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RESEARCH ARTICLE (Open Access)

Assessment of atherogenic index, long-chain omega-3 fatty acid and phospholipid content of prime beef: a survey of commercially sourced New Zealand Wagyu and Angus beef cattle

Emma N. Bermingham https://orcid.org/0000-0003-0952-5260 A B H , Michael Agnew C , Mariza Gomes Reis C , Kevin Taukiri A , Arjan Jonker D , David Cameron-Smith B E F G and Cameron R. Craigie A
+ Author Affiliations
- Author Affiliations

A Meat Quality Team, AgResearch Ltd, Te Ohu Rangahau Kai, Cnr University Ave and Riddet Road, Massey University, Palmerston North, New Zealand.

B High-Value Nutrition National Science Challenge, The University of Auckland, 85 Park Road, Grafton, Private Bag 92019, Auckland 1023, New Zealand.

C Dairy Foods Team AgResearch Ltd, Te Ohu Rangahau Kai, Cnr University Ave and Riddet Road, Massey University, Palmerston North, New Zealand.

D Animal Nutrition & Physiology Team, AgResearch Ltd, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand.

E Liggins Institute, The University of Auckland, 85 Park Road, Grafton, Private Bag 92019, Auckland 1023, New Zealand.

F Riddet Institute, Massey University, Private Bag Palmerston North, New Zealand.

G Singapore Institute for Clinical Sciences, Agency for Science, Technology and Research (A*STAR), Brenner Centre for Molecular Medicine, 30 Medical Drive, 117609, Singapore.

H Corresponding author. Email: emma.bermingham@agresearch.co.nz

Animal Production Science 61(2) 179-190 https://doi.org/10.1071/AN19427
Submitted: 5 August 2019  Accepted: 24 August 2020   Published: 30 September 2020

Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND

Abstract

Context: There is increasing interest in the composition of lipids in beef from pasture-fed Wagyu-cross cattle and how they compare to beef from traditional beef breeds.

Aim: The present study aimed to investigate the differences in fatty acid and phospholipid content of the ribeye, striploin and tenderloin obtained from commercially sourced beef.

Hypothesis: We hypothesised that long-chain omega-3 fatty acid and phospholipid concentrations would be higher in Wagyu beef sourced from pasture-based production systems than in those sourced from grain-finished Wagyu.

Methods: Beef was either derived from commercial cattle exclusively fed pasture (Angus, Wagyu × Angus and Wagyu × Dairy (Friesian × Jersey); n = 10 per breed) or finished on grain (Angus and Wagyu; n = 10 per breed).

Key results: Phosphatidylcholine was the predominant phospholipid observed in beef surveyed, followed by phosphatidylethanolamine and sphingomyelin. All classes of phospholipid measured were affected by where the commercial beef was obtained, with the concentrations of total phospholipids being highest (P < 0.05) in the ribeye, striploin and tenderloin from pasture-fed beef compared with grain-fed beef. The fatty acid composition also varied among the commercial cuts; typically total saturated fatty acid and monounsaturated fatty acid concentrations were highest in beef finished on grain, whereas the concentrations of long-chain omega-3 fatty acids were two-fold higher (P < 0.05) in striploin and tenderloin derived from pasture-fed Wagyu × Dairy cross cattle than in those from grain-fed cattle. Despite different fatty acid concentrations among the commercial beef breeds surveyed, the calculated atherogenic index was similar for ribeye and striploin. In contrast, the tenderloin obtained from pasture-fed Wagyu × Dairy had the lowest (P = 0.017) atherogenic index.

Conclusions: Depending on the cut of meat studied, pasture-fed Wagyu × Angus and Wagyu × Dairy have different lipid compositions, including lipids that have been associated with both health benefits and risks in human.

Implications: These results show that a serving of meat obtained from non-traditional beef breeds such as pasture-fed Wagyu × Dairy may contribute significantly to the recommended daily intake of long-chain omega-3 fatty acids.

Keywords: docosahexaenoic acid (DHA), docosapentaenoic acid (DPA), eicosapentaenoic acid (EPA), phosphatidylcholine, phosphatidylethanolamine, phosphatidylinositol, phosphatidylserine, sphingomyelin.


References

Adams TH, Walzem RL, Smith DR, Tseng S, Smith SB (2010) Hamburger high in total, saturated and trans-fatty acids decreases HDL cholesterol and LDL particle diameter, and increases TAG, in mildly hypercholesterolaemic men. British Journal of Nutrition 103, 91–98.
Hamburger high in total, saturated and trans-fatty acids decreases HDL cholesterol and LDL particle diameter, and increases TAG, in mildly hypercholesterolaemic men.Crossref | GoogleScholarGoogle Scholar | 19674491PubMed |

Agostoni C, Moreno L, Shamir R (2016) Palmitic acid and health: introduction. Critical Reviews in Food Science and Nutrition 56, 1941–1942.
Palmitic acid and health: introduction.Crossref | GoogleScholarGoogle Scholar | 25764181PubMed |

Aus-Meat Limited (2010) ‘Australian beef carcase evaluation beef & veal chiller assessment language.’ Available at https://www.ausmeat.com.au/WebDocuments/Producer_HAP_Beef_Small.pdf [Verified 10 September 2020]

Bartke N, Hannun YA (2009) Bioactive sphingolipids: metabolism and function Journal of Lipid Research 50, S91–6.
Bioactive sphingolipids: metabolism and functionCrossref | GoogleScholarGoogle Scholar | 19017611PubMed |

Beef + Lamb NewZealand (2010) ‘Beef + lamb New Zealand reference guide.’ 3rd edn. (Beef + Lamb New Zealand: Takapuna, Auckland’ Available at http://www.beeflambnz.co.nz/retailer-resources/Reference_Guide.pdf [Verified 10 September 2020]

Bermingham EN, Reis MG, Subbaraj AK, Cameron-Smith D, Fraser K, Jonker A, Craigie CR (2018) Distribution of fatty acids and phospholipids in different table cuts and co-products from New Zealand pasture-fed Wagyu–dairy cross beef cattle. Meat Science 140, 26–37.
Distribution of fatty acids and phospholipids in different table cuts and co-products from New Zealand pasture-fed Wagyu–dairy cross beef cattle.Crossref | GoogleScholarGoogle Scholar | 29501930PubMed |

Bier DM (2016) Saturated fats and cardiovascular disease: interpretations not as simple as they once were. Critical Reviews in Food Science and Nutrition 56, 1943–1946.
Saturated fats and cardiovascular disease: interpretations not as simple as they once were.Crossref | GoogleScholarGoogle Scholar | 25774535PubMed |

Bouvard V, Loomis D, Guyton KZ, Grosse Y, Ghissassi FE, Benbrahim-Tallaa L, Guha N, Mattock H, Straif K (2015) Carcinogenicity of consumption of red and processed meat. The Lancet. Oncology 16, 1599–1600.
Carcinogenicity of consumption of red and processed meat.Crossref | GoogleScholarGoogle Scholar | 26514947PubMed |

Burgess JW, Neville TA-M, Rouillard P, Harder Z, Beanlands DS, Sparks DL (2005) Phosphatidylinositol increases HDL-C levels in humans. Journal of Lipid Research 46, 350–355.
Phosphatidylinositol increases HDL-C levels in humans.Crossref | GoogleScholarGoogle Scholar | 15576836PubMed |

Byelashov OA, Sinclair AJ, Kaur G (2015) Dietary sources, current intakes, and nutritional role of omega-3 docosapentaenoic acid. Lipid Technology 27, 79–82.
Dietary sources, current intakes, and nutritional role of omega-3 docosapentaenoic acid.Crossref | GoogleScholarGoogle Scholar | 26097290PubMed |

Coleman LW, Hickson RE, Schreurs NM, Martin NP, Kenyon PR, Lopez-Villalobos N, Morris ST (2016) Carcass characteristics and meat quality of Hereford sired steers born to beef-cross-dairy and Angus breeding cows. Meat Science 121, 403–408.
Carcass characteristics and meat quality of Hereford sired steers born to beef-cross-dairy and Angus breeding cows.Crossref | GoogleScholarGoogle Scholar | 27448194PubMed |

Craigie CR, Johnson PL, Shorten PR, Charteris A, Maclennan G, Tate ML, Agnew MP, Taukiri KR, Stuart AD, Reis MM (2017) Application of hyperspectral imaging to predict the pH, intramuscular fatty acid content and composition of lamb M. longissimus lumborum at 24h post mortem. Meat Science 132, 19–28.
Application of hyperspectral imaging to predict the pH, intramuscular fatty acid content and composition of lamb M. longissimus lumborum at 24h post mortem.Crossref | GoogleScholarGoogle Scholar | 28551294PubMed |

Cui L, Decker EA (2016) Phospholipids in foods: prooxidants or antioxidants? Journal of the Science of Food and Agriculture 96, 18–31.
Phospholipids in foods: prooxidants or antioxidants?Crossref | GoogleScholarGoogle Scholar | 26108454PubMed |

Daley C, Abbott A, Doyle P, Nader G, Larson S (2010) A review of fatty acid profiles and antioxidant content in grass-fed and grain-fed beef. Nutrition Journal 9, 10
A review of fatty acid profiles and antioxidant content in grass-fed and grain-fed beef.Crossref | GoogleScholarGoogle Scholar | 20219103PubMed |

Dannenberger D, Nuernberg G, Scollan N, Ender K, Nuernberg K (2007) Diet alters the fatty acid composition of individual phospholipid classes in beef muscle. Journal of Agricultural and Food Chemistry 55, 452–460.
Diet alters the fatty acid composition of individual phospholipid classes in beef muscle.Crossref | GoogleScholarGoogle Scholar | 17227079PubMed |

De Smet S, Vossen E (2016) Meat: the balance between nutrition and health. A review. Meat Science 120, 145–156.
Meat: the balance between nutrition and health. A review.Crossref | GoogleScholarGoogle Scholar | 27107745PubMed |

de Souza RJ, Mente A, Maroleanu A, Cozma AI, Ha V, Kishibe T, Uleryk E, Budylowski P, Schunemann H, Beyene J, Anand SS (2015) Intake of saturated and trans unsaturated fatty acids and risk of all cause mortality, cardiovascular disease, and type 2 diabetes: systematic review and meta-analysis of observational studies. British Medical Journal 351, h3978
Intake of saturated and trans unsaturated fatty acids and risk of all cause mortality, cardiovascular disease, and type 2 diabetes: systematic review and meta-analysis of observational studies.Crossref | GoogleScholarGoogle Scholar | 26268692PubMed |

Delgado GE, Kramer BK, Lorkowski S, Marz W, von Schacky C, Kleber ME (2017) Individual omega-9 monounsaturated fatty acids and mortality: the Ludwigshafen risk and cardiovascular health study. Journal of Clin Lipidology 11, 126–135.e5.
Individual omega-9 monounsaturated fatty acids and mortality: the Ludwigshafen risk and cardiovascular health study.Crossref | GoogleScholarGoogle Scholar |

Dinicola S, Minini M, Unfer V, Verna R, Cucina A, Bizzarri M (2017) Nutritional and acquired deficiencies in inositol bioavailability. Correlations with metabolic disorders International Journal of Molecular Sciences 18, 2187

Ebbesson SO, Voruganti VS, Higgins PB, Fabsitz RR, Ebbesson LO, Laston S, Harris WS, Kennish J, Umans BD, Wang H, Devereux RB, Okin PM, Weissman NJ, MacCluer JW, Umans JG, Howard BV (2015) Fatty acids linked to cardiovascular mortality are associated with risk factors. International Journal of Circumpolar Health 74, 28055
Fatty acids linked to cardiovascular mortality are associated with risk factors.Crossref | GoogleScholarGoogle Scholar | 26274054PubMed |

FSANZ (2016) ‘Food standards code from 1 March 2016: standard 1.2.7 – nutrition, health and related claims food standards Australia New Zealand.’ Available at https://www.foodstandards.govt.nz/code/Pages/default.aspx. [Verified 10 September 2020]

Gilmore LA, Walzem RL, Crouse SF, Smith DR, Adams TH, Vaidyanathan V, Cao X, Smith SB (2011a) Consumption of high-oleic acid ground beef increases HDL-cholesterol concentration but both high- and low-oleic acid ground beef decrease HDL particle diameter in normocholesterolemic men. The Journal of Nutrition 141, 1188–1194.
Consumption of high-oleic acid ground beef increases HDL-cholesterol concentration but both high- and low-oleic acid ground beef decrease HDL particle diameter in normocholesterolemic men.Crossref | GoogleScholarGoogle Scholar | 21525253PubMed |

Gilmore LA, Walzem RL, Crouse SF, Smith DR, Adams TH, Vaidyanathan V, Cao X, Smith SB (2011b) Consumption of high-oleic acid ground beef increases HDL-cholesterol concentration but both high- and low-oleic acid ground beef decrease HDL particle diameter in normocholesterolemic men. The Journal of Nutrition 141, 1188–1194.
Consumption of high-oleic acid ground beef increases HDL-cholesterol concentration but both high- and low-oleic acid ground beef decrease HDL particle diameter in normocholesterolemic men.Crossref | GoogleScholarGoogle Scholar | 21525253PubMed |

Gotoh T, Joo ST (2016) Characteristics and health benefit of highly marbled Wagyu and Hanwoo beef. Han-gug Chugsan Sigpum Hag-hoeji 36, 709–718.
Characteristics and health benefit of highly marbled Wagyu and Hanwoo beef.Crossref | GoogleScholarGoogle Scholar |

Grundy SM (1994) Influence of stearic acid on cholesterol metabolism relative to other long-chain fatty acids. The American Journal of Clinical Nutrition 60, 986S–990S.
Influence of stearic acid on cholesterol metabolism relative to other long-chain fatty acids.Crossref | GoogleScholarGoogle Scholar | 7977157PubMed |

Heianza Y, Ma W, Manson JE, Rexrode KM, Qi L (2017) Gut microbiota metabolites and risk of major adverse cardiovascular disease events and death: a systematic review and meta‐analysis of prospective studies. Journal of the American Heart Association 6, e004947
Gut microbiota metabolites and risk of major adverse cardiovascular disease events and death: a systematic review and meta‐analysis of prospective studies.Crossref | GoogleScholarGoogle Scholar | 28663251PubMed |

Holub BJ (1982) The nutritional significance, metabolism, and function of myo-inositol and phosphatidylinositol in health and disease. Advances in Nutritional Research 4, 107–141.
The nutritional significance, metabolism, and function of myo-inositol and phosphatidylinositol in health and disease.Crossref | GoogleScholarGoogle Scholar | 6278902PubMed |

National Health and Medical Research Council (Aus) and Ministry of Health (NZ). (2017) Nutrient Reference Values for Australia and New Zealand. Fats: total fat & fatty acids. Available at https://www.nrv.gov.au/nutrients/fats-total-fat-fatty-acids [Verified 10 September 2020]

Huang Y-C, Li H-J, He Z-F, Wang T, Qin G (2010) Study on the flavor contribution of phospholipids and triglycerides to pork. Food Science and Biotechnology 19, 1267–1276.
Study on the flavor contribution of phospholipids and triglycerides to pork.Crossref | GoogleScholarGoogle Scholar |

Hwang YH, Joo ST (2017) Fatty acid profiles, meat quality, and sensory palatability of grain-fed and grass-fed beef from Hanwoo, American, and Australian crossbred cattle. Han-gug Chugsan Sigpum Hag-hoeji 37, 153–161.
Fatty acid profiles, meat quality, and sensory palatability of grain-fed and grass-fed beef from Hanwoo, American, and Australian crossbred cattle.Crossref | GoogleScholarGoogle Scholar |

Ian Givens D, Gibbs RA (2008) Current intakes of EPA and DHA in European populations and the potential of animal-derived foods to increase them. The Proceedings of the Nutrition Society 67, 273–280.
Current intakes of EPA and DHA in European populations and the potential of animal-derived foods to increase them.Crossref | GoogleScholarGoogle Scholar | 18498671PubMed |

Imaizumi K, Sekihara K, Sugano M (1991) Hypocholesterolemic action of dietary phosphatidylethanolamine in rats sensitive to exogenous cholesterol. The Journal of Nutritional Biochemistry 2, 251–254.
Hypocholesterolemic action of dietary phosphatidylethanolamine in rats sensitive to exogenous cholesterol.Crossref | GoogleScholarGoogle Scholar |

Ministry of Primary Industries (2016) Primary growth partnership annual report, 1 July 2015 to 30 June 2016. New Zealand Government, Wellington, New Zealand.

Ismail SR, Maarof SK, Siedar Ali S, Ali A (2018) Systematic review of palm oil consumption and the risk of cardiovascular disease. PLoS One 13, e0193533
Systematic review of palm oil consumption and the risk of cardiovascular disease.Crossref | GoogleScholarGoogle Scholar | 29489910PubMed |

Kato-Kataoka A, Sakai M, Ebina R, Nonaka C, Asano T, Miyamori T (2010) Soybean-derived phosphatidylserine improves memory function of the elderly Japanese subjects with memory complaints. Journal of Clinical Biochemistry and Nutrition 47, 246–255.
Soybean-derived phosphatidylserine improves memory function of the elderly Japanese subjects with memory complaints.Crossref | GoogleScholarGoogle Scholar | 21103034PubMed |

Kaur G, Cameron-Smith D, Garg M, Sinclair AJ (2011) Docosapentaenoic acid (22:5n-3): a review of its biological effects. Progress in Lipid Research 50, 28–34.
Docosapentaenoic acid (22:5n-3): a review of its biological effects.Crossref | GoogleScholarGoogle Scholar | 20655949PubMed |

Kaur G, Guo XF, Sinclair AJ (2016) Short update on docosapentaenoic acid: a bioactive long-chain n-3 fatty acid. Current Opinion in Clinical Nutrition and Metabolic Care 19, 88–91.
Short update on docosapentaenoic acid: a bioactive long-chain n-3 fatty acid.Crossref | GoogleScholarGoogle Scholar | 26808265PubMed |

Kazala EC, Lozeman FJ, Mir PS, Laroche A, Bailey DR, Weselake RJ (1999) Relationship of fatty acid composition to intramuscular fat content in beef from crossbred Wagyu cattle. Journal of Animal Science 77, 1717–1725.
Relationship of fatty acid composition to intramuscular fat content in beef from crossbred Wagyu cattle.Crossref | GoogleScholarGoogle Scholar | 10438017PubMed |

Knight TW, Knowles S, Death AF, West J, Agnew M, Morris CA, Purchas RW (2003) Factors affecting the variation in fatty acid concentrations in lean beef from grass‐fed cattle in New Zealand and the implications for human health. New Zealand Journal of Agricultural Research 46, 83–95.
Factors affecting the variation in fatty acid concentrations in lean beef from grass‐fed cattle in New Zealand and the implications for human health.Crossref | GoogleScholarGoogle Scholar |

Kullenberg D, Taylor LA, Schneider M, Massing U (2012) Health effects of dietary phospholipids. Lipids in Health and Disease 11, 3
Health effects of dietary phospholipids.Crossref | GoogleScholarGoogle Scholar | 22221489PubMed |

Landfald B, Valeur J, Berstad A, Raa J (2017) Microbial trimethylamine-N-oxide as a disease marker: something fishy? Microbial Ecology in Health and Disease 28, 1327309
Microbial trimethylamine-N-oxide as a disease marker: something fishy?Crossref | GoogleScholarGoogle Scholar | 28588431PubMed |

Larick DK, Turner BE (1989) Influence of finishing diet on the phospholipid composition and fatty acid profile of individual phospholipids in lean muscle of beef cattle. Journal of Animal Science 67, 2282–2293.
Influence of finishing diet on the phospholipid composition and fatty acid profile of individual phospholipids in lean muscle of beef cattle.Crossref | GoogleScholarGoogle Scholar |

Larick DK, Turner BE, Koch RM, Crouse JD (1989) Influence of phospholipid content and fatty acid composition of individual phospholipids in muscle from Bison, Hereford and Brahman steers on flavour. Journal of Food Science 54, 521–526.
Influence of phospholipid content and fatty acid composition of individual phospholipids in muscle from Bison, Hereford and Brahman steers on flavour.Crossref | GoogleScholarGoogle Scholar |

Lopez-Huertas E (2010) Health effects of oleic acid and long chain omega-3 fatty acids (EPA and DHA) enriched milks. A review of intervention studies. Pharmacological Research 61, 200–207.
Health effects of oleic acid and long chain omega-3 fatty acids (EPA and DHA) enriched milks. A review of intervention studies.Crossref | GoogleScholarGoogle Scholar | 19897038PubMed |

McAfee AJ, McSorley EM, Cuskelly GJ, Fearon AM, Moss BW, Beattie JA, Wallace JM, Bonham MP, Strain JJ (2011) Red meat from animals offered a grass diet increases plasma and platelet n-3 PUFA in healthy consumers. British Journal of Nutrition 105, 80–89.
Red meat from animals offered a grass diet increases plasma and platelet n-3 PUFA in healthy consumers.Crossref | GoogleScholarGoogle Scholar | 20807460PubMed |

Mir Z, Paterson LJ, Mir PS (2000) Fatty acid composition and conjugated linoleic acid content of intramuscular fat in crossbred cattle with and without Wagyu genetics fed a barley-based diet. Canadian Journal of Animal Science 80, 195–197.
Fatty acid composition and conjugated linoleic acid content of intramuscular fat in crossbred cattle with and without Wagyu genetics fed a barley-based diet.Crossref | GoogleScholarGoogle Scholar |

Nantapo CT, Muchenje V, Hugo A (2014) Atherogenicity index and health-related fatty acids in different stages of lactation from Friesian, Jersey and Friesian × Jersey cross cow milk under a pasture-based dairy system. Food Chemistry 146, 127–133.
Atherogenicity index and health-related fatty acids in different stages of lactation from Friesian, Jersey and Friesian × Jersey cross cow milk under a pasture-based dairy system.Crossref | GoogleScholarGoogle Scholar | 24176323PubMed |

Narvaez-Rivas M, Gallardo E, Rios JJ, Leon-Camacho M (2011) A new high-performance liquid chromatographic method with evaporative light scattering detector for the analysis of phospholipids. Application to Iberian pig subcutaneous fat. Journal of Chromatography. A 1218, 3453–3458.
A new high-performance liquid chromatographic method with evaporative light scattering detector for the analysis of phospholipids. Application to Iberian pig subcutaneous fat.Crossref | GoogleScholarGoogle Scholar | 21507406PubMed |

Ooi EM, Watts GF, Ng TW, Barrett PH (2015) Effect of dietary fatty acids on human lipoprotein metabolism: a comprehensive update. Nutrients 7, 4416–4425.
Effect of dietary fatty acids on human lipoprotein metabolism: a comprehensive update.Crossref | GoogleScholarGoogle Scholar | 26043038PubMed |

Patel D, Witt SN (2017) Ethanolamine and phosphatidylethanolamine: partners in health and disease. Oxidative Medicine and Cellular Longevity 2017, 18
Ethanolamine and phosphatidylethanolamine: partners in health and disease.Crossref | GoogleScholarGoogle Scholar |

Purchas RW, Knight TW, Busboom JR (2005) The effect of production system and age on concentrations of fatty acids in intramuscular fat of the longissimus and triceps brachii muscles of Angus-cross heifers. Meat Science 70, 597–603.
The effect of production system and age on concentrations of fatty acids in intramuscular fat of the longissimus and triceps brachii muscles of Angus-cross heifers.Crossref | GoogleScholarGoogle Scholar | 22063885PubMed |

Ramprasath VR, Jones PJ, Buckley DD, Woollett LA, Heubi JE (2013) Effect of dietary sphingomyelin on absorption and fractional synthetic rate of cholesterol and serum lipid profile in humans. Lipids in Health and Disease 12, 125
Effect of dietary sphingomyelin on absorption and fractional synthetic rate of cholesterol and serum lipid profile in humans.Crossref | GoogleScholarGoogle Scholar | 23958473PubMed |

Reis MG, Roy NC, Bermingham EN, Ryan L, Bibiloni R, Young W, Krause L, Berger B, North M, Stelwagen K, Reis MM (2013) Impact of dietary dairy polar lipids on lipid metabolism of mice fed a high-fat diet. Journal of Agricultural and Food Chemistry 61, 2729–2738.
Impact of dietary dairy polar lipids on lipid metabolism of mice fed a high-fat diet.Crossref | GoogleScholarGoogle Scholar | 23394615PubMed |

Richter Y, Herzog Y, Lifshitz Y, Hayun R, Zchut S (2013) The effect of soybean-derived phosphatidylserine on cognitive performance in elderly with subjective memory complaints: a pilot study. Clinical Interventions in Aging 8, 557–563.

Rohrmann S, Linseisen J, Allenspach M, von Eckardstein A, Muller D (2016) Plasma concentrations of trimethylamine-N-oxide are directly associated with dairy food consumption and low-grade inflammation in a German adult population. The Journal of Nutrition 146, 283–289.
Plasma concentrations of trimethylamine-N-oxide are directly associated with dairy food consumption and low-grade inflammation in a German adult population.Crossref | GoogleScholarGoogle Scholar | 26674761PubMed |

Sales-Campos H, Souza PR, Peghini BC, da Silva JS, Cardoso CR (2013) An overview of the modulatory effects of oleic acid in health and disease. Mini-Reviews in Medicinal Chemistry 13, 201–210.

Smith SB (2016) Marbling and its nutritional impact on risk factors for cardiovascular disease. Han-gug Chugsan Sigpum Hag-hoeji 36, 435–444.
Marbling and its nutritional impact on risk factors for cardiovascular disease.Crossref | GoogleScholarGoogle Scholar |

Sturdivant CA, Lunt DK, Smith GC, Smith SB (1992) Fatty acid composition of subcutaneous and intramuscular adipose tissues and M. longissimus dorsi of Wagyu cattle. Meat Science 32, 449–458.
Fatty acid composition of subcutaneous and intramuscular adipose tissues and M. longissimus dorsi of Wagyu cattle.Crossref | GoogleScholarGoogle Scholar | 22059895PubMed |

Tang WH, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL (2013) Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. The New England Journal of Medicine 368, 1575–1584.
Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk.Crossref | GoogleScholarGoogle Scholar | 23614584PubMed |

Thorning TK, Raziani F, Bendsen NT, Astrup A, Tholstrup T, Raben A (2015) Diets with high-fat cheese, high-fat meat, or carbohydrate on cardiovascular risk markers in overweight postmenopausal women: a randomized crossover trial. The American Journal of Clinical Nutrition 102, 573–581.
Diets with high-fat cheese, high-fat meat, or carbohydrate on cardiovascular risk markers in overweight postmenopausal women: a randomized crossover trial.Crossref | GoogleScholarGoogle Scholar | 26178720PubMed |

Turner TD, Jensen J, Pilfold JL, Prema D, Donkor KK, Cinel B, Thompson DJ, Dugan MER, Church JS (2015) Comparison of fatty acids in beef tissues from conventional, organic and natural feeding systems in western Canada. Canadian Journal of Animal Science 95, 49–58.
Comparison of fatty acids in beef tissues from conventional, organic and natural feeding systems in western Canada.Crossref | GoogleScholarGoogle Scholar |

Ulbricht TL, Southgate DA (1991) Coronary heart disease: seven dietary factors. Lancet 338, 985–992.
Coronary heart disease: seven dietary factors.Crossref | GoogleScholarGoogle Scholar | 1681350PubMed |

Van Hecke T, Jakobsen LM, Vossen E, Gueraud F, De Vos F, Pierre F, Bertram HC, De Smet S (2016) Short-term beef consumption promotes systemic oxidative stress, TMAO formation and inflammation in rats, and dietary fat content modulates these effects. Food & Function 7, 3760–3771.
Short-term beef consumption promotes systemic oxidative stress, TMAO formation and inflammation in rats, and dietary fat content modulates these effects.Crossref | GoogleScholarGoogle Scholar |

Vargas-Bello-Perez E, Larrain RE (2017) Impacts of fat from ruminants’ meat on cardiovascular health and possible strategies to alter its lipid composition. Journal of the Science of Food and Agriculture 97, 1969–1978.
Impacts of fat from ruminants’ meat on cardiovascular health and possible strategies to alter its lipid composition.Crossref | GoogleScholarGoogle Scholar | 27925211PubMed |

Vesper H, Schmelz E-M, Nikolova-Karakashian MN, Dillehay DL, Lynch DV, Merrill AH (1999) Sphingolipids in food and the emerging importance of sphingolipids to nutrition. The Journal of Nutrition 129, 1239–1250.
Sphingolipids in food and the emerging importance of sphingolipids to nutrition.Crossref | GoogleScholarGoogle Scholar | 10395583PubMed |

Weiland A, Bub A, Barth SW, Schrezenmeir J, Pfeuffer M (2016) Effects of dietary milk- and soya-phospholipids on lipid-parameters and other risk indicators for cardiovascular diseases in overweight or obese men: two double-blind, randomised, controlled, clinical trials. Journal of Nutritional Science 5, e21
Effects of dietary milk- and soya-phospholipids on lipid-parameters and other risk indicators for cardiovascular diseases in overweight or obese men: two double-blind, randomised, controlled, clinical trials.Crossref | GoogleScholarGoogle Scholar | 27293558PubMed |

Wood JD, Richardson RI, Nute GR, Fisher AV, Campo MM, Kasapidou E, Sheard PR, Enser M (2004) Effects of fatty acids on meat quality: a review. Meat Science 66, 21–32.
Effects of fatty acids on meat quality: a review.Crossref | GoogleScholarGoogle Scholar | 22063928PubMed |

Xie YR, Busboom JR, Cornforth DP, Shenton HT, Gaskins CT, Johnson KA, Reeves JJ, Wright RW, Cronrath JD (1996) Effects of time on feed and post-mortem aging on palatability and lipid composition of crossbred Wagyu beef. Meat Science 43, 157–166.
Effects of time on feed and post-mortem aging on palatability and lipid composition of crossbred Wagyu beef.Crossref | GoogleScholarGoogle Scholar | 22060570PubMed |

Zeisel SH, Warrier M (2017) Trimethylamine N-oxide (TMAO), the microbiome, and heart and kidney disease. Annual Review of Nutrition 37, 157-181

Zhang AQ, Mitchell SC, Smith RL (1999) Dietary precursors of trimethylamine in man: a pilot study. Food and Chemical Toxicology 37, 515–520.
Dietary precursors of trimethylamine in man: a pilot study.Crossref | GoogleScholarGoogle Scholar | 10456680PubMed |

Zhou L, Le Grandois J, Marchioni E, Zhao M, Ennahar S, Bindler F (2010) Improvement of total lipid and glycerophospholipid recoveries from various food matrices using pressurized liquid extraction. Journal of Agricultural and Food Chemistry 58, 9912–9917.
Improvement of total lipid and glycerophospholipid recoveries from various food matrices using pressurized liquid extraction.Crossref | GoogleScholarGoogle Scholar | 20738132PubMed |