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High intake of fatty fish, but not of lean fish, improved postprandial glucose regulation and increased the n-3 PUFA content in the leucocyte membrane in healthy overweight adults: a randomised trial

  • Anita Helland (a1), Marianne Bratlie (a1), Ingrid V. Hagen (a1), Svein A. Mjøs (a2) (a3), Steinar Sørnes (a4), Alfred Ingvar Halstensen (a4), Karl A. Brokstad (a5), Harald Sveier (a6), Grethe Rosenlund (a7), Gunnar Mellgren (a4) (a8) and Oddrun A. Gudbrandsen (a1)...
Abstract
Abstract

The prevalence of type 2 diabetes (T2D) is low in populations with a high fish intake; however prospective studies with fish intake have shown positive, negative or no association between fish intake and the risk for T2D. The aim of this study was to investigate the effects of high intake of lean or fatty fish on glucose tolerance, leucocyte membrane fatty acid composition and leucocyte function in overweight/obese adults. In this randomised clinical trial, sixty-eight healthy overweight/obese participants consumed 750 g/week of either lean or fatty fish as dinners, or were instructed to continue their normal eating habits but to avoid fish intake (control group), for 8 weeks. Energy and macronutrient intake and physical activity were not changed within the groups during the study period. High intake of fatty fish, but not of lean fish, significantly improved glucose regulation 120 min postprandially (P=0·012), but did not affect fasting glucose concentration. A smaller increase in fasting to 120 min postprandial insulin C-peptide concentration was seen after fatty fish intake (P=0·012). Lean fish increased the DHA content in leucocyte membranes (P=0·010), and fatty fish increased the total content of n-3 PUFA (P=0·00016) and reduced the content of n-6 PUFA (P=0·00057) in leucocyte membranes. Lean and fatty fish intake did not affect phagocytosis of bacteria ex vivo. The findings suggest that high intake of fatty fish, but not of lean fish, beneficially affected postprandial glucose regulation in overweight/obese adults, and may therefore prevent or delay the development of T2D in this population.

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* Corresponding author: O. A. Gudbrandsen, fax +47 55975890, email oddrun.gudbrandsen@k1.uib.no
References
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1. Trayhurn P (2005) The biology of obesity. Proc Nutr Soc 64, 3138.
2. Festa A, D’Agostino R Jr, Williams K, et al. (2001) The relation of body fat mass and distribution to markers of chronic inflammation. Int J Obes Relat Metab Disord 25, 14071415.
3. Pradhan AD, Manson JE, Rifai N, et al. (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286, 327334.
4. Lolmede K, Duffaut C, Zakaroff-Girard A, et al. (2011) Immune cells in adipose tissue: key players in metabolic disorders. Diabetes Metab 37, 283290.
5. Calder PC (2008) The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot Essent Fatty Acids 79, 101108.
6. Kromann N & Green A (1980) Epidemiological studies in the Upernavik district, Greenland. Incidence of some chronic diseases 1950–1974. Acta Med Scand 208, 401406.
7. Feskens EJ, Bowles CH & Kromhout D (1991) Inverse association between fish intake and risk of glucose intolerance in normoglycemic elderly men and women. Diabetes Care 14, 935941.
8. Nkondjock A & Receveur O (2003) Fish-seafood consumption, obesity, and risk of type 2 diabetes: an ecological study. Diabetes Metab 29, 635642.
9. Kaushik M, Mozaffarian D, Spiegelman D, et al. (2009) Long-chain omega-3 fatty acids, fish intake, and the risk of type 2 diabetes mellitus. Am J Clin Nutr 90, 613620.
10. Djousse L, Gaziano JM, Buring JE, et al. (2011) Dietary omega-3 fatty acids and fish consumption and risk of type 2 diabetes. Am J Clin Nutr 93, 143150.
11. van Woudenbergh GJ, van Ballegooijen AJ, Kuijsten A, et al. (2009) Eating fish and risk of type 2 diabetes: a population-based, prospective follow-up study. Diabetes Care 32, 20212026.
12. Schulze MB, Manson JE, Willett WC, et al. (2003) Processed meat intake and incidence of Type 2 diabetes in younger and middle-aged women. Diabetologia 46, 14651473.
13. Villegas R, Xiang YB, Elasy T, et al. (2011) Fish, shellfish, and long-chain n-3 fatty acid consumption and risk of incident type 2 diabetes in middle-aged Chinese men and women. Am J Clin Nutr 94, 543551.
14. Zampelas A, Panagiotakos DB, Pitsavos C, et al. (2005) Fish consumption among healthy adults is associated with decreased levels of inflammatory markers related to cardiovascular disease: the ATTICA study. J Am Coll Cardiol 46, 120124.
15. Flock MR, Rogers CJ, Prabhu KS, et al. (2013) Immunometabolic role of long-chain omega-3 fatty acids in obesity-induced inflammation. Diabetes Metab Res Rev 29, 431445.
16. Duntas LH (2009) Selenium and inflammation: underlying anti-inflammatory mechanisms. Horm Metab Res 41, 443447.
17. Schuller-Levis GB & Park E (2003) Taurine: new implications for an old amino acid. FEMS Microbiol Lett 226, 195202.
18. Ouellet V, Weisnagel SJ, Marois J, et al. (2008) Dietary cod protein reduces plasma C-reactive protein in insulin-resistant men and women. J Nutr 138, 23862391.
19. Pilon G, Ruzzin J, Rioux LE, et al. (2011) Differential effects of various fish proteins in altering body weight, adiposity, inflammatory status, and insulin sensitivity in high-fat-fed rats. Metabolism 60, 11221130.
20. Hagen IV, Helland A, Bratlie M, et al. (2016) High intake of fatty fish, but not of lean fish, affects serum concentrations of TAG and HDL-cholesterol in healthy, normal-weight adults: a randomised trial. Br J Nutr 116, 648657.
21. Nordisk Metodikkomite for Næringsmidler (2003) Nitrogen. Determination in Foods and Feeds According to Kjeldahl. Method No. 6, 4th ed. Oslo, Norway: NMKL.
22. Nordisk Metodikkomite for Næringsmidler (1991) Moisture and Ash. Gravimetric Determination in Meat and Meat Products. Method No. 23, 3rd ed. Oslo, Norway: NMKL.
23. Grahl-Nielsen O & Barnung T (1985) Variations in the fatty acid profile of marine animals caused by environmental and developmental changes. Mar Environ Res 17, 218221.
24. Lefebvre PJ & Luyckx AS (1976) The breakfast tolerance test: a return to physiology. Diabete Metab 2, 15.
25. The Norwegian Food Safety Authority, the Directorate for Health and the Department of Nutrition at the University of Oslo (2010) Mat på Data (Food Data). http://matportalen.no/Emner/matpadata (accessed February 2010).
26. Lehmann AK, Sornes S & Halstensen A (2000) Phagocytosis: measurement by flow cytometry. J Immunol Methods 243, 229242.
27. Meier S, Mjøs SA, Joensen H, et al. (2006) Validation of a one-step extraction/methylation method for determination of fatty acids and cholesterol in marine tissues. J Chromatogr A 1104, 291298.
28. Sciotto C & Mjøs SA (2012) Trans isomers of EPA and DHA in omega-3 products on the European market. Lipids 47, 659667.
29. Wasta Z & Mjøs SA (2013) A database of chromatographic properties and mass spectra of fatty acid methyl esters from omega-3 products. J Chromatogr A 1299, 94102.
30. Naess A, Stenhaug Kilhus K, Nystad TW, et al. (2006) Linezolid and human polymorphonuclear leukocyte function. Chemotherapy 52, 122124.
31. Vikøren LA, Nygard OK, Lied E, et al. (2013) A randomised study on the effects of fish protein supplement on glucose tolerance, lipids and body composition in overweight adults. Br J Nutr 109, 648657.
32. Streiner DL (2015) Best (but oft-forgotten) practices: the multiple problems of multiplicity-whether and how to correct for many statistical tests. Am J Clin Nutr 102, 721728.
33. Patel PS, Forouhi NG, Kuijsten A, et al. (2012) The prospective association between total and type of fish intake and type 2 diabetes in 8 European countries: EPIC-InterAct Study. Am J Clin Nutr 95, 14451453.
34. Mori TA, Bao DQ, Burke V, et al. (1999) 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 70, 817825.
35. Ouellet V, Marois J, Weisnagel SJ, et al. (2007) Dietary cod protein improves insulin sensitivity in insulin-resistant men and women: a randomized controlled trial. Diabetes Care 30, 28162821.
36. Madani Z, Louchami K, Sener A, et al. (2012) Dietary sardine protein lowers insulin resistance, leptin and TNF-alpha and beneficially affects adipose tissue oxidative stress in rats with fructose-induced metabolic syndrome. Int J Mol Med 29, 311318.
37. Lavigne C, Marette A & Jacques H (2000) Cod and soy proteins compared with casein improve glucose tolerance and insulin sensitivity in rats. Am J Physiol Endocrinol Metab 278, E491E500.
38. Lavigne C, Tremblay F, Asselin G, et al. (2001) Prevention of skeletal muscle insulin resistance by dietary cod protein in high fat-fed rats. Am J Physiol Endocrinol Metab 281, E62E71.
39. Drotningsvik A, Mjøs SA, Høgøy I, et al. (2015) A low dietary intake of cod protein is sufficient to increase growth, improve serum and tissue fatty acid compositions, and lower serum postprandial glucose and fasting non-esterified fatty acid concentrations in obese Zucker fa/fa rats. Eur J Nutr 54, 11511160.
40. Drotningsvik A, Mjøs SA, Pampanin DM, et al. (2016) Dietary fish protein hydrolysates containing bioactive motifs affect serum and adipose tissue fatty acid compositions, serum lipids, postprandial glucose regulation and growth in obese Zucker fa/fa rats. Br J Nutr 116, 13361345.
41. Bhathena SJ, Berlin E, Judd JT, et al. (1991) Effects of omega 3 fatty acids and vitamin E on hormones involved in carbohydrate and lipid metabolism in men. Am J Clin Nutr 54, 684688.
42. Kromhout D & de Goede J (2014) Update on cardiometabolic health effects of omega-3 fatty acids. Curr Opin Lipidol 25, 8590.
43. Glauber H, Wallace P, Griver K, et al. (1988) Adverse metabolic effect of omega-3 fatty acids in non-insulin-dependent diabetes mellitus. Ann Intern Med 108, 663668.
44. Popp-Snijders C, Schouten JA, Heine RJ, et al. (1987) Dietary supplementation of omega-3 polyunsaturated fatty acids improves insulin sensitivity in non-insulin-dependent diabetes. Diabetes Res 4, 141147.
45. Lara JJ, Economou M, Wallace AM, et al. (2007) Benefits of salmon eating on traditional and novel vascular risk factors in young, non-obese healthy subjects. Atherosclerosis 193, 213221.
46. Calder PC (2007) Immunomodulation by omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids 77, 327335.
47. Lamas O, Marti A & Martinez JA (2002) Obesity and immunocompetence. Eur J Clin Nutr 56, Suppl. 3, S42S45.
48. Milner JJ & Beck MA (2012) The impact of obesity on the immune response to infection. Proc Nutr Soc 71, 298306.
49. Antuna-Puente B, Feve B, Fellahi S, et al. (2008) Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab 34, 211.
50. Calder PC, Ahluwalia N, Albers R, et al. (2013) A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr 109, Suppl. 1, S1S34.
51. Kalupahana NS, Moustaid-Moussa N & Claycombe KJ (2012) Immunity as a link between obesity and insulin resistance. Mol Aspects Med 33, 2634.
52. He K (2009) Fish, long-chain omega-3 polyunsaturated fatty acids and prevention of cardiovascular disease – eat fish or take fish oil supplement? Prog Cardiovasc Dis 52, 95114.
53. van Bussel BC, Henry RM, Schalkwijk CG, et al. (2011) Fish consumption in healthy adults is associated with decreased circulating biomarkers of endothelial dysfunction and inflammation during a 6-year follow-up. J Nutr 141, 17191725.
54. Pot GK, Geelen A, Majsak-Newman G, et al. (2010) Increased consumption of fatty and lean fish reduces serum C-reactive protein concentrations but not inflammation markers in feces and in colonic biopsies. J Nutr 140, 371376.
55. Smith KM, Barraj LM, Kantor M, et al. (2009) Relationship between fish intake, n-3 fatty acids, mercury and risk markers of CHD (National Health and Nutrition Examination Survey 1999–2002). Public Health Nutr 12, 12611269.
56. Lindqvist HM, Langkilde AM, Undeland I, et al. (2009) Herring (Clupea harengus) intake influences lipoproteins but not inflammatory and oxidation markers in overweight men. Br J Nutr 101, 383390.
57. Meydani SN, Endres S, Woods MM, et al. (1991) Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women. J Nutr 121, 547555.
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