Nutrition
Volume 22, Issue 10 , Pages 1012-1024 , October 2006

Oily fish reduces plasma triacylglycerols: a primary prevention study in overweight men and women

  • Carmel S. Moore, Ph.D.

      Affiliations

    • Medical Research Council Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, United Kingdom
    • Corresponding Author InformationCorresponding author. Tel.: +0044-0-1223-426356; fax: +0044-0-1223-437515.
    • ,
  • Susan P. Bryant

      Affiliations

    • Medical Research Council Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, United Kingdom
    • ,
  • Gita D. Mishra, Ph.D.

      Affiliations

    • Medical Research Council Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, United Kingdom
    • ,
  • Jeremy D. Krebs, M.D.

      Affiliations

    • Medical Research Council Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, United Kingdom
    • ,
  • Lucy M. Browning, Ph.D.

      Affiliations

    • Medical Research Council Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, United Kingdom
    • ,
  • George J. Miller, M.D.

      Affiliations

    • Medical Research Council Cardiovascular Research Group, Wolfson Institute of Preventive Medicine, London, United Kingdom
    • ,
  • Susan A. Jebb, Ph.D.

      Affiliations

    • Medical Research Council Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, United Kingdom

Received 5 May 2006 ,Accepted 28 July 2006.

References 

  1. Burr ML, Fehily AM, Gilbert JF, Rogers S, Holliday RM, Sweetnam PM, et al. Effects of changes in fat, fish, and fibre intakes on death and myocardial reinfarction: diet and reinfarction trial (DART). Lancet. 1989;2(8666):757–761
  2. de Lorgeril M, Renaud S, Mamelle N, Salen P, Martin JL, Monjaud I, et al. Mediterranean alpha-linolenic acid-rich diet in secondary prevention of coronary heart disease. Lancet. 1994;343(8911):1454–1459
  3. Marchioli R, Barzi F, Bomba E, Chieffo C, Di Gregorio D, Di Mascio R, et al. Early protection against sudden death by n-3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Sopravvivenza nell’Infarto Miocardico (GISSI)-Prevenzione. Circulation. 2002;105:1897–1903
  4. Erkkila AT, Lichtenstein AH, Mozaffarian D, Herrington DM. Fish intake is associated with a reduced progression of coronary artery atherosclerosis in postmenopausal women with coronary artery disease. Am J Clin Nutr. 2004;80:626–632
  5. Popp-Snijders C, Schouten JA, Heine RJ, van der Meer J, van der Veen EA. Dietary supplementation of omega-3 polyunsaturated fatty acids improves insulin sensitivity in non-insulin-dependent diabetes. Diabetes Res. 1987;4:141–147
  6. Vessby B, Karlstrom B, Boberg M, Lithell H, Berne C. Polyunsaturated fatty acids may impair blood glucose control in type 2 diabetic patients. Diabet Med. 1992;9:126–133
  7. Tinker LF, Parks EJ, Behr SR, Schneeman BO, Davis PA. (N-3) fatty acid supplementation in moderately hypertriglyceridemic adults changes postprandial lipid and apolipoprotein B responses to a standardized test meal. J Nutr. 1999;129:1126–1134
  8. Mori TA, Bao DQ, Burke V, Puddey IB, Watts GF, Beilin LJ. Dietary fish as a major component of a weight-loss diet: effect on serum lipids, glucose, and insulin metabolism in overweight hypertensive subjects. Am J Clin Nutr. 1999;70:817–825
  9. Stark KD, Park EJ, Maines VA, Holub BJ. Effect of a fish-oil concentrate on serum lipids in postmenopausal women receiving and not receiving hormone replacement therapy in a placebo-controlled, double-blind trial. Am J Clin Nutr. 2000;72:389–394
  10. Mori TA, Burke V, Puddey IB, Watts GF, O’Neal DN, Best JD, et al. Purified eicosapentaenoic and docosahexaenoic acids have differential effects on serum lipids and lipoproteins, LDL particle size, glucose, and insulin in mildly hyperlipidemic men. Am J Clin Nutr. 2000;71:1085–1094
  11. Lovegrove JA, Lovegrove SS, Lesauvage SV, Brady LM, Saini N, Minihane AM, et al. Moderate fish-oil supplementation reverses low-platelet, long-chain n-3 polyunsaturated fatty acid status and reduces plasma triacylglycerol concentrations in British Indo-Asians. Am J Clin Nutr. 2004;79:974–982
  12. Brady LM, Williams CM, Lovegrove JA. Dietary PUFA and the metabolic syndrome in Indian Asians living in the UK. Proc Nutr Soc. 2004;63:115–125
  13. Browning LM, Krebs JD, Moore CS, Mishra GD, O’Connell MA, Jebb SA. The impact of long chain n-3 polyunsaturated fatty acid supplementation on inflammation, insulin sensitivity and CVD risk in a group of overweight women with an inflammatory phenotype. Diabetes Obes Metab. 2006;(in press)
  14. Toft I, Bonaa KH, Ingebretsen OC, Nordoy A, Jenssen T. Effects of n-3 polyunsaturated fatty acids on glucose homeostasis and blood pressure in essential hypertension (A randomized, controlled trial). Ann Intern Med. 1995;123:911–918
  15. Hooper L, Thompson RL, Harrison RA, Summerbell CD, Moore H, Worthington HV, et al. Omega 3 fatty acids for prevention and treatment of cardiovascular disease. Cochrane Database Syst Rev. 2004;(4):CD003177
  16. von Lossonczy TO, Ruiter A, Bronsgeest-Schoute HC, van Gent CM, Hermus JJ. The effect of a fish diet on serum lipids in healthy human subjects. Am J Clin Nutr. 1978;31:1340–1346
  17. Fehilly AM, Burr ML, Phillips KM, Deadman NM. The effect of fatty fish on plasma lipid and lipoprotein concentrations. Am J Clin Nutr. 1983;38:349–351
  18. Lindgren FT, Adamson GL, Shore VG, Schmidt PC. Effect of a salmon diet on the distribution of plasma lipoproteins and alipoproteins in normolipidemic adult men. Lipids. 1991;26:97–101
  19. Tidwell DK, McNaughton JP, Pellum LK, McLaurin BP, Chen S. Comparison of the effects of adding fish high or low in n-3 fatty acids to a diet conforming to the dietary guidelines for Americans. J Am Diet Assoc. 1993;93:1124–1128
  20. Adler AI, Boyko EJ, Schraer CD, Murphy NJ. Lower prevalence of impaired glucose tolerance and diabetes associated with daily seal oil or salmon consumption among Alaska Natives. Diabetes Care. 1994;17:1498–1501
  21. Feskens EJ, Bowles CH, Kromhout D. Inverse association between fish intake and risk of glucose intolerance in normoglycemic elderly men and women. Diabetes Care. 1991;14:935–941
  22. Dewailly E, Blanchet C, Lemieux S, Sauve L, Gingras S, Ayotte P, et al. N-3 fatty acids and cardiovascular disease risk factors among the Inuit of Nunavik. Am J Clin Nutr. 2001;74:464–473
  23. Bjerregaard P, Pedersen HS, Mulvad G. The associations of a marine diet with plasma lipids, blood glucose, blood pressure and obesity among the Inuit in Greenland. Eur J Clin Nutr. 2000;54:732–737
  24. Dewailly EE, Blanchet C, Gingras S, Lemieux S, Sauve L, Bergeron J, et al. Relations between n-3 fatty acid status and cardiovascular disease risk factors among Quebecers. Am J Clin Nutr. 2001;74:603–611
  25. Harding AH, Day NE, Khaw KT, Bingham SA, Luben RN, Welsh A, et al. Habitual fish consumption and glycated haemoglobin: the EPIC-Norfolk study. Eur J Clin Nutr. 2004;58:277–284
  26. Freese R, Mutanen M, Valsta LM, Salminen I. Comparison of the effects of two diets rich in monounsaturated fatty acids differing in their linoleic/alpha-linolenic acid ratio on platelet aggregation. Thromb Haemost. 1994;71:73–77
  27. Nestel PJ, Pomeroy SE, Sasahara T, Yamashita T, Liang YL, Dart AM, et al. Arterial compliance in obese subjects is improved with dietary plant n-3 fatty acid from flaxseed oil despite increased LDL oxidizability. Arterioscler Thromb Vasc Biol. 1997;17:1163–1170
  28. Academies IoMotN. Dietary reference intakes: energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. Washington, DC: National Academy Press; 2002;
  29. Bemelmans WJ, Broer J, Feskens EJ, Smit AJ, Muskiet FA, Lefrandt JD, et al. Effect of an increased intake of alpha-linolenic acid and group nutritional education on cardiovascular risk factors: the Mediterranean Alpha-linolenic Enriched Groningen Dietary Intervention (MARGARIN) study. Am J Clin Nutr. 2002;75:221–227
  30. Burdge G. Alpha-linolenic acid metabolism in men and women: nutritional and biological implications. Curr Opin Clin Nutr Metab Care. 2004;7:137–144
  31. Sellmayer A, Witzgall H, Lorenz RL, Weber PC. Effects of dietary fish oil on ventricular premature complexes. Am J Cardiol. 1995;76:974–977
  32. Christensen JH, Gustenhoff P, Korup E, Aaroe J, Toft E, Moller J, et al. Effect of fish oil on heart rate variability in survivors of myocardial infarction: a double blind randomised controlled trial. BMJ. 1996;312(7032):677–678
  33. Nestel P, Shige H, Pomeroy S, Cehun M, Abbey M, Raederstorff D. The n-3 fatty acids eicosapentaenoic acid and docosahexaenoic acid increase systemic arterial compliance in humans. Am J Clin Nutr. 2002;76:326–330
  34. McVeigh GE, Brennan GM, Cohn JN, Finkelstein SM, Hayes RJ, Johnston GD. Fish oil improves arterial compliance in non–insulin-dependent diabetes mellitus. Arterioscler Thromb. 1994;14:1425–1429
  35. Appel LJ, Miller ER, Seidler AJ, Whelton PK. Does supplementation of diet with ‘fish oil’ reduce blood pressure? A meta-analysis of controlled clinical trials. Arch Intern Med. 1993;153:1429–1438
  36. Morris MC, Sacks F, Rosner B. Does fish oil lower blood pressure? A meta-analysis of controlled trials. Circulation. 1993;88:523–533
  37. Mori TA, Watts GF, Burke V, Hilme E, Puddey IB, Beilin LJ. Differential effects of eicosapentaenoic acid and docosahexaenoic acid on vascular reactivity of the forearm microcirculation in hyperlipidemic, overweight men. Circulation. 2000;102:1264–1269
  38. Mann N, Sinclair A, Pille M, Johnson L, Warrick G, Reder E, et al. The effect of short-term diets rich in fish, red meat, or white meat on thromboxane and prostacyclin synthesis in humans. Lipids. 1997;32:635–644
  39. Cobiac L, Clifton PM, Abbey M, Belling GB, Nestel PJ. Lipid, lipoprotein, and hemostatic effects of fish vs fish-oil n-3 fatty acids in mildly hyperlipidemic males. Am J Clin Nutr. 1991;53:1210–1216
  40. Knapp HR. Dietary fatty acids in human thrombosis and hemostasis. Am J Clin Nutr. 1997;65(suppl):1687S–1698S
  41. Shahar E, Folsom AR, Wu KK, Dennis BH, Shimakawa T, Conlan MG, et al. Associations of fish intake and dietary n-3 polyunsaturated fatty acids with a hypocoagulable profile (The Atherosclerosis Risk in Communities (ARIC) Study). Arterioscler Thromb. 1993;13:1205–1212
  42. Archer SL, Green D, Chamberlain M, Dyer AR, Liu K. Association of dietary fish and n-3 fatty acid intake with hemostatic factors in the coronary artery risk development in young adults (CARDIA) study. Arterioscler Thromb Vasc Biol. 1998;18:1119–1123
  43. Marckmann P, Bladbjerg EM, Jespersen J. Dietary fish oil (4 g daily) and cardiovascular risk markers in healthy men. Arterioscler Thromb Vasc Biol. 1997;17:3384–3391
  44. Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000;342:836–843
  45. Chae CU, Lee RT, Rifai N, Ridker PM. Blood pressure and inflammation in apparently healthy men. Hypertension. 2001;38:399–403
  46. Browning LM, Jebb SA, Mishra GD, Cooke JH, O’Connell MA, Crook MA, et al. Elevated sialic acid, but not CRP, predicts features of the metabolic syndrome independently of BMI in women. Int J Obes Relat Metab Disord. 2004;28:1004–1010
  47. Engstrom K, Wallin R, Saldeen T. Effect of low-dose aspirin in combination with stable fish oil on whole blood production of eicosanoids. Prostaglandins Leukot Essent Fatty Acids. 2001;64:291–297
  48. Endres S, Ghorbani R, Kelley VE, Georgilis K, Lonnemann G, van der Meer JW, et al. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N Engl J Med. 1989;320:265–271
  49. Meydani SN, Endres S, Woods MM, Goldin BR, Soo C, Morrill-Labrode A, et al. Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women. J Nutr. 1991;121:547–555
  50. Meydani SN, Lichtenstein AH, Cornwall S, Meydani M, Goldin BR, Rasmussen H, et al. Immunologic effects of national cholesterol education panel step-2 diets with and without fish-derived N-3 fatty acid enrichment. J Clin Invest. 1993;92:105–113
  51. Gallai V, Sarchielli P, Trequattrini A, Franceschini M, Floridi A, Firenze C, et al. Cytokine secretion and eicosanoid production in the peripheral blood mononuclear cells of MS patients undergoing dietary supplementation with n-3 polyunsaturated fatty acids. J Neuroimmunol. 1995;56:143–153
  52. Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ. The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr. 1996;63:116–122
  53. Schmidt EB, Nielsen LK, Pedersen JO, Kornerup HJ, Dyerberg J. The effect of n-3 polyunsaturated fatty acids on lipids, platelet function, coagulation, fibrinolysis and monocyte chemotaxis in patients with hypertension. Clin Chim Acta. 1990;189:25–32
  54. Rallidis LS, Paschos G, Liakos GK, Velissaridou AH, Anastasiadis G, Zampelas A. Dietary alpha-linolenic acid decreases C-reactive protein, serum amyloid A and interleukin-6 in dyslipidaemic patients. Atherosclerosis. 2003;167:237–242
  55. Friedwald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma without the use of the preparative ultracentrifuge. Clin Chem. 1972;18:499–502
  56. Morrisey JH, Macik BG, Nuenschwander PF, Comp PC. Quantitation of activated factor VII levels in plasma using a tissue factor mutant selectivity deficient in promoting factor VII activation. Blood. 1993;81:734–744
  57. Clauss A. Gerrinnung sphysiologische scnellmethode zur bestimmung des fibrinogens. Acta Haematol. 1957;17:237–246
  58. Definition, diagnosis and classification of diabetes mellitus and its complications. Report of a WHO consultattion. Part 1: diagnosis and classification of diabetes mellitus. Geneva: World Health Organization; 1999;
  59. Anderson L, Dinesen B, Jorgensen P, Poulson F, Roder M. Enzyme immunoasay for intact insulin in serum or plasma. Clin Chem. 1993;39:578–582
  60. Holland B, Welch AA, Unwin ID, Buss DH, Paul AA, Southgate AT. The composition of foods. 5th ed. London: Royal Society of Chemistry, Cambridge and the Ministry of Agriculture, Fisheries and Food; 1991;
  61. MAFF. Fatty acids. Seventh Supplement to the Fifth Edition of McCance and Widdowson’s The Composition of Foods. Cambridge: Royal Society of Chemistry; 1998;
  62. McNaughton SA, Moore CS, Bryant SP, Matthews N, Paul AA, Jebb SA. Relationship between dietary intake of essential polyunsaturated fatty acids and plasma status in a food-based intervention study. Proc Nutr Soc. 2004;63(38A):
  63. Folch J, Lees M, Sloane-Stanley G. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem. 1957;226:497–509
  64. Henderson L, Gregory J, Irving K. The national diet and nutrition survey: adults age 19–64 years. London: HMSO; 2003;
  65. Harris WS. N-3 fatty acids and serum lipoproteins: human studies. Am J Clin Nutr. 1997;65(suppl):1645S–1654S
  66. Stampfer MJ, Krauss RM, Ma J, Blanche PJ, Holl LG, Sacks FM, et al. A prospective study of triglyceride level, low-density lipoprotein particle diameter, and risk of myocardial infarction. JAMA. 1996;18:882–888
  67. Woollett L, Spady D, Dietschy J. Saturated and unsaturated fatty acids independently regulate low density lipoprotein receptor activity and production rate. J. Lipid Res. 1992;33:77–88
  68. Wijendran V, Hayes KC. Dietary n-6 and n-3 fatty acid balance and cardiovascular health. Annu Rev Nutr. 2004;24:597–615
  69. Woodman RJ, Mori TA, Burke V, Puddey IB, Watts GF, Beilin LJ. Effects of purified eicosapentaenoic and docosahexaenoic acids on glycemic control, blood pressure, and serum lipids in type 2 diabetic patients with treated hypertension. Am J Clin Nutr. 2002;76:1007–1015
  70. Finnegan YE, Howarth D, Minihane AM, Kew S, Miller GJ, Calder PC, et al. Plant and marine derived (n-3) polyunsaturated fatty acids do not affect blood coagulation and fibrinolytic factors in moderately hyperlipidemic humans. J Nutr. 2003;133:2210–2213
  71. Levy J, Morris R, Hammersley M, Turner R. Discrimination, adjusted correlation, and equivalence of imprecise tests: application to glucose tolerance. Am J Physiol. 1999;276(2 Pt 1):E365–E375
  72. Wallace FA, Miles EA, Calder PC. Comparison of the effects of linseed oil and different doses of fish oil on mononuclear cell function in healthy human subjects. Br J Nutr. 2003;89:679–689
  73. Chan DC, Watts GF, Barrett PH, Beilin LJ, Mori TA. Effect of atorvastatin and fish oil on plasma high-sensitivity C-reactive protein concentrations in individuals with visceral obesity. Clin Chem. 2002;48(6 Pt 1):877–883
  74. Geelen A, Brouwer IA, Schouten EG, Kluft C, Katan MB, Zock PL. Intake of n-3 fatty acids from fish does not lower serum concentrations of C-reactive protein in healthy subjects. Eur J Clin Nutr. 2004;58:1440–1442
  75. Madsen T, Christensen JH, Blom M, Schmidt EB. The effect of dietary n-3 fatty acids on serum concentrations of C-reactive protein: a dose-response study. Br J Nutr. 2003;89:517–522
  76. Grimble RF, Howell WM, O’Reilly G, Turner SJ, Markovic O, Hirrell S, et al. The ability of fish oil to suppress tumor necrosis factor alpha production by peripheral blood mononuclear cells in healthy men is associated with polymorphisms in genes that influence tumor necrosis factor alpha production. Am J Clin Nutr. 2002;76:454–459
  77. Feskens EJ, Kromhout D. Habitual dietary intake and glucose tolerance in euglycaemic men: the Zutphen Study. Int J Epidemiol. 1990;19:953–959
  78. Krebs JD, Browning LM, McLean N, Rothwell J, Mishra GD, Moore CS, et al. Additive benefits of long chain n-3 polyunsaturated fatty acids and weight-loss in the management of cardiovascular disease risk in overweight hyperinsulinaemic women. Int J Obes. 2006;(in press)
  79. Kris-Etherton PM, Harris WS, Appel LJ. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation. 2002;106:2747–2757

 This study was supported by funding from the United Kingdom Food Standards Agency (Project Number NO2026) and Medical Research Council.

PII: S0899-9007(06)00301-7

doi: 10.1016/j.nut.2006.07.005

Nutrition
Volume 22, Issue 10 , Pages 1012-1024 , October 2006

Article Tools

* Image Usage & Resolution