.40 mg) and 22:6n-3 (0 vs 2.50 mg) replicated with three substrates (starch, glucose or cellobiose). As planned, the addition of 18:2n-6 in combination with 22:6n-3 resulted in greater accumulation of trans-11-18:1 than did the other treatments (2.73 ± 0.125 vs 0.37 ± 0.157 mg/flask). After P1, 18:2n-6 (3.20 mg) was added to all flasks and after 14 h of incubation, formation of trans-10-18:1 and trans-11-18:1 was evaluated. The apparent production of both trans-10-18:1 (0.057 vs 0.812 mg/flask) and trans-11-18:1 (–0.013 vs 1.100 mg/flask) for cultures receiving 22:6n-3 in P1 was greater independent of 18:2n-6 addition in P1 (P > 0.10). This lack of a significant interaction suggests that trans-11-18:1 accumulation was not a major factor explaining trans-10-18:1 production under the studied conditions.

Additional keywords: biohydrogenation, docosahexaenoic acid, in vitro, linoleic acid.


References

Boeckaert C, Vlaeminck B, Fievez V, Maignien L, Dijkstra J, Boon N (2008) Accumulation of trans C-18:1 fatty acids in the rumen after dietary algal supplementation is associated with changes in the Butyrivibrio community. Applied and Environmental Microbiology 74, 6923–6930.
Accumulation of trans C-18:1 fatty acids in the rumen after dietary algal supplementation is associated with changes in the Butyrivibrio community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVaru73J&md5=03ba11f4925a9c39c7c438aded8fa4d9CAS | 18820074PubMed |

Castro-Montoya J, De Campeneere S, Van Ranst G, Fievez V (2012) Interactions between methane mitigation additives and basal substrates on in vitro methane and VFA production. Animal Feed Science and Technology 176, 47–60.
Interactions between methane mitigation additives and basal substrates on in vitro methane and VFA production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyksbbO&md5=dfd49aa818f712aecf1545f1089f5c70CAS |

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, 828–855.
Diet, rumen biohydrogenation and nutritional quality of cow and goat milk fat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSnsrrO&md5=236361d5f8df4b239ea3a129c8cf0282CAS |

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, 740–756.
Assessing rumen biohydrogenation and its manipulation in vivo, in vitro and in situ.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSnsr3J&md5=550c4472a203d50bff61363258cdba2eCAS |

Fuentes MC, Calsamiglia S, Cardozo PW, Vlaeminck B (2009) Effect of pH and level of concentrate in the diet on the production of biohydrogenation intermediates in a dual-flow continuous culture. Journal of Dairy Science 92, 4456–4466.
Effect of pH and level of concentrate in the diet on the production of biohydrogenation intermediates in a dual-flow continuous culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKqtr%2FK&md5=fd1e1a79151a6ae87116799b6620a476CAS | 19700707PubMed |

Fuentes MC, Calsamiglia S, Fievez V, Blanch M, Mercadal D (2011) Effect of pH on ruminal fermentation and biohydrogenation of diets rich in omega-3 or omega-6 fatty acids in continuous culture of ruminal fluid. Animal Feed Science and Technology 169, 35–45.
Effect of pH on ruminal fermentation and biohydrogenation of diets rich in omega-3 or omega-6 fatty acids in continuous culture of ruminal fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFeku7%2FL&md5=dc3f94caf3458cf8ffa9aa29c2aa1489CAS |

Harfoot C, Noble R, Moore J (1973) Factors influencing the extent of biohydrogenation of linoleic acid by rumen micro-organisms in vitro. Journal of the Science of Food and Agriculture 24, 961–970.
Factors influencing the extent of biohydrogenation of linoleic acid by rumen micro-organisms in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXltVamt7k%3D&md5=e6a69fae08f8e0cbd9cd0d7429173408CAS | 4731354PubMed |

Jenkins TC, Wallace RJ, Moate PJ, Mosley EE (2008) Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. Journal of Animal Science 86, 397–412.
Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVajsL4%3D&md5=bf642c0ab50729b802647a7f235d3108CAS | 18042812PubMed |

Kepler CR, Tove SB (1967) Biohydrogenation of unsaturated fatty acids III. Purification and properties of a linoleate Δ12-cis, Δ11-trans-isomerase from Butyrivibrio fibrisolvens. The Journal of Biological Chemistry 242, 5686–5692.

Kepler CR, Hirons KP, McNeill JJ, Tove SB (1966) Intermediates and products of the biohydrogenation of linoleic acid by Butyrivibrio fibrisolvens. The Journal of Biological Chemistry 241, 1350–1354.

Kepler CR, Tucker WP, Tove SB (1970) Biohydrogenation of unsaturated fatty acids IV. Substrate specificity and inhibition of linoleate Δ12-cis, Δ11-trans-isomerase from Butyrivibrio fibrisolvens. The Journal of Biological Chemistry 245, 3612–3620.

Kim YJ, Liu RH, Rychlik JL, Russell JB (2002) The enrichment of a ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10, cis-12 isomer of conjugated linoleic acid. Journal of Applied Microbiology 92, 976–982.
The enrichment of a ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10, cis-12 isomer of conjugated linoleic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksVSrsbY%3D&md5=644e4ab70d8e7a354b3eaecedf362a94CAS | 11972704PubMed |

Klein CM, Thurmond SK, Morris PH, Jenkins TC (2011) Hourly changes in fatty acid profile of ruminal contents in continuous cultures as soybean oil is added and removed from the diet. Journal of Dairy Science E-Supplement 1, 136

Liavonchanka A, Hornung E, Feussner I, Rudolph MG (2006) Structure and mechanism of the Propionibacterium acnes polyunsaturated fatty acid isomerase. Proceedings of the National Academy of Sciences, USA 103, 2576–2581.
Structure and mechanism of the Propionibacterium acnes polyunsaturated fatty acid isomerase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksF2rsLo%3D&md5=fc5e9144ab644410f7b578e6ded6b4a1CAS |

Lourenço M, Ramos-Morales E, Wallace RJ (2010) The role of microbes in rumen lipolysis and biohydrogenation and their manipulation. Animal 4, 1008–1023.
The role of microbes in rumen lipolysis and biohydrogenation and their manipulation.Crossref | GoogleScholarGoogle Scholar | 22444606PubMed |

Maia MR, Chaudhary LC, Figueres L, Wallace RJ (2007) Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen. Antonie van Leeuwenhoek 91, 303–314.
Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslWgtrc%3D&md5=1cfa6af436abf677ca869143843e1f7eCAS | 17072533PubMed |

Maia MR, Bessa RJ, Wallace RJ (2009) Is the trans-10 shift that sometimes occurs in the ruminal biohydrogenation of linoleic acid caused by low pH or starch? A Rusitec study. In ‘XIth international symposium on ruminant physiology, Clermont-Ferrand, France’. (Eds Y Chilliard, F Glasser, Y Faulconnier, F Bocquier, I Veissier, M Doreau) pp. 276–277. (Wageningen Academic Publishers: Wageningen, The Netherlands)

McIntosh FM, Shingfield KJ, Devillard E, Russell WR, Wallace RJ (2009) Mechanism of conjugated linoleic acid and vaccenic acid formation in human faecal suspensions and pure cultures of intestinal bacteria. Microbiology-SGM 155, 285–294.
Mechanism of conjugated linoleic acid and vaccenic acid formation in human faecal suspensions and pure cultures of intestinal bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12rtbs%3D&md5=dbe9cf80879a3bd097b24e0f5ed93e88CAS |

McKain N, Shingfield KJ, Wallace RJ (2010) Metabolism of conjugated linoleic acids and 18:1 fatty acids by ruminal bacteria: products and mechanisms. Microbiology-SGM 156, 579–588.
Metabolism of conjugated linoleic acids and 18:1 fatty acids by ruminal bacteria: products and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivVSlsbk%3D&md5=987f30713843c9b89ff0abff04687c59CAS |

Moate PJ, Boston RC, Jenkins TC, Lean IJ (2008) Kinetics of ruminal lipolysis of triacylglycerol and biohydrogenation of long-chain fatty acids: new insights from old data. Journal of Dairy Science 91, 731–742.
Kinetics of ruminal lipolysis of triacylglycerol and biohydrogenation of long-chain fatty acids: new insights from old data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVait74%3D&md5=590d21fe383a3c24216cbf873d3154fcCAS | 18218761PubMed |

Morgavi DP, Boudra H, Jouany JP, Michalet-Doreau B (2004) Effect and stability of gliotoxin, an Aspergillus fumigates toxin, on in vitro rumen fermentation. Food Additives and Contaminants 21, 871–878.
Effect and stability of gliotoxin, an Aspergillus fumigates toxin, on in vitro rumen fermentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWiurvI&md5=2f820481194edcb3245d4bfdbcde1fa9CAS | 15666981PubMed |

Mould FL, Morgan R, Kliem KE, Krystallidou E (2005) A review and simplification of the in vitro incubation medium. Animal Feed Science and Technology 123–124, 155–172.
A review and simplification of the in vitro incubation medium.Crossref | GoogleScholarGoogle Scholar |

Noble RC, Moore JH, Harfoot CG (1974) Observations on the pattern on biohydrogenation of esterified and unesterified linoleic acid in the rumen. The British Journal of Nutrition 31, 99–108.
Observations on the pattern on biohydrogenation of esterified and unesterified linoleic acid in the rumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXmvFKjtQ%3D%3D&md5=c635fa23d505eb1e535860db06f81cb3CAS | 4810360PubMed |

Shingfield KJ, Griinari JM (2007) Role of biohydrogenation intermediates in milk fat depression. European Journal of Lipid Science and Technology 109, 799–816.
Role of biohydrogenation intermediates in milk fat depression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSnsrrM&md5=fcd713bca0b87fca118a9c8a14b9b00aCAS |

Shingfield KJ, Reynolds CK, Hervas G, Griinari JM, Grandison AS, Beever DE (2006) Examination of the persistency of milk fatty acid composition responses to fish oil and sunflower oil in the diet of dairy cows. Journal of Dairy Science 89, 714–732.
Examination of the persistency of milk fatty acid composition responses to fish oil and sunflower oil in the diet of dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWrtLo%3D&md5=1e120641531f589edc8a6478b702e02aCAS | 16428640PubMed |

Shingfield KJ, Kairenius P, Arola A, Paillard D, Muetzel S, Ahvenjarvi S, Vanhatalo A, Huhtanen P, Toivonen V, Griinari JM, Wallace RJ (2012) Dietary fish oil supplements modify ruminal biohydrogenation, alter the flow of fatty acids at the omasum, and induce changes in the ruminal Butyrivibrio population in lactating cows. The Journal of Nutrition 142, 1437–1448.
Dietary fish oil supplements modify ruminal biohydrogenation, alter the flow of fatty acids at the omasum, and induce changes in the ruminal Butyrivibrio population in lactating cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFajsLrI&md5=7d19ad3f03d7061431c3f23982a03a00CAS | 22739367PubMed |

Vlaeminck B, Mengistu G, Fievez V, de Jonge L, Dijkstra J (2008) Effect of in vitro docosahexaenoic acid supplementation to marine algae-adapted and unadapted rumen inoculum on the biohydrogenation of unsaturated fatty acids in freeze-dried grass. Journal of Dairy Science 91, 1122–1132.
Effect of in vitro docosahexaenoic acid supplementation to marine algae-adapted and unadapted rumen inoculum on the biohydrogenation of unsaturated fatty acids in freeze-dried grass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivFemtLk%3D&md5=86cfc1b5773d0649805c3aece2660940CAS | 18292268PubMed |

Vlaeminck B, Braeckman T, Fievez V (2014) Rumen metabolism of 22:6n-3 in vitro is dependent on its concentration and inoculum size, but less dependent on substrate carbohydrate composition. Lipids 49, 517–525.
Rumen metabolism of 22:6n-3 in vitro is dependent on its concentration and inoculum size, but less dependent on substrate carbohydrate composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVKgur4%3D&md5=69abe4cedc30a58500100994890ab16fCAS | 24748509PubMed |

Wąsowska I, Maia MRG, Niedzwiedzka KM, Czauderna M, Ribeiro JMCR, Devillard E, Shingfield KJ, Wallace RJ (2006) Influence of fish oil on ruminal biohydrogenation of C18 unsaturated fatty acids. The British Journal of Nutrition 95, 1199–1211.
Influence of fish oil on ruminal biohydrogenation of C18 unsaturated fatty acids.Crossref | GoogleScholarGoogle Scholar | 16768845PubMed |

Zened A, Troegeler-Meynadier A, Nicot MC, Combes S, Cauquil L, Farizon Y, Enjalbert F (2011) Starch and oil in the donor cow diet and starch in substrate differently affect the in vitro ruminal biohydrogenation of linoleic and linolenic acids. Journal of Dairy Science 94, 5634–5645.
Starch and oil in the donor cow diet and starch in substrate differently affect the in vitro ruminal biohydrogenation of linoleic and linolenic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2qsLvN&md5=09b62579deba3ec1c5f439e5a291b8b3CAS | 22032386PubMed |

Zened A, Enjalbert F, Nicot MC, Troegeler-Meynadier A (2013) Starch plus sunflower oil addition to the diet of dry dairy cows results in a trans-11 to trans-10 shift of biohydrogenation. Journal of Dairy Science 96, 451–459.
Starch plus sunflower oil addition to the diet of dry dairy cows results in a trans-11 to trans-10 shift of biohydrogenation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2rt77P&md5=bfa5953bfa7b48c39f938bd227918e87CAS | 23127910PubMed |