Skip to main content
Top
Published in: European Journal of Nutrition 1/2017

01-02-2017 | Original Contribution

Associations between intake of fish and n-3 long-chain polyunsaturated fatty acids and plasma metabolites related to the kynurenine pathway in patients with coronary artery disease

Authors: Therese Karlsson, Elin Strand, Jutta Dierkes, Christian A. Drevon, Jannike Øyen, Øivind Midttun, Per M. Ueland, Oddrun A. Gudbrandsen, Eva Ringdal Pedersen, Ottar Nygård

Published in: European Journal of Nutrition | Issue 1/2017

Login to get access

Abstract

Purpose

Enhanced tryptophan degradation via the kynurenine pathway has been related to several pathological conditions. However, little is known about the effect of diet on individual metabolites of this pathway. We investigated cross-sectional associations between reported intake of fish and omega-3 (n-3) long-chain PUFA (LC-PUFA) and plasma metabolites related to the kynurenine pathway.

Methods

Participants were 2324 individuals with coronary artery disease from the Western Norway B Vitamin Intervention Trial. Fish and n-3 LC-PUFA intakes were assessed using a food frequency questionnaire. Plasma concentrations of tryptophan, kynurenine, kynurenic acid, anthranilic acid, 3-hydroxykynurenine, xanthurenic acid, 3-hydroxyanthranilic acid, neopterin, and kynurenine-to-tryptophan ratio (KTR) were analyzed. Associations were investigated using partial Spearman’s rank correlations and multiple linear regressions.

Results

Median age at inclusion was 62 years (80 % males), and 84 % had stable angina pectoris. Intake of fatty fish and n-3 LC-PUFA was inversely associated with plasma 3-hydroxykynurenine. Consumption of total fish, lean fish, and n-3 LC-PUFA was inversely associated with plasma neopterin. Intake of total fish, fatty fish, and n-3 LC-PUFA was inversely associated with KTR. All these correlations were weak (ρ between −0.12 and −0.06, P < 0.01). In 306 patients with diabetes, lean fish intake was positively associated with plasma 3-hydroxyanthranilic acid (ρ = 0.22, P < 0.001, P for interaction = 0.01), and total fish intake was inversely associated with KTR (ρ = −0.17, P < 0.01, P for interaction = 0.02).

Conclusion

Fish intake was not an important determinant of individual metabolites in the kynurenine pathway. However, some correlations were stronger in patients with diabetes. The inverse associations of fish or n-3 LC-PUFA with neopterin and KTR may suggest a slightly lower IFN-γ-mediated immune activation with a higher intake.
Appendix
Available only for authorised users
Literature
2.
go back to reference Stevens CO, Henderson LM (1959) Riboflavin and hepatic kynurenine hydroxylase. J Biol Chem 234:1191–1194 Stevens CO, Henderson LM (1959) Riboflavin and hepatic kynurenine hydroxylase. J Biol Chem 234:1191–1194
3.
go back to reference Midttun O, Ulvik A, Ringdal Pedersen E, Ebbing M, Bleie O, Schartum-Hansen H, Nilsen RM, Nygard O, Ueland PM (2011) Low plasma vitamin B-6 status affects metabolism through the kynurenine pathway in cardiovascular patients with systemic inflammation. J Nutr 141:611–617. doi:10.3945/jn.110.133082 CrossRef Midttun O, Ulvik A, Ringdal Pedersen E, Ebbing M, Bleie O, Schartum-Hansen H, Nilsen RM, Nygard O, Ueland PM (2011) Low plasma vitamin B-6 status affects metabolism through the kynurenine pathway in cardiovascular patients with systemic inflammation. J Nutr 141:611–617. doi:10.​3945/​jn.​110.​133082 CrossRef
4.
go back to reference Schroecksnadel K, Frick B, Winkler C, Fuchs D (2006) Crucial role of interferon-gamma and stimulated macrophages in cardiovascular disease. Curr Vasc Pharmacol 4:205–213CrossRef Schroecksnadel K, Frick B, Winkler C, Fuchs D (2006) Crucial role of interferon-gamma and stimulated macrophages in cardiovascular disease. Curr Vasc Pharmacol 4:205–213CrossRef
6.
go back to reference Theofylaktopoulou D, Midttun O, Ulvik A, Ueland PM, Tell GS, Vollset SE, Nygard O, Eussen SJ (2013) A community-based study on determinants of circulating markers of cellular immune activation and kynurenines: the Hordaland Health Study. Clin Exp Immunol 173:121–130. doi:10.1111/cei.12092 CrossRef Theofylaktopoulou D, Midttun O, Ulvik A, Ueland PM, Tell GS, Vollset SE, Nygard O, Eussen SJ (2013) A community-based study on determinants of circulating markers of cellular immune activation and kynurenines: the Hordaland Health Study. Clin Exp Immunol 173:121–130. doi:10.​1111/​cei.​12092 CrossRef
7.
go back to reference Nilsen RM, Bjorke-Monsen AL, Midttun O, Nygard O, Pedersen ER, Ulvik A, Magnus P, Gjessing HK, Vollset SE, Ueland PM (2012) Maternal tryptophan and kynurenine pathway metabolites and risk of preeclampsia. Obstet Gynecol 119:1243–1250. doi:10.1097/AOG.0b013e318255004e CrossRef Nilsen RM, Bjorke-Monsen AL, Midttun O, Nygard O, Pedersen ER, Ulvik A, Magnus P, Gjessing HK, Vollset SE, Ueland PM (2012) Maternal tryptophan and kynurenine pathway metabolites and risk of preeclampsia. Obstet Gynecol 119:1243–1250. doi:10.​1097/​AOG.​0b013e318255004e​ CrossRef
8.
go back to reference Zuo H, Tell GS, Vollset SE, Ueland PM, Nygard O, Midttun O, Meyer K, Ulvik A, Eussen SJ (2014) Interferon-gamma-induced inflammatory markers and the risk of cancer: the Hordaland Health Study. Cancer 120:3370–3377. doi:10.1002/cncr.28869 CrossRef Zuo H, Tell GS, Vollset SE, Ueland PM, Nygard O, Midttun O, Meyer K, Ulvik A, Eussen SJ (2014) Interferon-gamma-induced inflammatory markers and the risk of cancer: the Hordaland Health Study. Cancer 120:3370–3377. doi:10.​1002/​cncr.​28869 CrossRef
9.
go back to reference Sulo G, Vollset SE, Nygard O, Midttun O, Ueland PM, Eussen SJ, Pedersen ER, Tell GS (2013) Neopterin and kynurenine-tryptophan ratio as predictors of coronary events in older adults, the Hordaland Health Study. Int J Cardiol 168:1435–1440. doi:10.1016/j.ijcard.2012.12.090 CrossRef Sulo G, Vollset SE, Nygard O, Midttun O, Ueland PM, Eussen SJ, Pedersen ER, Tell GS (2013) Neopterin and kynurenine-tryptophan ratio as predictors of coronary events in older adults, the Hordaland Health Study. Int J Cardiol 168:1435–1440. doi:10.​1016/​j.​ijcard.​2012.​12.​090 CrossRef
10.
11.
go back to reference Munipally PK, Agraharm SG, Valavala VK, Gundae S, Turlapati NR (2011) Evaluation of indoleamine 2,3-dioxygenase expression and kynurenine pathway metabolites levels in serum samples of diabetic retinopathy patients. Arch Physiol Biochem 117:254–258. doi:10.3109/13813455.2011.623705 CrossRef Munipally PK, Agraharm SG, Valavala VK, Gundae S, Turlapati NR (2011) Evaluation of indoleamine 2,3-dioxygenase expression and kynurenine pathway metabolites levels in serum samples of diabetic retinopathy patients. Arch Physiol Biochem 117:254–258. doi:10.​3109/​13813455.​2011.​623705 CrossRef
12.
go back to reference Pedersen ER, Tuseth N, Eussen SJ, Ueland PM, Strand E, Svingen GF, Midttun O, Meyer K, Mellgren G, Ulvik A, Nordrehaug JE, Nilsen DW, Nygard O (2015) Associations of plasma kynurenines with risk of acute myocardial infarction in patients with stable angina pectoris. Arterioscler Thromb Vasc Biol 35:455–462. doi:10.1161/ATVBAHA.114.304674 CrossRef Pedersen ER, Tuseth N, Eussen SJ, Ueland PM, Strand E, Svingen GF, Midttun O, Meyer K, Mellgren G, Ulvik A, Nordrehaug JE, Nilsen DW, Nygard O (2015) Associations of plasma kynurenines with risk of acute myocardial infarction in patients with stable angina pectoris. Arterioscler Thromb Vasc Biol 35:455–462. doi:10.​1161/​ATVBAHA.​114.​304674 CrossRef
16.
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:S214–S227. doi:10.1017/S0007114512001602 CrossRef 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:S214–S227. doi:10.​1017/​S000711451200160​2 CrossRef
17.
go back to reference Ebbing M, Bleie O, Ueland PM, Nordrehaug JE, Nilsen DW, Vollset SE, Refsum H, Pedersen EK, Nygard O (2008) Mortality and cardiovascular events in patients treated with homocysteine-lowering B vitamins after coronary angiography: a randomized controlled trial. JAMA 300:795–804. doi:10.1001/jama.300.7.795 CrossRef Ebbing M, Bleie O, Ueland PM, Nordrehaug JE, Nilsen DW, Vollset SE, Refsum H, Pedersen EK, Nygard O (2008) Mortality and cardiovascular events in patients treated with homocysteine-lowering B vitamins after coronary angiography: a randomized controlled trial. JAMA 300:795–804. doi:10.​1001/​jama.​300.​7.​795 CrossRef
18.
go back to reference Andersen LF, Solvoll K, Johansson LR, Salminen I, Aro A, Drevon CA (1999) Evaluation of a food frequency questionnaire with weighed records, fatty acids, and alpha-tocopherol in adipose tissue and serum. Am J Epidemiol 150:75–87CrossRef Andersen LF, Solvoll K, Johansson LR, Salminen I, Aro A, Drevon CA (1999) Evaluation of a food frequency questionnaire with weighed records, fatty acids, and alpha-tocopherol in adipose tissue and serum. Am J Epidemiol 150:75–87CrossRef
19.
go back to reference Nes M, Frost Andersen L, Solvoll K, Sandstad B, Hustvedt BE, Lovo A, Drevon CA (1992) Accuracy of a quantitative food frequency questionnaire applied in elderly Norwegian women. Eur J Clin Nutr 46:809–821 Nes M, Frost Andersen L, Solvoll K, Sandstad B, Hustvedt BE, Lovo A, Drevon CA (1992) Accuracy of a quantitative food frequency questionnaire applied in elderly Norwegian women. Eur J Clin Nutr 46:809–821
20.
go back to reference Den store matvaretabellen (1995) The Norwegian food composition table. National Nutrition Council and The Food Control Authority, Oslo (in Norwegian) Den store matvaretabellen (1995) The Norwegian food composition table. National Nutrition Council and The Food Control Authority, Oslo (in Norwegian)
21.
go back to reference Andersen LF, Solvoll K, Drevon CA (1996) Very-long-chain n-3 fatty acids as biomarkers for intake of fish and n-3 fatty acid concentrates. Am J Clin Nutr 64:305–311 Andersen LF, Solvoll K, Drevon CA (1996) Very-long-chain n-3 fatty acids as biomarkers for intake of fish and n-3 fatty acid concentrates. Am J Clin Nutr 64:305–311
22.
go back to reference Andersen LF, Veierod MB, Johansson L, Sakhi A, Solvoll K, Drevon CA (2005) Evaluation of three dietary assessment methods and serum biomarkers as measures of fruit and vegetable intake, using the method of triads. Br J Nutr 93:519–527CrossRef Andersen LF, Veierod MB, Johansson L, Sakhi A, Solvoll K, Drevon CA (2005) Evaluation of three dietary assessment methods and serum biomarkers as measures of fruit and vegetable intake, using the method of triads. Br J Nutr 93:519–527CrossRef
24.
go back to reference Strand E, Pedersen ER, Svingen GF, Schartum-Hansen H, Rebnord EW, Bjorndal B, Seifert R, Bohov P, Meyer K, Hiltunen JK, Nordrehaug JE, Nilsen DW, Berge RK, Nygard O (2013) Dietary intake of n-3 long-chain polyunsaturated fatty acids and risk of myocardial infarction in coronary artery disease patients with or without diabetes mellitus: a prospective cohort study. BMC Med 11:216. doi:10.1186/1741-7015-11-216 CrossRef Strand E, Pedersen ER, Svingen GF, Schartum-Hansen H, Rebnord EW, Bjorndal B, Seifert R, Bohov P, Meyer K, Hiltunen JK, Nordrehaug JE, Nilsen DW, Berge RK, Nygard O (2013) Dietary intake of n-3 long-chain polyunsaturated fatty acids and risk of myocardial infarction in coronary artery disease patients with or without diabetes mellitus: a prospective cohort study. BMC Med 11:216. doi:10.​1186/​1741-7015-11-216 CrossRef
25.
go back to reference Midttun O, Hustad S, Ueland PM (2009) Quantitative profiling of biomarkers related to B-vitamin status, tryptophan metabolism and inflammation in human plasma by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 23:1371–1379. doi:10.1002/rcm.4013 CrossRef Midttun O, Hustad S, Ueland PM (2009) Quantitative profiling of biomarkers related to B-vitamin status, tryptophan metabolism and inflammation in human plasma by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 23:1371–1379. doi:10.​1002/​rcm.​4013 CrossRef
26.
go back to reference Ueland PM, Midttun O, Windelberg A, Svardal A, Skalevik R, Hustad S (2007) Quantitative profiling of folate and one-carbon metabolism in large-scale epidemiological studies by mass spectrometry. Clin Chem Lab Med 45:1737–1745. doi:10.1515/CCLM.2007.339 CrossRef Ueland PM, Midttun O, Windelberg A, Svardal A, Skalevik R, Hustad S (2007) Quantitative profiling of folate and one-carbon metabolism in large-scale epidemiological studies by mass spectrometry. Clin Chem Lab Med 45:1737–1745. doi:10.​1515/​CCLM.​2007.​339 CrossRef
27.
28.
go back to reference Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S–1228S Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S–1228S
29.
go back to reference Hiratsuka C, Fukuwatari T, Sano M, Saito K, Sasaki S, Shibata K (2013) Supplementing healthy women with up to 5.0 g/d of l-tryptophan has no adverse effects. J Nutr 143:859–866. doi:10.3945/jn.112.173823 CrossRef Hiratsuka C, Fukuwatari T, Sano M, Saito K, Sasaki S, Shibata K (2013) Supplementing healthy women with up to 5.0 g/d of l-tryptophan has no adverse effects. J Nutr 143:859–866. doi:10.​3945/​jn.​112.​173823 CrossRef
33.
go back to reference Soyland E, Nenseter MS, Braathen L, Drevon CA (1993) Very long chain n-3 and n-6 polyunsaturated fatty acids inhibit proliferation of human T-lymphocytes in vitro. Eur J Clin Invest 23:112–121CrossRef Soyland E, Nenseter MS, Braathen L, Drevon CA (1993) Very long chain n-3 and n-6 polyunsaturated fatty acids inhibit proliferation of human T-lymphocytes in vitro. Eur J Clin Invest 23:112–121CrossRef
34.
go back to reference Schleithoff SS, Zittermann A, Tenderich G, Berthold HK, Stehle P, Koerfer R (2006) Vitamin D supplementation improves cytokine profiles in patients with congestive heart failure: a double-blind, randomized, placebo-controlled trial. Am J Clin Nutr 83:754–759 Schleithoff SS, Zittermann A, Tenderich G, Berthold HK, Stehle P, Koerfer R (2006) Vitamin D supplementation improves cytokine profiles in patients with congestive heart failure: a double-blind, randomized, placebo-controlled trial. Am J Clin Nutr 83:754–759
35.
go back to reference Gallai V, Sarchielli P, Trequattrini A, Franceschini M, Floridi A, Firenze C, Alberti A, Di Benedetto D, Stragliotto E (1995) 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 56:143–153CrossRef Gallai V, Sarchielli P, Trequattrini A, Franceschini M, Floridi A, Firenze C, Alberti A, Di Benedetto D, Stragliotto E (1995) 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 56:143–153CrossRef
36.
go back to reference Dawczynski C, Massey KA, Ness C, Kiehntopf M, Stepanow S, Platzer M, Grun M, Nicolaou A, Jahreis G (2013) Randomized placebo-controlled intervention with n-3 LC-PUFA-supplemented yoghurt: effects on circulating eicosanoids and cardiovascular risk factors. Clin Nutr 32:686–696. doi:10.1016/j.clnu.2012.12.010 CrossRef Dawczynski C, Massey KA, Ness C, Kiehntopf M, Stepanow S, Platzer M, Grun M, Nicolaou A, Jahreis G (2013) Randomized placebo-controlled intervention with n-3 LC-PUFA-supplemented yoghurt: effects on circulating eicosanoids and cardiovascular risk factors. Clin Nutr 32:686–696. doi:10.​1016/​j.​clnu.​2012.​12.​010 CrossRef
37.
38.
go back to reference Thies F, Nebe-von-Caron G, Powell JR, Yaqoob P, Newsholme EA, Calder PC (2001) Dietary supplementation with gamma-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older humans. J Nutr 131:1918–1927 Thies F, Nebe-von-Caron G, Powell JR, Yaqoob P, Newsholme EA, Calder PC (2001) Dietary supplementation with gamma-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older humans. J Nutr 131:1918–1927
39.
go back to reference Trebble TM, Wootton SA, Miles EA, Mullee M, Arden NK, Ballinger AB, Stroud MA, Burdge GC, Calder PC (2003) Prostaglandin E2 production and T cell function after fish-oil supplementation: response to antioxidant cosupplementation. Am J Clin Nutr 78:376–382 Trebble TM, Wootton SA, Miles EA, Mullee M, Arden NK, Ballinger AB, Stroud MA, Burdge GC, Calder PC (2003) Prostaglandin E2 production and T cell function after fish-oil supplementation: response to antioxidant cosupplementation. Am J Clin Nutr 78:376–382
40.
go back to reference Murr C, Winklhofer-Roob BM, Schroecksnadel K, Maritschnegg M, Mangge H, Bohm BO, Winkelmann BR, Marz W, Fuchs D (2009) Inverse association between serum concentrations of neopterin and antioxidants in patients with and without angiographic coronary artery disease. Atherosclerosis 202:543–549. doi:10.1016/j.atherosclerosis.2008.04.047 CrossRef Murr C, Winklhofer-Roob BM, Schroecksnadel K, Maritschnegg M, Mangge H, Bohm BO, Winkelmann BR, Marz W, Fuchs D (2009) Inverse association between serum concentrations of neopterin and antioxidants in patients with and without angiographic coronary artery disease. Atherosclerosis 202:543–549. doi:10.​1016/​j.​atherosclerosis.​2008.​04.​047 CrossRef
41.
go back to reference Theofylaktopoulou D, Ulvik A, Midttun O, Ueland PM, Vollset SE, Nygard O, Hustad S, Tell GS, Eussen SJ (2014) Vitamins B2 and B6 as determinants of kynurenines and related markers of interferon-gamma-mediated immune activation in the community-based Hordaland Health Study. Br J Nutr 112:1065–1072. doi:10.1017/S0007114514001858 CrossRef Theofylaktopoulou D, Ulvik A, Midttun O, Ueland PM, Vollset SE, Nygard O, Hustad S, Tell GS, Eussen SJ (2014) Vitamins B2 and B6 as determinants of kynurenines and related markers of interferon-gamma-mediated immune activation in the community-based Hordaland Health Study. Br J Nutr 112:1065–1072. doi:10.​1017/​S000711451400185​8 CrossRef
42.
go back to reference Murr C, Talasz H, Artner-Dworzak E, Schroecksnadel K, Fiegl M, Fuchs D, Denz HA (2007) Inverse association between serum selenium concentrations and parameters of immune activation in patients with cardiac disorders. Clin Chem Lab Med 45:1224–1228. doi:10.1515/CCLM.2007.264 CrossRef Murr C, Talasz H, Artner-Dworzak E, Schroecksnadel K, Fiegl M, Fuchs D, Denz HA (2007) Inverse association between serum selenium concentrations and parameters of immune activation in patients with cardiac disorders. Clin Chem Lab Med 45:1224–1228. doi:10.​1515/​CCLM.​2007.​264 CrossRef
43.
go back to reference Wennberg M, Vessby B, Johansson I (2009) Evaluation of relative intake of fatty acids according to the Northern Sweden FFQ with fatty acid levels in erythrocyte membranes as biomarkers. Public Health Nutr 12:1477–1484. doi:10.1017/S1368980008004503 CrossRef Wennberg M, Vessby B, Johansson I (2009) Evaluation of relative intake of fatty acids according to the Northern Sweden FFQ with fatty acid levels in erythrocyte membranes as biomarkers. Public Health Nutr 12:1477–1484. doi:10.​1017/​S136898000800450​3 CrossRef
44.
45.
go back to reference Totland TH, Mehæs B, Lundberg-Hallén N, Helland-Kigen KM, Lund-Blix NA, Myhre J, Johansen AM, Løken E, Frost Andersen L (2012) Norkost 3. En landsomfattande kostholdsundersøkelse blant menn og kvinner i Norge i alderen 18-70 år, 2010-11. (Norkost 3. A national dietary survey among males and females aged 18–70 years in Norway, 2010–11.). Helsedirektoratet, Oslo, Norway (in Norwegian) Totland TH, Mehæs B, Lundberg-Hallén N, Helland-Kigen KM, Lund-Blix NA, Myhre J, Johansen AM, Løken E, Frost Andersen L (2012) Norkost 3. En landsomfattande kostholdsundersøkelse blant menn og kvinner i Norge i alderen 18-70 år, 2010-11. (Norkost 3. A national dietary survey among males and females aged 18–70 years in Norway, 2010–11.). Helsedirektoratet, Oslo, Norway (in Norwegian)
46.
go back to reference Agostoni C, Bresson J-L, Fairweather-Tait S, Flynn A, Golly I, Korhonen H, Lagiou P, Løvik M, Marchelli R, Martin A, Moseley B, Neuhäuser-Berthold M, Przyrembel H, Salminen S, Sanz Y, Strain S, Strobel S, Tetens I, Tomé D, van Loveren H, Verhagen H (2010) Scientific opinion on dietary reference values for fats, including fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J 8:1461. doi:10.2903/j.efsa.2010.1461 CrossRef Agostoni C, Bresson J-L, Fairweather-Tait S, Flynn A, Golly I, Korhonen H, Lagiou P, Løvik M, Marchelli R, Martin A, Moseley B, Neuhäuser-Berthold M, Przyrembel H, Salminen S, Sanz Y, Strain S, Strobel S, Tetens I, Tomé D, van Loveren H, Verhagen H (2010) Scientific opinion on dietary reference values for fats, including fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J 8:1461. doi:10.​2903/​j.​efsa.​2010.​1461 CrossRef
Metadata
Title
Associations between intake of fish and n-3 long-chain polyunsaturated fatty acids and plasma metabolites related to the kynurenine pathway in patients with coronary artery disease
Authors
Therese Karlsson
Elin Strand
Jutta Dierkes
Christian A. Drevon
Jannike Øyen
Øivind Midttun
Per M. Ueland
Oddrun A. Gudbrandsen
Eva Ringdal Pedersen
Ottar Nygård
Publication date
01-02-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-1077-9

Other articles of this Issue 1/2017

European Journal of Nutrition 1/2017 Go to the issue