Content and Composition of Branched-Chain Fatty Acids in Bovine Milk Are Affected by Lactation Stage and Breed of Dairy Cow

Melissa L Bainbridge, Laura M Cersosimo, André-Denis G Wright, Jana Kraft, Melissa L Bainbridge, Laura M Cersosimo, André-Denis G Wright, Jana Kraft

Abstract

Dairy products contain bioactive fatty acids (FA) and are a unique dietary source of an emerging class of bioactive FA, branched-chain fatty acids (BCFA). The objective of this study was to compare the content and profile of bioactive FA in milk, with emphasis on BCFA, among Holstein (HO), Jersey (JE), and first generation HO x JE crossbreeds (CB) across a lactation to better understand the impact of these factors on FA of interest to human health. Twenty-two primiparous cows (n = 7 HO, n = 7 CB, n = 8 JE) were followed across a lactation. All cows were fed a consistent total mixed ration (TMR) at a 70:30 forage to concentrate ratio. Time points were defined as 5 days in milk (DIM), 95 DIM, 185 DIM, and 275 DIM. HO and CB had a higher content of n-3 FA at 5 DIM than JE and a lower n-6:n-3 ratio. Time point had an effect on the n-6:n-3 ratio, with the lowest value observed at 5 DIM and the highest at 185 DIM. The content of vaccenic acid was highest at 5 DIM, yet rumenic acid was unaffected by time point or breed. Total odd and BCFA (OBCFA) were higher in JE than HO and CB at 185 and 275 DIM. Breed affected the content of individual BCFA. The content of iso-14:0 and iso-16:0 in milk was higher in JE than HO and CB from 95 to 275 DIM. Total OBCFA were affected by time point, with the highest content in milk at 275 DIM. In conclusion, HO and CB exhibited a higher content of several bioactive FA in milk than JE. Across a lactation the greatest content of bioactive FA in milk occurred at 5 DIM and OBCFA were highest at 275 DIM.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1
Content of total branched-chain fatty acids (BCFA) [A], iso-15:0 [B], iso-17:0 [C], and 17:0 [D] per serving of whole milk (3.25% milk fat). Means are presented as least-squares (LS) means (n = 7 Holstein (HO), n = 8 Jersey (JE), and n = 7 HO x JE crossbreeds (CB)) and standard error. LS means without a common letter differ significantly (P<0.05). DIM = Days in milk.
Fig 2
Fig 2
Content of n-3 FA [A], n-6 FA [B], vaccenic acid (VA) [C], and rumenic acid (RA) [D] per serving of whole milk (3.25% milk fat). Means are presented as least-squares (LS) means (n = 7 Holstein (HO), n = 8 Jersey (JE), and n = 7 HO x JE crossbreeds (CB)) and standard error. LS means without a common letter differ significantly (P<0.05). DIM = Days in milk.

References

    1. Parodi PW. Cows’ milk fat components as potential anticarcinogenic agents. J. Nutr. 1997; 127: 1055–60.
    1. Moon H. Biological effects of conjugated linoleic acid on obesity-related cancers. Chem. Biol. Interact. 2014; 224: 189–95.
    1. Field CJ, Blewett HH, Proctor S, Vine D. Human health benefits of vaccenic acid. Appl. Physiol. Nutr. Metab. 2009; 34: 979–91. 10.1139/H09-079
    1. Zhao G, Etherton TD, Martin KR, West SG, Gillies PJ, Kris-Etherton PM. Dietary alpha-linolenic acid reduces inflammatory and lipid cardiovascular risk factors in hypercholesterolemic men and women. J. Nutr. 2004; 134: 2991–7.
    1. Pan H, Hu XZ, Jacobowitz DM, Chen C, McDonough J, Van Shura K, et al. Alpha-linolenic acid is a potent neuroprotective agent against soman-induced neuropathology. Neurotoxicology. 2012; 33: 1219–29. 10.1016/j.neuro.2012.07.001
    1. Fleming J, Kris-Etherton P. The evidence for α-linolenic acid and cardiovascular disease benefits: Comparisons with eicosapentaenoic acid and docosahexaenoic acid. Adv. Nutr. 2014; 5: 863–76S.
    1. Rice BH, Quann EE, Miller GD. Meeting and exceeding dairy recommendations: Effects of dairy consumption on nutrient intakes and risk of chronic disease. Nutr. Rev. 2013; 71: 209–23. 10.1111/nure.12007
    1. Gao D, Ning N, Wang C, Wang Y, Li Q, Meng Z, et al. Dairy products consumption and risk of type 2 diabetes: systematic review and dose-response meta-analysis. PLoS One. 2013; 8: e73965 10.1371/journal.pone.0073965
    1. Vatten LJ, Aune D, Norat T. Dairy products and the risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies. Am. J. Clin. Nutr. 2013; 98: 1066–83. 10.3945/ajcn.113.059030
    1. Soedamah-Muthu SS, Ding EL, Al-Delaimy WK, Hu FB, Engberink MF, Willett WC, et al. Milk and dairy consumption and incidence of cardiovascular diseases and all-cause mortality: dose-response meta-analysis of prospective cohort studies. Am. J. Clin. Nutr. 2011; 93: 158–71. 10.3945/ajcn.2010.29866
    1. Wongtangtintharn S, Oku H, Iwasaki H, Toda T. Effect of branched-chain fatty acids on fatty acid biosynthesis of human breast cancer cells. J. Nutr. Sci. Vitaminol. 2004; 50: 137–43.
    1. Ran-Ressler RR, Khailova L, Arganbright KM, Adkins-Rieck CK, Jouni ZE, Koren O, et al. Branched chain fatty acids reduce the incidence of necrotizing enterocolitis and alter gastrointestinal microbial ecology in a neonatal rat model. PLoS One. 2011; 6: e29032 10.1371/journal.pone.0029032
    1. Cai Q, Huang H, Qian D, Chen K, Luo J, Tian Y, et al. 13-Methyltetradecanoic acid exhibits anti-tumor activity on T-cell lymphomas in vitro and in vivo by down-regulating p-AKT and activating caspase-3. PLoS One. 2013; 8: 2–11.
    1. Kraft J, Jetton T, Satish B, Gupta D. Dairy-derived bioactive fatty acids improve pancreatic ß-cell function. FASEB J. 2015; 29: 608.25.
    1. Stefanov I, Baeten V, Abbas O, Colman E, Vlaeminck B, De Baets B, et al. Analysis of milk odd- and branched-chain fatty acids using fourier transform (FT)-Raman spectroscopy. J. Agric. Food Chem. 2010; 58: 10804–11. 10.1021/jf102037g
    1. Lock AL, Bauman DE. Modifying milk fat composition of dairy cows to enhance fatty acids beneficial to human health. Lipids. 2004; 39: 1197–206.
    1. Vlaeminck B, Dufour C, van Vuuren M, Cabrita RJ, Dewhurst RJ, Demeyer D, et al. Use of odd and branched-chain fatty acids in rumen contents and milk as a potential microbial marker. J. Dairy Sci. 2005; 88: 1031–42.
    1. Vlaeminck B, Fievez V, Cabrita RJ, Fonseca JM, Dewhurst RJ. Factors affecting odd- and branched-chain fatty acids in milk: A review. Anim. Feed Sci. Technol. 2006; 131: 389–417.
    1. Bainbridge ML, Cersosimo LM, Wright A-DG, Kraft J. Rumen bacterial communities in three breeds of dairy cattle shift from early to peak lactation. J. Dairy Sci. 2015; 98, E-Supplement 1: 245–246.
    1. Craninx M, Steen A, Van Laar H, Van Nespen T, Martín-Tereso J, De Baets B, et al. Effect of lactation stage on the odd- and branched-chain milk fatty acids of dairy cattle under grazing and indoor conditions. J. Dairy Sci. 2008; 91: 2662–77. 10.3168/jds.2007-0656
    1. USDA. Dairy 2007, Part I: Reference of dairy cattle health and management practices in the United States, 2007 USDAAPHIS-VS; 2007.
    1. Capper JL, Cady R. A comparison of the environmental impact of Jersey compared with Holstein milk for cheese production. J. Dairy Sci. 2012; 95: 165–76. 10.3168/jds.2011-4360
    1. White SL, Bertrand J, Wade MR, Washburn SP, Green JT, Jenkins TC. Comparison of fatty acid content of milk from Jersey and Holstein cows consuming pasture or a total mixed ration. J. Dairy Sci. 2001; 84: 2295–301.
    1. Kelsey J, Corl B, Collier RJ, Bauman DE. The effect of breed, parity, and stage of lactation on conjugated linoleic acid (CLA) in milk fat from dairy cows. J. Dairy Sci. 2003; 86: 2588–97.
    1. Palladino R, Buckley F, Prendiville R, Murphy JJ, Callan J, Kenny D. A comparison between Holstein-Friesian and Jersey dairy cows and their F(1) hybrid on milk fatty acid composition under grazing conditions. J. Dairy Sci. 2010; 93: 2176–84. 10.3168/jds.2009-2453
    1. Bainbridge ML, Lock AL, Kraft J. Lipid-encapsulated echium oil (Echium plantagineum) increases the content of stearidonic acid in plasma lipid fractions and milk fat of dairy cows. J. Agric. Food Chem. 2015; 63: 4827–35. 10.1021/acs.jafc.5b00857
    1. Glasser F, Doreau M, Ferlay A, Chilliard Y. Technical note: Estimation of milk fatty acid yield from milk fat data. J. Dairy Sci. 2007; 90: 2302–4.
    1. U.S. Department of Agriculture Agricultural Research Service. USDA National Nutrient Database for Standard Reference, Release 21. 2008.
    1. Moate PJ, Chalupa W, Boston RC, Lean IJ. Milk fatty acids. I. Variation in the concentration of individual fatty acids in bovine milk. J. Dairy Sci. 2007; 90: 4730–9.
    1. Kristensen T, Jensen C, Østergaard S, Weisbjerg MR, Aaes O, Nielsen NI. Feeding, production, and efficiency of Holstein-Friesian, Jersey, and mixed-breed lactating dairy cows in commercial Danish herds. J. Dairy Sci. 2015; 98: 263–74. 10.3168/jds.2014-8532
    1. Rastani RR, Andrew SM, Zinn S, Sniffen CJ. Body composition and estimated tissue energy balance in Jersey and Holstein cows during early lactation. J. Dairy Sci. 2001; 84: 1201–9.
    1. Ran-Ressler RR, Sim D, O’Donnell-Megaro M, Bauman DE, Barbano DM, Brenna JT. Branched chain fatty acid content of United States retail cow’s milk and implications for dietary intake. Lipids. 2011; 46: 569–76. 10.1007/s11745-011-3530-8
    1. Kaneda T. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 1991; 55: 288–302.
    1. Massart-Leën AM, Roets E, Peeters G, Verbeke R. Propionate for fatty acid synthesis by the mammary gland of the lactating goat. J. Dairy Sci. 1983; 66: 1445–54.
    1. Vlaeminck B, Gervais R, Rahman MM, Gadeyne F, Gorniak M, Doreau M, et al. Postruminal synthesis modifies the odd- and branched-chain fatty acid profile from the duodenum to milk. J. Dairy Sci. 2015; 98: 4829–40. 10.3168/jds.2014-9207
    1. Golley RK, Hendrie G. Evaluation of the relative concentration of serum fatty acids C14:0, C15:0 and C17:0 as markers of children’s dairy fat intake. Ann. Nutr. Metabol. 2014; 65: 310–6.
    1. Warensjö E, Jansson J-HK, Cederholm T, Boman K, Eliasson M, Hallmans G, et al. Biomarkers of milk fat and the risk of myocardial infarction in men and women : a prospective, matched case-control study. Am. J. Clin. Nutr. 2010; 92: 194–202. 10.3945/ajcn.2009.29054
    1. Santaren ID, Watkins SM, Liese AD, Wagenknecht LE, Rewers MJ, Haffner SM, et al. Serum pentadecanoic acid (15:0), a short-term marker of dairy food intake, is inversely associated with incident type 2 diabetes and its underlying disorders. Am. J. Clin. Nutr. 2014; 100: 1532–40. 10.3945/ajcn.114.092544
    1. Poger D, Caron B, Mark AE. Effect of methyl-branched fatty acids on the structure of lipid bilayers. J. Phys. Chem. 2014; 118: 13838–48.
    1. Suutari M, Laakso S. Unsaturated and branched chain-fatty acids in temperature adaptation of Bacillus subtilis and Bacillus megaterium. Biochim. Biophys. Acta. 1992; 1126: 119–24.
    1. Fievez V, Colman E, Castro-Montoya JM, Stefanov I, Vlaeminck B. Milk odd- and branched-chain fatty acids as biomarkers of rumen function—An update. Anim. Feed Sci. Technol. 2012; 172: 51–65.
    1. Vlaeminck B, Fievez V, Tamminga S, Dewhurst RJ, van Vuuren A, De Brabander D, et al. Milk odd- and branched-chain fatty acids in relation to the rumen fermentation pattern. J. Dairy Sci. 2006; 89: 3954–64.
    1. Yang Z, Liu S, Chen X, Chen H, Huang M, Zheng J. Induction of apoptotic cell death and in vivo growth inhibition of human cancer cells by a saturated branched-chain fatty acid, 13-methyltetradecanoic acid. Cancer Res. 2000; 60: 505–9.
    1. Baumann E, Chouinard PY, Lebeuf Y, Gervais R. Milk odd- and branched-chain fatty acid profile is affected by lactation stage in dairy cows. J. Dairy Sci. 2015; 98, E-Supplement 1: 141–142.
    1. Ran-Ressler RR, Devapatla S, Lawrence P, Brenna JT. Branched chain fatty acids are constituents of the normal healthy newborn gastrointestinal tract. Pediatr. Res. 2008; 64: 605–9. 10.1203/PDR.0b013e318184d2e6
    1. Bermudez B, Ortega-Gomez A, Varela LM, Villar J, Abia R, Muriana FJG, et al. Clustering effects on postprandial insulin secretion and sensitivity in response to meals with different fatty acid compositions. Food Funct. 2014; 5: 1374–80. 10.1039/c4fo00067f
    1. Hunter JE, Zhang J, Kris-Etherton PM. Cardiovascular disease risk of dietary stearic acid compared with trans, other saturated, and unsaturated fatty acids: a systematic review. Am. J. Clin. Nutr. 2010; 91: 46–63. 10.3945/ajcn.2009.27661
    1. Lemaitre RN, Fretts AM, Sitlani CM, Biggs ML, Mukamal K, King IB, et al. Plasma phospholipid very-long-chain saturated fatty acids and incident diabetes in older adults: the Cardiovascular Health Study. Am. J. Clin. Nutr. 2015; 101: 1047–54. 10.3945/ajcn.114.101857
    1. Dabadie H, Peuchant E, Bernard M, Leruyet P, Mendy F. Moderate intake of myristic acid in sn-2 position has beneficial lipidic effects and enhances DHA of cholesteryl esters in an interventional study. J. Nutr. Biochem. 2005; 16: 375–82.
    1. Temme EH, Mensink RP, Hornstra G. Effects of medium chain fatty acids (MCFA), myristic acid, and oleic acid on serum lipoproteins in healthy subjects. J. Lipid Res. 1997; 38: 1746–54.
    1. Poulsen N, Gustavsson F, Glantz M, Paulsson M, Larsen LB, Larsen MK. The influence of feed and herd on fatty acid composition in 3 dairy breeds (Danish Holstein, Danish Jersey, and Swedish Red). J. Dairy Sci. 2012; 95: 6362–71. 10.3168/jds.2012-5820
    1. Larsen MK, Hymøller L, Brask-Pedersen DB, Weisbjerg MR. Milk fatty acid composition and production performance of Danish Holstein and Danish Jersey cows fed different amounts of linseed and rapeseed. J. Dairy Sci. 2012; 95: 3569–78. 10.3168/jds.2011-5163
    1. Nantapo CTW, Muchenje V, Hugo A. Atherogenicity index and health-related fatty acids in different stages of lactation from Friesian, Jersey and Friesian x Jersey cross cow milk under a pasture-based dairy system. Food Chem. 2014; 146: 127–33. 10.1016/j.foodchem.2013.09.009
    1. Kay JK, Weber WJ, Moore CE, Bauman DE, Hansen LB, Chester-Jones H, et al. Effects of week of lactation and genetic selection for milk yield on milk fatty acid composition in Holstein cows. J. Dairy Sci. 2005; 88: 3886–93.
    1. Lerch S, Pires J, Delavaud C, Shingfield KJ, Pomiès D, Martin B, et al. Rapeseed or linseed in dairy cow diets over 2 consecutive lactations: Effects on adipose fatty acid profile and carry-over effects on milk fat composition in subsequent early lactation. J. Dairy Sci. 2015; 98: 1005–18. 10.3168/jds.2014-8578
    1. Zachut M, Arieli A, Lehrer H, Livshitz L, Yakoby S, Moallem U. Effects of increased supplementation of n-3 fatty acids to transition dairy cows on performance and fatty acid profile in plasma, adipose tissue, and milk fat. J. Dairy Sci. 2010; 93: 5877–89. 10.3168/jds.2010-3427
    1. Bauman DE, Currie BW. Partitioning of nutrients during pregnancy and lactation: A review of mechanisms involving homeostasis and homeorhesis. J. Dairy Sci. 1980; 63: 1514–29.
    1. Lock AL, Horne CM, Bauman DE, Salter AM. Butter naturally enriched in conjugated linoleic acid and vaccenic acid alters tissue fatty acids and improves the plasma lipoprotein profile in cholesterol-fed hamsters. J. Nutr. 2005; 135: 1934–9.
    1. Turpeinen AM, Mutanen M, Aro A, Salminen I, Basu S, Palmquist DL, et al. Bioconversion of vaccenic acid to conjugated linoleic acid in humans. Am. J. Clin. Nutr. 2002; 76: 504–10.
    1. Soyeurt H, Dehareng F, Mayeres P, Bertozzi C, Gengler N. Variation of Δ9-desaturase activity in dairy cattle. J. Dairy Sci. 2008; 91: 3211–24. 10.3168/jds.2007-0518
    1. IOM. Dietary Reference intakes for energy, carbohydrate, fiber, Fat, fatty acids, cholesterol, protein, and amino acids Washington D.C.: National Academies Press; 2005.
    1. Butler G, Stergiadis S, Seal C, Eyre M, Leifert C. Fat composition of organic and conventional retail milk in northeast England. J. Dairy Sci. 2011; 94: 24–36. 10.3168/jds.2010-3331
    1. Simopoulos AP. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 2002; 56: 365–79.
    1. U.S. Department of Agriculture and U.S. Department of Health and Human Services. Dietary Guidelines for Americans, 2010.

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