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Acute effects of meal fatty acids on postprandial NEFA, glucose and apo E response: implications for insulin sensitivity and lipoprotein regulation?

Published online by Cambridge University Press:  08 March 2007

Kim G. Jackson*
Affiliation:
Hugh Sinclair Unit of Human Nutrition, School of Food Biosciences, University of Reading, Reading, RG6 6AP, UK
Emma J. Wolstencroft
Affiliation:
Hugh Sinclair Unit of Human Nutrition, School of Food Biosciences, University of Reading, Reading, RG6 6AP, UK
Paul A. Bateman
Affiliation:
Hugh Sinclair Unit of Human Nutrition, School of Food Biosciences, University of Reading, Reading, RG6 6AP, UK
Parveen Yaqoob
Affiliation:
Hugh Sinclair Unit of Human Nutrition, School of Food Biosciences, University of Reading, Reading, RG6 6AP, UK
Christine M. Williams
Affiliation:
Hugh Sinclair Unit of Human Nutrition, School of Food Biosciences, University of Reading, Reading, RG6 6AP, UK
*
*Corresponding author: Dr Kim Jackson, fax +44 (0) 118 931 0080, email [email protected]
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Abstract

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Our aim was to determine whether meal fatty acids influence insulin and glucose responses to mixed meals and whether these effects can be explained by variations in postprandial NEFA and Apo, which regulate the metabolism of triacylglycerol-rich lipoproteins (Apo C and E). A single-blind crossover study examined the effects of single meals enriched in saturated fatty acids SFA), n-6 PUFA and MUFA on plasma metabolite and insulin responses. The triacylglycerol response following the PUFA meal showed a lower net incremental area under the curve than following the SFA and MUFA meals (P<0·007). Compared with the SFA meal, the PUFA meal showed a lower net incremental area under the curve for the NEFA response from initial suppression to the end of the postprandial period (180–480 min; P<0·02), and both PUFA and MUFA showed a lower net incremental glucose response (P<0·02), although insulin concentrations were similar between meals. The pattern of the Apo E response was also different following the SFA meal (P<0·02). There was a significant association between the net incremental NEFA (180–480 min) and glucose response (rs=0·409, P=0·025), and in multiple regression analysis the NEFA response accounted for 24 % of the variation in glucose response. Meal SFA have adverse effects on the postprandial glucose response that may be due to greater elevations in NEFA arising from differences in the metabolism of SFA- v. PUFA- and MUFA-rich lipoproteins. Elevated Apo E responses to high-SFA meals may have important implications for the hepatic metabolism of triacylglycerol-rich lipoproteins.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2005

References

Batal, R, Tremblay, M, Barrett, PHR, Jacques, H, Fredenrich, A, Mamer, O, Davignon, J & Cohn, JS (2000) Plasma kinetics of apo C-III and apo E in normolipidaemic and hypertriglyceridaemic subject. J Lipid Res 41, 706718.CrossRefGoogle Scholar
Beysen, C, Karpe, F, Fielding, A, Clark, A, Levy, JC & Frayn, KN (2002) Interaction between specific fatty acids, GLP-1 and insulin secretion in humans. Diabetologia 45, 15331541.Google ScholarPubMed
Blum, CB (1982) Dynamics of apolipoprotein E metabolism in humans. J Lipid Res 23, 13081316.CrossRefGoogle ScholarPubMed
Brouwer, CB, de Bruin, TWA, Jansen, H & Erkelens, DW (1993) Different clearance of intravenously administered olive oil and soybean emulsion: role of hepatic lipase. Am J Clin Nutr 57, 533539.CrossRefGoogle ScholarPubMed
Demacker, PNM, Reijnen, IGM, Katan, MB, Stuyt, PMJ & Stahlenhoef, AFH (1991) Increased removal of remnants of triglyceride-rich lipoproteins on a diet rich in polyunsaturated fatty acids. Eur J Clin Nutr 21, 197203.Google Scholar
Dresner, A, Laurent, D & Marcucci, M (1999) Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity. J Clin Invest 103, 253259.CrossRefGoogle ScholarPubMed
Edelstein, C & Scanu, M (1986) Precautionary measures for collecting blood destined for lipoprotein isolation. Methods Enzymol 128, 151155.CrossRefGoogle ScholarPubMed
Frayn, KN, Williams, CM & Arner, P (1996) Are increased plasma non-esterified fatty acid concentrations a risk marker for coronary heart disease and other chronic diseases?. Clin Sci 90, 243253.CrossRefGoogle ScholarPubMed
Gannon, MC, Nuttal, FQ, Westphal, SA, Neil, BJ & Seaquist, ER (1989) Effects of dose of ingested glucose on plasma metabolite and hormone responses in type II diabetes subjects. Diabetes Care 12, 544552.CrossRefGoogle Scholar
Gannon, MC, Nuttall, FQ, Westphal, SA & Seaquist, ER (1993) The effect of fat and carbohydrate on plasma glucose, insulin, c-peptide, and triglycerides in normal male subjects. J Am Coll Nutr 12, 3641.CrossRefGoogle ScholarPubMed
Gatti, E, Noe, D, Pazzucconi, F, Gianfranceschi, G, Porrini, M, Testolin, G & Sirtori, CR (1992) Differential effect of unsaturated oils and butter on blood glucose and insulin response to carbohydrate in normal volunteers. Eur J Clin Nutr 46, 161166.Google ScholarPubMed
Grill, V & Qvidstad, E (2000) Fatty acids and insulin secretion. Br J Nutr 83, S79S84.CrossRefGoogle ScholarPubMed
Hansen, PA, Han, DH, Marshall, BA, Nolte, LA, Chen, MM, Mueckler, M & Holloszy, JO (1998) A high fat diet impairs stimulation of glucose transport in muscle – functional evaluation of potential mechanisms. J Biol Chem 273, 2615726163.CrossRefGoogle ScholarPubMed
Holland, BA, Welch, AA, Unwin, ID, Buss, DH, Paul, AA & Southgate, DAT (1991) McCance and Widdowson's the Composition of Foods 5th ed. Cambridge Royal Society of Chemistry and Agriculture, Fisheries and FoodGoogle Scholar
Jackson, KG, Robertson, MD, Fielding, BA, Frayn, KN & Williams, CM (2002) Measurement of apolipoprotein B-48 in the Svedberg flotation rate (S f )>400, S f 60–400 and S f 20–60 lipoprotein fractions reveals novel findings with respect to the effects of dietary fatty acids on triglyceride-rich lipoproteins in postmenopausal women. Clin Sci 103, 227237.CrossRefGoogle Scholar
Jackson, KG, Robertson, MD, Fielding, BA, Frayn, KN & Williams, CM (2002b) Olive oil increases the number of triacylglycerol-rich chylomicron particles compared with other oils: an effect retained when a second standard meal is fed. Am J Clin Nutr 76, 942949.CrossRefGoogle Scholar
Jackson, KG, Wolstencroft, EJ, Bateman, PA, Yaqoob, P & Williams, CM (2005) Increased enrichment of triacylglycerol-rich lipoproteins with apolipoproteins E and C-III following saturated compared with unsaturated fatty acid-rich meals. Am J Clin Nutr 81, 2534.CrossRefGoogle Scholar
Joannic, J-L, Auboiron, S, Raison, J, Basdevant, A, Bornet, F, Guy-Grand, B (1997) How the degree of unsaturation of dietary fatty acids influences the glucose and insulin responses to different carbohydrates in mixed meals. Am J Clin Nutr 65, 14271433.CrossRefGoogle ScholarPubMed
Jong, MC, Hofker, MH & Havekas, LM (1999) Role of apoC in lipoprotein metabolism. Functional differences between apo C1, apo C2 and apo C3. Arterioscler Thromb Vasc Biol 19, 472484.CrossRefGoogle Scholar
Kraegen, E, Cooney, G, Ye, J-M & Furler, S (2002) Peroxisome proliferator activated receptors, fatty acids and muscle insulin resistance. J Roy Soc Med 95, Suppl.1422.Google ScholarPubMed
Lovejoy, JC, Champagne, CM, Smith, SR, DeLany, JP, Bray, GA, Lefevre, M, Denkins, YM & Rood, JC (2001) Relationship of dietary fat and serum cholesterol ester and phospholipid fatty acids to markers of insulin resistance in men and women with a range of glucose tolerance. Metabolism 50, 8692.CrossRefGoogle ScholarPubMed
Macintosh, CG, Holt, SHA, Brand-Miller, JC (2003) The degree of fat saturation does not alter glycemic, insulinemic or satiety responses to a starchy staple in healthy men. J Nutr 133, 25772580.CrossRefGoogle ScholarPubMed
Matthews, DR (1988) Time series analysis in endocrinology. Acta Paediatr Scand 347, 5562.Google ScholarPubMed
Mekki, N, Charbonnier, M, Borel, P, Leonardi, J, Juhel, C, Portugal, H & Lairon, D (2002) Butter differs from olive oil and sunflower oil in its effects on postprandial lipemia and triacylglycerol-rich lipoproteins after single mixed meals in healthy young men. J Nutr 132, 36423649.CrossRefGoogle ScholarPubMed
Mero, N, Syvanne, M, Rosseneu, M, Labeur, C, Hilden, H & Taskinen, M-R (1998) Comparison of three fatty meals in healthy normolipidaemic men: high post-prandial retinyl ester response to soybean oil. Eur J Clin Invest 28, 407415.CrossRefGoogle ScholarPubMed
Oakes, ND, Bell, KS, Furler, SM, Camilleri, S, Saha, AK, Ruderman, NB, Chisolm, DJ & Kraegan, EW (1997) Diet induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise – parallel relationship between insulin stimulation of glucose uptake and suppression of long chain fatty acyl-CoA. Diabetes 46, 20222028.CrossRefGoogle ScholarPubMed
Pedersen, A, Marckmann, P & Sanstrom, B (1999) Postprandial lipoprotein, glucose and insulin responses after two consecutive meals containing rapeseed oil, sunflower or palm oil with or without glucose at the first meal. Br J Nutr 82, 97104.CrossRefGoogle ScholarPubMed
Petersen, KF & Shulman, GI (2002) Pathogenesis of skeletal muscle insulin resistance in type 2 diabetes mellitus. Am J Cardio 90 11G – 18GCrossRefGoogle ScholarPubMed
Randle, PJ, Garland, PB, Hales, CN & Newsholme, EA (1963) The glucose fatty acid cycle: its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet i, 785789.CrossRefGoogle Scholar
Robertson, MD, Jackson, KG, Fielding, BA, Williams, CM & Frayn, KN (2002) Acute effects of meal fatty acid composition on insulin sensitivity in healthy post-menopausal women. Br J Nutr 88, 635640.CrossRefGoogle ScholarPubMed
Roche, HM, Zampelas, A, Jackson, KG, Williams, CM & Gibney, MJ (1998) The effect of test meal monounsaturated fatty acid: saturated fatty acid ration on postprandial lipid metabolism. Br J Nutr 79, 419424.CrossRefGoogle Scholar
Roden, M, Perseghin, G, Petersen, KF, Hwang, JW, Cline, GW, Gerow, K, Rothman, DL & Shulman, GI (1996) The roles of insulin and glucagons in the regulation of hepatic glycogen synthesis and turnover in humans. J Clin Invest 97, 642648.CrossRefGoogle ScholarPubMed
Sanders, TAB, de Grassi, T, Miller, GJ & Morrissey, JH (2000) Influence of fatty acid chain length and cis/trans isomerisation on postprandial lipaemia and factor VII in healthy subjects (postprandial lipids and factor VII). Atherosclerosis 149, 413420.CrossRefGoogle ScholarPubMed
Storlien, LH, Baur, LA, Kriketos, AD, Pan, DA, Cooney, GJ, Jenkins, AB, Calvert, GD & Campbell, LV (1996) Dietary fats and insulin action. Diabetologia 39, 621631.CrossRefGoogle ScholarPubMed
Storlien, LH, Kriketos, AD, Calvert, GD, Baur, LA & Jenkins, AB (1997) Fatty acids, triglycerides and syndromes of insulin resistance. Prostaglandins Leukot Essent Fatty Acids 57, 379385.CrossRefGoogle ScholarPubMed
Tholstrup, T, Sandstrom, B, Bysted, A & Holmer, G (2001) Effect of 6 dietary fatty acids on the postprandial lipid profile, plasma fatty acids, lipoprotein lipase, and cholesterol ester transfer activities in healthy young men. Am J Clin Nutr 73, 198208.CrossRefGoogle ScholarPubMed
Thomson, C, Rasmussen, O, Lousen, T, Holst, JJ, Fenselau, S, Schrezenmeir, J & Hermansen, K (1999) Differential effects of saturated and monounsaturated fatty acids on postprandial lipaemia and incretin responses in healthy subjects. Am J Clin Nutr 69, 11351143.CrossRefGoogle Scholar
Vessby, B, Uusitupa, M & Hermansen, K (2001) Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU study. Diabetologia 44, 312319.CrossRefGoogle ScholarPubMed
Weintraub, MS, Zechner, R, Brown, A, Eisenberg, S & Breslow, JL (1988) Dietary polyunsaturated fats of the W-6 and W-3 series reduce postprandial lipoprotein levels. Chronic and acute effects of fat saturation on postprandial lipoprotein metabolism. J Clin Invest 82, 18841893.CrossRefGoogle ScholarPubMed
Welch, IM, Bruce, C, Hill, SE & Read, NW (1987) Duodenal and ileal lipid suppresses postprandial blood glucose and insulin responses in man: possible implications for the dietary management of diabetes mellitus. Clin Sci 72, 209216.CrossRefGoogle ScholarPubMed
Williams, CM (1997) Postprandial lipid metabolism: effects of dietary fatty acids. Proc Nutr Soc 56, 679692.CrossRefGoogle ScholarPubMed
Wolever, TMS (2004) Effect of blood sampling schedule and method of calculating the area under the curve on validity and precision of glycaemic index values. Br J Nutr 91, 295300.CrossRefGoogle ScholarPubMed
Zampelas, A, Murphy, M, Morgan, LM & Williams, CM (1994) Postprandial lipoprotein lipase, insulin and gastric inhibitory polypeptide responses to test meals of different fatty acid composition: Comparison of saturated, n-6 and n-3 polyunsaturated fatty acids. Eur J Clin Nutr 48, 849858.Google ScholarPubMed