Skip to main content
Top
Published in: European Journal of Nutrition 6/2017

Open Access 01-09-2017 | Original Contribution

Circulating linoleic acid and alpha-linolenic acid and glucose metabolism: the Hoorn Study

Authors: Mieke Cabout, Marjan Alssema, Giel Nijpels, Coen D. A. Stehouwer, Peter L. Zock, Ingeborg A. Brouwer, Amany K. Elshorbagy, Helga Refsum, Jacqueline M. Dekker

Published in: European Journal of Nutrition | Issue 6/2017

Login to get access

Abstract

Purpose

Data on the relation between linoleic acid (LA) and alpha-linolenic acid (ALA) and type 2 diabetes mellitus (T2DM) risk are scarce and inconsistent. The aim of this study was to investigate the association of serum LA and ALA with fasting and 2 h post-load plasma glucose and glycated hemoglobin (HbA1c).

Method

This study included 667 participants from third examination (2000) of the population-based Hoorn study in which individuals with glucose intolerance were overrepresented. Fatty acid profiles in serum total lipids were measured at baseline, in 2000. Diabetes risk markers were measured at baseline and follow-up in 2008. Linear regression models were used in cross-sectional and prospective analyses.

Results

In cross-sectional analyses (n = 667), serum LA was inversely associated with plasma glucose, both in fasting conditions (B = −0.024 [−0.045, −0.002]) and 2 h after glucose tolerance test (B = −0.099 [−0.158, −0.039]), but not with HbA1c (B = 0.000 [−0.014, 0.013]), after adjustment for relevant factors. In prospective analyses (n = 257), serum LA was not associated with fasting (B = 0.003 [−0.019, 0.025]) or post-load glucose (B = −0.026 [−0.100, 0.049]). Furthermore, no significant associations were found between serum ALA and glucose metabolism in cross-sectional or prospective analyses.

Conclusions

In this study, serum LA was inversely associated with fasting and post-load glucose in cross-sectional, but not in prospective analyses. Further studies are needed to elucidate the exact role of serum LA and ALA levels and dietary polyunsaturated fatty acids in glucose metabolism.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mensink RP, Zock PL, Kester AD, Katan MB (2003) Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled trials. Am J Clin Nutr 77:1146–1155 Mensink RP, Zock PL, Kester AD, Katan MB (2003) Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled trials. Am J Clin Nutr 77:1146–1155
2.
go back to reference Farvid MS, Ding M, Pan A, Sun Q, Chiuve SE, Steffen LM, Willett WC, Hu FB (2014) Dietary linoleic acid and risk of coronary heart disease: a systematic review and meta-analysis of prospective cohort studies. Circulation 130:1568–1578CrossRef Farvid MS, Ding M, Pan A, Sun Q, Chiuve SE, Steffen LM, Willett WC, Hu FB (2014) Dietary linoleic acid and risk of coronary heart disease: a systematic review and meta-analysis of prospective cohort studies. Circulation 130:1568–1578CrossRef
4.
go back to reference Perk J, De BG, Gohlke H, Graham I, Reiner Z, Verschuren M, Albus C, Benlian P, Boysen G, Cifkova R, Deaton C, Ebrahim S, Fisher M, Germano G, Hobbs R, Hoes A, Karadeniz S, Mezzani A, Prescott E, Ryden L, Scherer M, Syvanne M, Scholte op Reimer WJ, Vrints C, Wood D, Zamorano JL, Zannad F (2012) European guidelines on cardiovascular disease prevention in clinical practice (version 2012). The Fifth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of nine societies and by invited experts). Eur Heart J 33:1635–1701CrossRef Perk J, De BG, Gohlke H, Graham I, Reiner Z, Verschuren M, Albus C, Benlian P, Boysen G, Cifkova R, Deaton C, Ebrahim S, Fisher M, Germano G, Hobbs R, Hoes A, Karadeniz S, Mezzani A, Prescott E, Ryden L, Scherer M, Syvanne M, Scholte op Reimer WJ, Vrints C, Wood D, Zamorano JL, Zannad F (2012) European guidelines on cardiovascular disease prevention in clinical practice (version 2012). The Fifth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of nine societies and by invited experts). Eur Heart J 33:1635–1701CrossRef
5.
go back to reference Schwab U, Lauritzen L, Tholstrup T, Haldorssoni T, Riserus U, Uusitupa M, Becker W (2014) Effect of the amount and type of dietary fat on cardiometabolic risk factors and risk of developing type 2 diabetes, cardiovascular diseases, and cancer: a systematic review. Food Nutr Res 58:25145. doi:10.3402/fnr.v58.25145 CrossRef Schwab U, Lauritzen L, Tholstrup T, Haldorssoni T, Riserus U, Uusitupa M, Becker W (2014) Effect of the amount and type of dietary fat on cardiometabolic risk factors and risk of developing type 2 diabetes, cardiovascular diseases, and cancer: a systematic review. Food Nutr Res 58:25145. doi:10.​3402/​fnr.​v58.​25145 CrossRef
7.
go back to reference Food and Agriculture Organization of the United Nations. FAO report of an expert consultation on fats and fatty acids in human nutrition. ISSN 0254 4725 FAO Food and Nutrition Paper 91. 2010. Rome, Italy 2010 Food and Agriculture Organization of the United Nations. FAO report of an expert consultation on fats and fatty acids in human nutrition. ISSN 0254 4725 FAO Food and Nutrition Paper 91. 2010. Rome, Italy 2010
8.
go back to reference Meyer KA, Kushi LH, Jacobs DR Jr, Folsom AR (2001) Dietary fat and incidence of type 2 diabetes in older Iowa women. Diabetes Care 24:1528–1535CrossRef Meyer KA, Kushi LH, Jacobs DR Jr, Folsom AR (2001) Dietary fat and incidence of type 2 diabetes in older Iowa women. Diabetes Care 24:1528–1535CrossRef
9.
go back to reference Salmeron J, Hu FB, Manson JE, Stampfer MJ, Colditz GA, Rimm EB, Willett WC (2001) Dietary fat intake and risk of type 2 diabetes in women. Am J Clin Nutr 73:1019–1026 Salmeron J, Hu FB, Manson JE, Stampfer MJ, Colditz GA, Rimm EB, Willett WC (2001) Dietary fat intake and risk of type 2 diabetes in women. Am J Clin Nutr 73:1019–1026
10.
go back to reference Harding AH, Day NE, Khaw KT, Bingham S, Luben R, Welsh A, Wareham NJ (2004) Dietary fat and the risk of clinical type 2 diabetes: the European prospective investigation of Cancer-Norfolk study. Am J Epidemiol 159:73–82CrossRef Harding AH, Day NE, Khaw KT, Bingham S, Luben R, Welsh A, Wareham NJ (2004) Dietary fat and the risk of clinical type 2 diabetes: the European prospective investigation of Cancer-Norfolk study. Am J Epidemiol 159:73–82CrossRef
11.
go back to reference Patel PS, Sharp SJ, Jansen E, Luben RN, Khaw KT, Wareham NJ, Forouhi NG (2010) Fatty acids measured in plasma and erythrocyte-membrane phospholipids and derived by food-frequency questionnaire and the risk of new-onset type 2 diabetes: a pilot study in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk cohort. Am J Clin Nutr 92:1214–1222CrossRef Patel PS, Sharp SJ, Jansen E, Luben RN, Khaw KT, Wareham NJ, Forouhi NG (2010) Fatty acids measured in plasma and erythrocyte-membrane phospholipids and derived by food-frequency questionnaire and the risk of new-onset type 2 diabetes: a pilot study in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk cohort. Am J Clin Nutr 92:1214–1222CrossRef
12.
go back to reference van Dam RM, Willett WC, Rimm EB, Stampfer MJ, Hu FB (2002) Dietary fat and meat intake in relation to risk of type 2 diabetes in men. Diabetes Care 25:417–424CrossRef van Dam RM, Willett WC, Rimm EB, Stampfer MJ, Hu FB (2002) Dietary fat and meat intake in relation to risk of type 2 diabetes in men. Diabetes Care 25:417–424CrossRef
13.
go back to reference Kroger J, Zietemann V, Enzenbach C, Weikert C, Jansen EH, Doring F, Joost HG, Boeing H, Schulze MB (2011) Erythrocyte membrane phospholipid fatty acids, desaturase activity, and dietary fatty acids in relation to risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Am J Clin Nutr 93:127–142CrossRef Kroger J, Zietemann V, Enzenbach C, Weikert C, Jansen EH, Doring F, Joost HG, Boeing H, Schulze MB (2011) Erythrocyte membrane phospholipid fatty acids, desaturase activity, and dietary fatty acids in relation to risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Am J Clin Nutr 93:127–142CrossRef
14.
go back to reference Hodge AM, English DR, O’Dea K, Sinclair AJ, Makrides M, Gibson RA, Giles GG (2007) Plasma phospholipid and dietary fatty acids as predictors of type 2 diabetes: interpreting the role of linoleic acid. Am J Clin Nutr 86:189–197 Hodge AM, English DR, O’Dea K, Sinclair AJ, Makrides M, Gibson RA, Giles GG (2007) Plasma phospholipid and dietary fatty acids as predictors of type 2 diabetes: interpreting the role of linoleic acid. Am J Clin Nutr 86:189–197
15.
go back to reference Voss S, Kroke A, Klipstein-Grobusch K, Boeing H (1998) Is macronutrient composition of dietary intake data affected by underreporting? Results from the EPIC-Potsdam Study. European Prospective Investigation into Cancer and Nutrition. Eur J Clin Nutr 52:119–126CrossRef Voss S, Kroke A, Klipstein-Grobusch K, Boeing H (1998) Is macronutrient composition of dietary intake data affected by underreporting? Results from the EPIC-Potsdam Study. European Prospective Investigation into Cancer and Nutrition. Eur J Clin Nutr 52:119–126CrossRef
16.
go back to reference Goris AH, Westerterp-Plantenga MS, Westerterp KR (2000) Undereating and underrecording of habitual food intake in obese men: selective underreporting of fat intake. Am J Clin Nutr 71:130–134 Goris AH, Westerterp-Plantenga MS, Westerterp KR (2000) Undereating and underrecording of habitual food intake in obese men: selective underreporting of fat intake. Am J Clin Nutr 71:130–134
17.
go back to reference Ma J, Folsom AR, Shahar E, Eckfeldt JH (1995) Plasma fatty acid composition as an indicator of habitual dietary fat intake in middle-aged adults. The Atherosclerosis Risk in Communities (ARIC) Study Investigators. Am J Clin Nutr 62:564–571 Ma J, Folsom AR, Shahar E, Eckfeldt JH (1995) Plasma fatty acid composition as an indicator of habitual dietary fat intake in middle-aged adults. The Atherosclerosis Risk in Communities (ARIC) Study Investigators. Am J Clin Nutr 62:564–571
18.
go back to reference Hodson L, Skeaff CM, Fielding BA (2008) Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Prog Lipid Res 47:348–380CrossRef Hodson L, Skeaff CM, Fielding BA (2008) Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Prog Lipid Res 47:348–380CrossRef
19.
go back to reference Lankinen MA, Stancakova A, Uusitupa M, Agren J, Pihlajamaki J, Kuusisto J, Schwab U, Laakso M (2015) Plasma fatty acids as predictors of glycaemia and type 2 diabetes. Diabetologia 58:2533–2544CrossRef Lankinen MA, Stancakova A, Uusitupa M, Agren J, Pihlajamaki J, Kuusisto J, Schwab U, Laakso M (2015) Plasma fatty acids as predictors of glycaemia and type 2 diabetes. Diabetologia 58:2533–2544CrossRef
20.
go back to reference Vessby B, Aro A, Skarfors E, Berglund L, Salminen I, Lithell H (1994) The risk to develop NIDDM is related to the fatty acid composition of the serum cholesterol esters. Diabetes 43:1353–1357CrossRef Vessby B, Aro A, Skarfors E, Berglund L, Salminen I, Lithell H (1994) The risk to develop NIDDM is related to the fatty acid composition of the serum cholesterol esters. Diabetes 43:1353–1357CrossRef
21.
go back to reference Wang L, Folsom AR, Zheng ZJ, Pankow JS, Eckfeldt JH (2003) Plasma fatty acid composition and incidence of diabetes in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) Study. Am J Clin Nutr 78:91–98 Wang L, Folsom AR, Zheng ZJ, Pankow JS, Eckfeldt JH (2003) Plasma fatty acid composition and incidence of diabetes in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) Study. Am J Clin Nutr 78:91–98
22.
go back to reference Mahendran Y, Agren J, Uusitupa M, Cederberg H, Vangipurapu J, Stancakova A, Schwab U, Kuusisto J, Laakso M (2014) Association of erythrocyte membrane fatty acids with changes in glycemia and risk of type 2 diabetes. Am J Clin Nutr 99:79–85CrossRef Mahendran Y, Agren J, Uusitupa M, Cederberg H, Vangipurapu J, Stancakova A, Schwab U, Kuusisto J, Laakso M (2014) Association of erythrocyte membrane fatty acids with changes in glycemia and risk of type 2 diabetes. Am J Clin Nutr 99:79–85CrossRef
23.
go back to reference Krachler B, Norberg M, Eriksson JW, Hallmans G, Johansson I, Vessby B, Weinehall L, Lindahl B (2008) Fatty acid profile of the erythrocyte membrane preceding development of type 2 diabetes mellitus. Nutr Metab Cardiovasc Dis 18:503–510CrossRef Krachler B, Norberg M, Eriksson JW, Hallmans G, Johansson I, Vessby B, Weinehall L, Lindahl B (2008) Fatty acid profile of the erythrocyte membrane preceding development of type 2 diabetes mellitus. Nutr Metab Cardiovasc Dis 18:503–510CrossRef
24.
go back to reference Wu JH, Micha R, Imamura F, Pan A, Biggs ML, Ajaz O, Djousse L, Hu FB, Mozaffarian D (2012) Omega-3 fatty acids and incident type 2 diabetes: a systematic review and meta-analysis. Br J Nutr 107(Suppl 2):S214–S227CrossRef Wu JH, Micha R, Imamura F, Pan A, Biggs ML, Ajaz O, Djousse L, Hu FB, Mozaffarian D (2012) Omega-3 fatty acids and incident type 2 diabetes: a systematic review and meta-analysis. Br J Nutr 107(Suppl 2):S214–S227CrossRef
25.
go back to reference Mooy JM, Grootenhuis PA, de Vries H, Valkenburg HA, Bouter LM, Kostense PJ, Heine RJ (1995) Prevalence and determinants of glucose intolerance in a Dutch Caucasian population. Hoorn stud. Diabetes Care 18:1270–1273CrossRef Mooy JM, Grootenhuis PA, de Vries H, Valkenburg HA, Bouter LM, Kostense PJ, Heine RJ (1995) Prevalence and determinants of glucose intolerance in a Dutch Caucasian population. Hoorn stud. Diabetes Care 18:1270–1273CrossRef
26.
go back to reference Bos G, Poortvliet MC, Scheffer PG, Dekker JM, Ocke MC, Nijpels G, Stehouwer CD, Bouter LM, Teerlink T, Heine RJ (2007) Dietary polyunsaturated fat intake is associated with low-density lipoprotein size, but not with susceptibility to oxidation in subjects with impaired glucose metabolism and type II diabetes: the Hoorn study. Eur J Clin Nutr 61:205–211CrossRef Bos G, Poortvliet MC, Scheffer PG, Dekker JM, Ocke MC, Nijpels G, Stehouwer CD, Bouter LM, Teerlink T, Heine RJ (2007) Dietary polyunsaturated fat intake is associated with low-density lipoprotein size, but not with susceptibility to oxidation in subjects with impaired glucose metabolism and type II diabetes: the Hoorn study. Eur J Clin Nutr 61:205–211CrossRef
27.
go back to reference Spijkerman AM, Dekker JM, Nijpels G, Adriaanse MC, Kostense PJ, Ruwaard D, Stehouwer CD, Bouter LM, Heine RJ (2003) Microvascular complications at time of diagnosis of type 2 diabetes are similar among diabetic patients detected by targeted screening and patients newly diagnosed in general practice: the Hoorn screening study. Diabetes Care 26:2604–2608CrossRef Spijkerman AM, Dekker JM, Nijpels G, Adriaanse MC, Kostense PJ, Ruwaard D, Stehouwer CD, Bouter LM, Heine RJ (2003) Microvascular complications at time of diagnosis of type 2 diabetes are similar among diabetic patients detected by targeted screening and patients newly diagnosed in general practice: the Hoorn screening study. Diabetes Care 26:2604–2608CrossRef
28.
go back to reference van den Hurk K, Alssema M, Kamp O, Henry RM, Stehouwer CD, Smulders YM, Nijpels G, Paulus WJ, Dekker JM (2012) Independent associations of glucose status and arterial stiffness with left ventricular diastolic dysfunction: an 8-year follow-up of the Hoorn study. Diabetes Care 35:1258–1264CrossRef van den Hurk K, Alssema M, Kamp O, Henry RM, Stehouwer CD, Smulders YM, Nijpels G, Paulus WJ, Dekker JM (2012) Independent associations of glucose status and arterial stiffness with left ventricular diastolic dysfunction: an 8-year follow-up of the Hoorn study. Diabetes Care 35:1258–1264CrossRef
29.
go back to reference Lapolla A, Mosca A, Fedele D (2011) The general use of glycated haemoglobin for the diagnosis of diabetes and other categories of glucose intolerance: still a long way to go. Nutr Metab Cardiovasc Dis 21:467–475CrossRef Lapolla A, Mosca A, Fedele D (2011) The general use of glycated haemoglobin for the diagnosis of diabetes and other categories of glucose intolerance: still a long way to go. Nutr Metab Cardiovasc Dis 21:467–475CrossRef
30.
go back to reference van den Berg E, Biessels GJ, Stehouwer CD, Kappelle LJ, Heine RJ, Nijpels G, Dekker JM (2010) Ten-year time course of risk factors for increased carotid intima-media thickness: the Hoorn Study. Eur J Cardiovasc Prev Rehabil 17:168–174CrossRef van den Berg E, Biessels GJ, Stehouwer CD, Kappelle LJ, Heine RJ, Nijpels G, Dekker JM (2010) Ten-year time course of risk factors for increased carotid intima-media thickness: the Hoorn Study. Eur J Cardiovasc Prev Rehabil 17:168–174CrossRef
33.
go back to reference Henry RM, Kostense PJ, Spijkerman AM, Dekker JM, Nijpels G, Heine RJ, Kamp O, Westerhof N, Bouter LM, Stehouwer CD (2003) Arterial stiffness increases with deteriorating glucose tolerance status: the Hoorn study. Circulation 107:2089–2095CrossRef Henry RM, Kostense PJ, Spijkerman AM, Dekker JM, Nijpels G, Heine RJ, Kamp O, Westerhof N, Bouter LM, Stehouwer CD (2003) Arterial stiffness increases with deteriorating glucose tolerance status: the Hoorn study. Circulation 107:2089–2095CrossRef
34.
go back to reference Wendel-Vos GC, Schuit AJ, Saris WH, Kromhout D (2003) Reproducibility and relative validity of the short questionnaire to assess health-enhancing physical activity. J Clin Epidemiol 56:1163–1169CrossRef Wendel-Vos GC, Schuit AJ, Saris WH, Kromhout D (2003) Reproducibility and relative validity of the short questionnaire to assess health-enhancing physical activity. J Clin Epidemiol 56:1163–1169CrossRef
35.
go back to reference Grootenhuis PA, Westenbrink S, Sie CM, de Neeling JN, Kok FJ, Bouter LM (1995) A semiquantitative food frequency questionnaire for use in epidemiologic research among the elderly: validation by comparison with dietary history. J Clin Epidemiol 48:859–868CrossRef Grootenhuis PA, Westenbrink S, Sie CM, de Neeling JN, Kok FJ, Bouter LM (1995) A semiquantitative food frequency questionnaire for use in epidemiologic research among the elderly: validation by comparison with dietary history. J Clin Epidemiol 48:859–868CrossRef
36.
go back to reference Voedingscentrum DHTN (2001) Dutch food composition database: NEVO. Bilthoven, The Netherlands Voedingscentrum DHTN (2001) Dutch food composition database: NEVO. Bilthoven, The Netherlands
37.
go back to reference Rosqvist F, Iggman D, Kullberg J, Cedernaes J, Johansson HE, Larsson A, Johansson L, Ahlstrom H, Arner P, Dahlman I, Riserus U (2014) Overfeeding polyunsaturated and saturated fat causes distinct effects on liver and visceral fat accumulation in humans. Diabetes 63:2356–2368CrossRef Rosqvist F, Iggman D, Kullberg J, Cedernaes J, Johansson HE, Larsson A, Johansson L, Ahlstrom H, Arner P, Dahlman I, Riserus U (2014) Overfeeding polyunsaturated and saturated fat causes distinct effects on liver and visceral fat accumulation in humans. Diabetes 63:2356–2368CrossRef
38.
go back to reference Pan A, Chen M, Chowdhury R, Wu JH, Sun Q, Campos H, Mozaffarian D, Hu FB (2012) Alpha-linolenic acid and risk of cardiovascular disease: a systematic review and meta-analysis. Am J Clin Nutr 96:1262–1273CrossRef Pan A, Chen M, Chowdhury R, Wu JH, Sun Q, Campos H, Mozaffarian D, Hu FB (2012) Alpha-linolenic acid and risk of cardiovascular disease: a systematic review and meta-analysis. Am J Clin Nutr 96:1262–1273CrossRef
39.
go back to reference 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 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
40.
go back to reference Field CJ, Ryan EA, Thomson AB, Clandinin MT (1990) Diet fat composition alters membrane phospholipid composition, insulin binding, and glucose metabolism in adipocytes from control and diabetic animals. J Biol Chem 265:11143–11150 Field CJ, Ryan EA, Thomson AB, Clandinin MT (1990) Diet fat composition alters membrane phospholipid composition, insulin binding, and glucose metabolism in adipocytes from control and diabetic animals. J Biol Chem 265:11143–11150
41.
go back to reference Summers LK, Fielding BA, Bradshaw HA, Ilic V, Beysen C, Clark ML, Moore NR, Frayn KN (2002) Substituting dietary saturated fat with polyunsaturated fat changes abdominal fat distribution and improves insulin sensitivity. Diabetologia 45:369–377CrossRef Summers LK, Fielding BA, Bradshaw HA, Ilic V, Beysen C, Clark ML, Moore NR, Frayn KN (2002) Substituting dietary saturated fat with polyunsaturated fat changes abdominal fat distribution and improves insulin sensitivity. Diabetologia 45:369–377CrossRef
42.
go back to reference DeFronzo RA, Tripathy D (2009) Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32(Suppl 2):S157–S163CrossRef DeFronzo RA, Tripathy D (2009) Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32(Suppl 2):S157–S163CrossRef
43.
go back to reference Taskinen MR (2003) LDL-cholesterol, HDL-cholesterol or triglycerides—Which is the culprit? Diabetes Res Clin Pract 61(Suppl 1):S19–S26CrossRef Taskinen MR (2003) LDL-cholesterol, HDL-cholesterol or triglycerides—Which is the culprit? Diabetes Res Clin Pract 61(Suppl 1):S19–S26CrossRef
44.
go back to reference Bjermo H, Iggman D, Kullberg J, Dahlman I, Johansson L, Persson L, Berglund J, Pulkki K, Basu S, Uusitupa M, Rudling M, Arner P, Cederholm T, Ahlstrom H, Riserus U (2012) Effects of n–6 PUFAs compared with SFAs on liver fat, lipoproteins, and inflammation in abdominal obesity: a randomized controlled trial. Am J Clin Nutr 95:1003–1012CrossRef Bjermo H, Iggman D, Kullberg J, Dahlman I, Johansson L, Persson L, Berglund J, Pulkki K, Basu S, Uusitupa M, Rudling M, Arner P, Cederholm T, Ahlstrom H, Riserus U (2012) Effects of n–6 PUFAs compared with SFAs on liver fat, lipoproteins, and inflammation in abdominal obesity: a randomized controlled trial. Am J Clin Nutr 95:1003–1012CrossRef
45.
go back to reference Nakamura MT, Nara TY (2004) Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 24:345–376CrossRef Nakamura MT, Nara TY (2004) Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 24:345–376CrossRef
46.
go back to reference Warensjo E, Riserus U, Vessby B (2005) Fatty acid composition of serum lipids predicts the development of the metabolic syndrome in men. Diabetologia 48:1999–2005CrossRef Warensjo E, Riserus U, Vessby B (2005) Fatty acid composition of serum lipids predicts the development of the metabolic syndrome in men. Diabetologia 48:1999–2005CrossRef
Metadata
Title
Circulating linoleic acid and alpha-linolenic acid and glucose metabolism: the Hoorn Study
Authors
Mieke Cabout
Marjan Alssema
Giel Nijpels
Coen D. A. Stehouwer
Peter L. Zock
Ingeborg A. Brouwer
Amany K. Elshorbagy
Helga Refsum
Jacqueline M. Dekker
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 6/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-016-1261-6

Other articles of this Issue 6/2017

European Journal of Nutrition 6/2017 Go to the issue