Organic production enhances milk nutritional quality by shifting fatty acid composition: A United States-wide, 18-month study

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Benbrook, Charles M ^a   Butler, Gillian ^b   Latif, Maged A ^c   Leifert, Carlo ^b   Davis, Donald R ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c Organic Valley CROPP Cooperative Organic Prairie   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOCOSAPENTAENOIC ACID; ICOSAPENTAENOIC ACID; LINOLEIC ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID;

ADULT; ARTICLE; CONJUGATION; CONTROLLED STUDY; DAIRY PRODUCT; DIETARY REFERENCE INTAKE; FATTY ACID ANALYSIS; FEMALE; FOOD ANALYSIS; FOOD INTAKE; FOOD QUALITY; HUMAN; LIPID COMPOSITION; MILK; MILK PRODUCTION; NUTRITIONAL VALUE; ORGANIC FOOD; PRODUCT SAFETY; SEA FOOD; SEASONAL VARIATION; UNITED STATES; YOUNG ADULT;

ADULT; ALPHA-LINOLENIC ACID; ANIMALS; DAIRYING; FATTY ACIDS; FEMALE; FISHES; GEOGRAPHY; HUMANS; LINOLEIC ACID; MILK; NUTRITIVE VALUE; ORGANIC AGRICULTURE; SEASONS; TIME FACTORS; UNITED STATES; YOUNG ADULT;

EID: 84891919776     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082429     Document Type: Article

References (78)

1. U.S. Department of Agriculture (2010) Dietary guidelines for Americans, 7th Edition. Available: http://www.cnpp.usda.gov/DGAs2010-PolicyDocument. htm. Accessed 2013 Mar 15.
2. Chardigny J-M, Destaillats F, Malpuech-Brugère C, Moulin J, Bauman DE, et al. (2008) Do trans fatty acids from industrially produced sources and from natural sources have the same effect on cardiovascular diseases risk factors in healthy subjects? Results of the trans Fatty Acids Collaboration (TRANSFACT) study. Am J Clin Nutr 87: 558-566. (Pubitemid 351364535)
3. Mozaffarian D, Cao H, King IB, Lemaitre RN, Song X, et al. (2010) Transpalmitoleic acid, metabolic risk factors, and new-onset diabetes in U.S. adults. Ann Intern Med 153: 790-799.
4. German JB, Gibson RA, Krauss RM, Nestel P, Lamarche B, et al. (2009) A reappraisal of the impact of dairy foods and milk. Eur J Nutr 48: 191-203.
5. Elwood PC, Pickering JE, Givens DI, Gallacher JE (2010) The consumption of milk and dairy foods and the incidence of vascular disease and diabetes: an overview. Lipids 45: 925-939.
6. Ludwig DS, Willett WC (2013) Three daily servings of reduced-fat milk: an evidence-based recommendation? JAMA Pediatr doi:10.1001/jamapediatrics. 2013.2408. Accessed 3 July 2013.
7. Rosell M, Hakansson NN, Wolk A (2006) Association between dairy food consumption and weight change over 9 y in 19,352 perimenopausal women. Am J Clin Nutr 84: 1481-1488. (Pubitemid 44912834)
8. Stancliffe RA, Thorpe T, Zemel MB (2011) Dairy attenuates oxidative and inflammatory stress in metabolic syndrome. Am J Clin Nutr 94: 422-30.
9. Bonthuis M, Hughes MCB, Ibiebele TI, Green AC, van der Pols JC (2010) Dairy consumption and patterns of mortality of Australian adults. Eur J Clin Nutr 64: 569-577.
10. Larsson SC, Bergkvist L, Wolk A (2005) High-fat dairy food and conjugated linoleic acid intakes in relation to colorectal cancer incidence in the Swedish Mammography Cohort. Am J Clin Nutr 82: 894-900. (Pubitemid 43779706)
11. Rice BH, Quann EE, Miller GD (2013) Meeting and exceeding dairy recommendations: effects of dairy consumption on nutrient intakes and risk of chronic disease. Nutr Rev 71: 209-223.
12. Haug A, Høstmark AT, Harstad OM (2007) Bovine milk in human nutrition-a review. Lipids Health Dis 6: 25, doi: 10.1186/1476-511X-6-25 Available: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2039733. Accessed 2013 Aug 10.
13. Simopoulos AP (2006) Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biomed Pharmacother 60: 502-507. (Pubitemid 44635081)
14. Russo GL (2009) Dietary n-6 and n-3 polyunsaturated fatty acids: From biochemistry to clinical implications in cardiovascular prevention. Biochem Pharma 77: 937-946.
15. Couvreur S, Hurtaud C, Lopez C, Delaby L, Peyraud JL (2006) The linear relationship between the proportion of fresh grass in the cow diet, milk fatty acid composition, and butter properties. J Dairy Sci 89: 1956-1969. (Pubitemid 44365782)
16. Lock AL, Bauman DE (2004) Modifying milk fat composition of dairy cows to enhance fatty acids beneficial to human health. Lipids 39: 1197-1206.
17. O'Donnell AM, Spatny KP, Vicini JL, Bauman DE (2010) Survey of the fatty acid composition of retail milk differing in label claims based on production management practices. J Dairy Sci 93: 1918-1925.
18. Butler G, Nielsen JH, Slots T, Seal C, Eyre MD, et al. (2008) Fatty acid and fatsoluble antioxidant concentrations in milk from high- and low-input conventional and organic systems: seasonal variation. J Sci Food Agric 88: 1431-1441. (Pubitemid 351744673)
19. Stergiadis S, Leifert C, Seal CJ, Eyre MD, Nielsen JH, et al. (2012) Effect of feeding intensity and milking system on nutritionally relevant milk components in dairy farming systems in North East of England. J Ag Food Chem 60: 7270-7281.
20. Krogh LM, Nielsen J, Leifert C, Slots T, Hald Kristensen G, et al. (2010). Milk quality as affected by feeding regimes in a country with climatic variation. J Dairy Sci 73: 2863-2873.
21. Butler G, Nielsen JH, Larsen ML, Rehberger B, Stergiadis S, et al. (2011) The effect of dairy management and processing on quality characteristics of milk and dairy products. NJAS - Wageningen J Life Sci 58: 97-102.
22. Butler G, Stergiadis S, Seal C, Eyre M, Leifert C (2011) Fat composition of organic and conventional retail milk in North East England. J Dairy Sci 94: 24-36.
23. Slots T, Butler G, Leifert C, Kristensen T, Skibsted LH, et al. (2009) Potentials to differentiate milk composition by different feeding strategies. J Dairy Sci 92: 2057-2066.
24. Blasbalg TL, Hibbeln JR, Ramsden CE, Majchrzak SF, Rawlings RR (2011) Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr 93: 950-962.
25. Hibbeln JR, Nieminen LRG, Blasbalg TL, Riggs JA, Lands WEM (2006) Healthy intakes of ω-3 and ω-6 fatty acids: estimations considering worldwide diversity. Am J Clin Nutr 83: 1483S-1493S. (Pubitemid 44713089)
26. Kris-Etherton PM, Taylor DS, Yu-Poth S, Huth P, Moriarty K, et al. (2000) Polyunsaturated fatty acids in the food chain in the United States. Am J Clin Nutr 71: 179S-188S. (Pubitemid 30046114)
27. Masters C (1996) Fatty acids and the peroxisome. Mol Cell Biochem 165: 83-93.
28. Ailhaud G, Massiera F, Alessandri J-M, Guesnet P (2007) Fatty acid composition as an early determinant of childhood obesity. Genes Nutr 2: 39-40.
29. Gebauer SK, Psota TL, Harris WS, Kris-Etherton PM (2006) n-3 fatty acid dietary recommendations and food sources to achieve essentiality and cardiovascular benefits. Am J Clin Nutr 83: S1526-15355.
30. Yamagishi K, Iso H, Date C, Fukui M, Wakai K, et al. (2008) Fish, omega-3 polyunsaturated fatty acids, and mortality from cardiovascular diseases in a nationwide community-based cohort of Japanese men and women. J Am Coll Cardio 52: 988-996.
31. De Caterina R (2011) n-3 fatty acids in cardiovascular disease. New Eng J Med 364: 2439-2450.
32. 13C and the a-linolenic acid content of milk fat. J Agric Food Chem 57: 785-790.
33. Rist L, Mueller A, Barthel C, Snijders B, Jansen M, et al. (2007) Influence of organic diet on the amount of conjugated linoleic acids in breast milk of lactating women in the Netherlands. Brit J Nutr 97: 735-743. (Pubitemid 46470682)
34. Woods VB, Fearon AM (2009) Dietary sources of unsaturated fatty acids for animals and their transfer into meat, milk and eggs: A review. Livestock Sci 126: 1-20.
35. Rinehart L, Baier A (2011) Pasture for organic ruminant livestock: understanding and implementing the national organic program (NOP) pasture rule. Agricultural Marketing Service, U.S. Department of Agriculture. Available: http://www.ams.usda.gov/AMSv1.0/getfile?dDocName=STELPRDC5091036.Accessed 2013May 1.
36. McBride W, Greene C (2009) Characteristics, costs, and issues for organic dairy farming. Economic research report no. 82, Washington, DC: U.S. Department of Agriculture. Available: http://www.ers.usda.gov/publications/err- economicresearch-report/err82.aspx#.UZPDOUouffA. Accessed 2013 May 1.
37. Donahue SMA, Rifas-Shiman SL, Gold DR, Jouni ZE, Gillman MW, et al. (2011) Prenatal fatty acid status and child adiposity at age 3 y: results from a US pregnancy cohort. Am J Clin Nutr 93: 780-788.
38. Brostow DP, Odegaard AO, Koh WP, Duval S, Gross MD, et al. (2011) Omega- 3 fatty acids and incident type 2 diabetes: the Singapore Chinese Health Study. Am J Clin Nutr 94: 520-526.
39. Moon RJ, Harvey NC, Robinson SM, Ntani G, Davies JH, et al. (2013) Maternal plasma polyunsaturated fatty acid status in late pregnancy is associated with offspring body composition in childhood. J Clin Endocrinol Metab 98: 299-307.
40. Schuchardt JP, Huss M, Strauss-Grabo M, Hahn A (2010) Significance of longchain polyunsaturated fatty acids (PUFAs) for the development and behavior of children. Eur J Pediatr 169: 149-164.
41. Ryan AS, Astwood JD, Gautier S, Kuratko CN, Nelson EB, et al. (2010) Effects of long-chain polyunsaturated fatty acid supplementation on neurodevelopment in childhood: A review of human studies. Prostag Leukotr ESS 82: 305-314.
42. Kummeling I, Thijs C, Huber M, van de Vijver LPL, Snijders BEP, et al. (2007) Consumption of organic foods and risk of atopic disease during the first 2 years of life in the Netherlands. Brit J Nutr 99: 598-605.
43. Wang L, Folsom AR, Zheng ZJ, Pankow JS, Eckfeldt JH (2003) Plasma fatty acid composition and incidence of diabetes in middle-aged adults. Am J Clin Nutr 78: 91-98.
44. Djousse L, Biggs ML, Lemaitre RN, King IB, Song X, et al. (2011) Plasma omega-3 fatty acids and incident diabetes in older adults. Am J Clin Nutr 94: 527-533.
45. Safarinejad MR, Hosseini SY, Dadkhah F, Asgari MA (2009) Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and antioxidant status of seminal plasma: A comparison between fertile and infertile men. Clin Nutr 29: 100-105.
46. Yehuda S, Rabinovitz-Shenkar S, Carasso RL (2011) Effects of essential fatty acids in iron deficient and sleep-disturbed attention deficit hyperactivity disorder (ADHD) children. Eur J Clin Nutr 65: 1167-1169.
47. Studer M, Briel M, Leimenstroll B, Glass TR, Bucher HC (2005) Effect of different antilipidemic agents and diets on mortality. Arch Int Med 165: 725-730. (Pubitemid 40569423)
48. Ailhaud G, Guesnet P (2004) Fatty acid composition of fats is an early determinant of childhood obesity: a short review and opinion. Obes Rev 5: 21-26. (Pubitemid 38173591)
49. AOAC International (2012) Official methods of analysis of AOAC International, 19th ed., Gaithersburg, MD, U.S.
50. McCullough BD, Heiser DA (2008) On the accuracy of statistical procedures in Microsoft Excel 2007. Comput Stat Data An 52: 4570-4578.
51. Forkman J (2009) Estimator and tests for common coefficients of variation in normal distributions. Commun Stat A-Theor 38: 233-251.
52. Smit LA, Baylin A, Campos H (2010) Conjugated linoleic acid in adipose tissue and risk of myocardial infraction. Am J Clin Nutr 92: 34-40.
53. Li G, Barnes D, Butz D, Bjorling D, Cook M (2005) 10t,12c-conjugated linoleic acid inhibits lipopolysaccharide-induced cyclooxygenase expression in vitro and in vivo. J Lipid Res 46: 2134-2142. (Pubitemid 41377465)
54. (2004) The role of conjugated linoleic acid in human health. Proceedings of a workshop. Winnipeg, Canada, March 13-15, 2003. Am J Clin Nutr 79: 1131S-1220S.
55. U.S. Department of Agriculture (2012) National nutrient database for standard reference, release 25. Available: http://ndb.nal.usda.gov. Accessed 2013 Mar 8.
56. Glasser F, Doreau M, Ferlay A, Chilliard Y (2007) Technical note: estimation of milk fatty acid yield from milk fat data. J Dairy Sci 90: 2302-2304. (Pubitemid 350063992)
57. Rymer C, Givens DI, Wahle KWJ (2003) Dietary strategies for increasing docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) concentrations in bovine milk: a review. Nutr Abs Rev Series B, Livestock Feeds and Feeding 73: 9R-25R.
58. Palupi E, Jayanegara A, Ploegera A, Kahl J (2012) Comparison of nutritional quality between conventional and organic dairy products: a meta-analysis. J Sci Food Agric DOI: 10.1002/jsfa.5639.
59. U.S. Department of Agriculture (2008) Dairy 2007, Part II: Changes in the U.S. dairy cattle industry, 1991-2007, USDA-APHIS-VS, CEAH, Fort Collins, Co. #N481.0308. Available: http://www.aphis.usda.gov/animal-health/nahms/dairy/ downloads/dairy07/Dairy07-dr-PartII.pdf. Accessed 2013 May 1.
60. Mathews KH, McConnell MJ (2009) Ethanol co-product use in U.S. cattle feeding: lessons learned and considerations. FDS-09D-01, Economic Research Service, U.S. Department of Agriculture. Available: http://usda01.library. cornell.edu/usda/ers/FDS//2000s/2009/FDS-04-17-2009-Special-Report.pdf. Accessed 2013 Oct 10.
61. Butler LJ (2002) The economics of organic milk production in California: a comparison with conventional costs. Am J Alt Agric 17: 83-91. (Pubitemid 34609322)
62. Massiera F, Barbry P, Guesnet P, Joly A, Luquet S, et al. (2010) A Western-like fat diet is sufficient to induce a gradual enhancement in fat mass over generations. J Lipid Res 51: 2352-2361.
63. Meyer BJ, Mann NJ, Lewis JL, Milligan GC, Sinclair AJ, et al. (2006) Dietary intakes and food sources of omega-6 and omega-3 polyunsaturated fatty acids. Lipids 38: 391-398.
64. Wood JAT, Williams JS, Pandarinathan L, Janero DR, Lammi-Keefe CJ, et al. (2010) Dietary docosahexaenoic acid supplementation alters select physiological endocannabinoid-system metabolites in brain and plasma. J Lipid Res 51: 1416-1423.
65. Amminger GP, Schafer MR, Papageorgiou K, Klier CM, Cotton SM, et al. (2010) Long-chain ω-3 fatty acids for indicated prevention of psychotic disorders: a randomized, placebo-controlled trial. Arch Gen Psychiatry 67: 146-154.
66. Ruxton CHS, Calder PC, Reed SC, Simpson MJA (2005) The impact of longchain n-3 polyunsaturated fatty acids on human health. Nutr Res Rev 18: 113-129. (Pubitemid 40826918)
67. Childs CE, Romeu-Nadal M, Burdge GC, Calder PC (2008) Gender differences in the ω-3 fatty acid content of tissues, Proc Nutr Soc 67: 19-27. (Pubitemid 351185353)
68. Pawlosky R, Hibbeln RJ, Lin Y, Salem N (2003) n-3 fatty acid metabolism in women. Brit J Nutr 90: 993-994. (Pubitemid 37328074)
69. Williams CM, Burdge G (2006) Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc 65: 42-50. (Pubitemid 43259983)
70. Gibson RA, Muhlhausler B, Makrides M (2011) Conversion of linoleic acid and alpha-linolenic acid to long-chain polyunsaturated fatty acids (LCPUFAs), with a focus on pregnancy, lactation and the first 2 years of life. Matern Child Nutr 7 Suppl 2: 17-26.
71. Emkin EA, Adlof RO, Gulley RM (1994) Dietary linoleic acid influences desaturation and acylation of deuterium-labeled linoleic and linolenic acids in young adult males. Biochim Biophys Acta 1213: 277-288. (Pubitemid 24262911)
72. Arterburn LM, Hall EB, Oken H (2006) Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr 83: 1467S-1476S. (Pubitemid 44713087)
73. Burdge GC, Calder PC (2005) a-Linolenic acid metabolism in adult humans: the effects of gender and age on conversion to longer-chain polyunsaturated fatty acids. Eur J Lipid Sci Technol 107: 426-439. (Pubitemid 40898344)
74. Brenna JT (2002) Efficiency of conversion of alpha-linolenic acid to long-chain n-3 fatty acids in man. Curr Opin Clin Nutr Metab Care 5: 127-132.
75. Burdge GC, Calder PC (2005) Conversion of alpha-linolenic acid to longerchain polyunsaturated fatty acids in human adults. Reprod Nutr Dev 45: 581-597. (Pubitemid 41511883)
76. Gebauer SK, Chardigny J-M, Jakobsen MU, Lamarche B, Lock AL, et al. (2011) Effects of ruminant trans fatty acids on cardiovascular disease and cancer: a comprehensive review of epidemiological, clinical, and mechanistic studies. Adv Nutr 2: 332-354.
77. U.S. Food and Drug Administration (2003) Regulation 21 CFR 101.9(c)(2)(ii) "Trans fat" or "Trans." Federal Register 68: 41502. Available: http://web.archive.org/web/20070103035701/http://www.cfsan. fda.gov/~acrobat/fr03711a.pdf. Accessed 2013 May 15.
78. Lacroix E, Charest A, Cyr A, Baril-Gravel L, Lebeuf Y, et al. (2012) Randomized controlled study of the effect of a butter naturally enriched in trans fatty acids on blood lipids in healthy women. Am J Clin Nutr 95: 318-325.