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Erschienen in: European Journal of Nutrition 1/2018

22.08.2016 | Original Contribution

Dietary choline and betaine; associations with subclinical markers of cardiovascular disease risk and incidence of CVD, coronary heart disease and stroke: the Jackson Heart Study

verfasst von: Heather R. Millard, Solomon K. Musani, Daniel T. Dibaba, Sameera A. Talegawkar, Herman A. Taylor, Katherine L. Tucker, Aurelian Bidulescu

Erschienen in: European Journal of Nutrition | Ausgabe 1/2018

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Abstract

Purpose

Several mechanisms have been described through which dietary intake of choline and its derivative betaine may be associated in both directions with subclinical atherosclerosis. We assessed the association of dietary intake of choline and betaine with cardiovascular risk and markers of subclinical cardiovascular disease.

Methods

Data from 3924 Jackson Heart Study (JHS) African-American participants with complete food frequency questionnaire at baseline and follow-up measurements of heart disease measures were used. Multivariable linear regression models were employed to assess associations between choline and betaine intake with carotid intima-media thickness, coronary artery calcium, abdominal aortic calcium and left ventricular mass. Cox proportional hazards regression models were used to estimate associations with time to incident coronary heart disease (CHD), ischemic stroke and cardiovascular disease (CVD).

Results

During an average nine years of follow-up, 124 incident CHD events, 75 incident stroke events and 153 incident CVD events were documented. In women, greater choline intake was associated with lower left ventricular mass (p = 0.0006 for trend across choline quartiles) and with abdominal aortic calcium score. Among all JHS participants, there was a statistically significant inverse association between dietary choline intake and incident stroke, β = −0.33 (p = 0.04). Betaine intake was associated with greater risk of incident CHD when comparing the third quartile of intake with the lowest quartile of intake (HR 1.89, 95 % CI 1.14, 3.15).

Conclusions

Among our African-American participants, higher dietary choline intake was associated with a lower risk of incident ischemic stroke, and thus putative dietary benefits. Higher dietary betaine intake was associated with a nonlinear higher risk of incident CHD.
Literatur
1.
Zurück zum Zitat Niculescu MD, Zeisel SH (2002) Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr 132(8 Suppl):2333S–2335SCrossRef Niculescu MD, Zeisel SH (2002) Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr 132(8 Suppl):2333S–2335SCrossRef
2.
Zurück zum Zitat Zeisel SH (2008) Is there a new component of the Mediterranean diet that reduces inflammation? Am J Clin Nutr 87(2):277–278CrossRef Zeisel SH (2008) Is there a new component of the Mediterranean diet that reduces inflammation? Am J Clin Nutr 87(2):277–278CrossRef
3.
Zurück zum Zitat Dong C, Yoon W, Goldschmidt-Clermont PJ (2002) DNA methylation and atherosclerosis. J Nutr 132(8 Suppl):2406S–2409SCrossRef Dong C, Yoon W, Goldschmidt-Clermont PJ (2002) DNA methylation and atherosclerosis. J Nutr 132(8 Suppl):2406S–2409SCrossRef
4.
Zurück zum Zitat Zaina S, Lindholm MW, Lund G (2005) Nutrition and aberrant DNA methylation patterns in atherosclerosis: more than just hyperhomocysteinemia? J Nutr 135(1):5–8CrossRef Zaina S, Lindholm MW, Lund G (2005) Nutrition and aberrant DNA methylation patterns in atherosclerosis: more than just hyperhomocysteinemia? J Nutr 135(1):5–8CrossRef
5.
Zurück zum Zitat da Costa KA, Gaffney CE, Fischer LM, Zeisel SH (2005) Choline deficiency in mice and humans is associated with increased plasma homocysteine concentration after a methionine load. Am J Clin Nutr 81(2):440–444CrossRef da Costa KA, Gaffney CE, Fischer LM, Zeisel SH (2005) Choline deficiency in mice and humans is associated with increased plasma homocysteine concentration after a methionine load. Am J Clin Nutr 81(2):440–444CrossRef
6.
Zurück zum Zitat Homocysteine Studies C (2002) Homocysteine and risk of ischemic heart disease and stroke: a meta-analysis. JAMA. J Am Med Assoc 288(16):2015–2022CrossRef Homocysteine Studies C (2002) Homocysteine and risk of ischemic heart disease and stroke: a meta-analysis. JAMA. J Am Med Assoc 288(16):2015–2022CrossRef
7.
Zurück zum Zitat Wu LL, Wu JT (2002) Hyperhomocysteinemia is a risk factor for cancer and a new potential tumor marker. Clin Chim Acta 322(1–2):21–28CrossRef Wu LL, Wu JT (2002) Hyperhomocysteinemia is a risk factor for cancer and a new potential tumor marker. Clin Chim Acta 322(1–2):21–28CrossRef
8.
Zurück zum Zitat Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg IH, D’Agostino RB, Wilson PW, Wolf PA (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer’s disease. N Engl J Med 346(7):476–483CrossRef Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg IH, D’Agostino RB, Wilson PW, Wolf PA (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer’s disease. N Engl J Med 346(7):476–483CrossRef
9.
Zurück zum Zitat van Meurs JB, Dhonukshe-Rutten RA, Pluijm SM, van der Klift M, de Jonge R, Lindemans J, de Groot LC, Hofman A, Witteman JC, van Leeuwen JP et al (2004) Homocysteine levels and the risk of osteoporotic fracture. N Engl J Med 350(20):2033–2041CrossRef van Meurs JB, Dhonukshe-Rutten RA, Pluijm SM, van der Klift M, de Jonge R, Lindemans J, de Groot LC, Hofman A, Witteman JC, van Leeuwen JP et al (2004) Homocysteine levels and the risk of osteoporotic fracture. N Engl J Med 350(20):2033–2041CrossRef
10.
Zurück zum Zitat Zeisel SH (2000) Choline: an essential nutrient for humans. Nutrition 16(7–8):669–671CrossRef Zeisel SH (2000) Choline: an essential nutrient for humans. Nutrition 16(7–8):669–671CrossRef
11.
Zurück zum Zitat Shaw GM, Finnell RH, Blom HJ, Carmichael SL, Vollset SE, Yang W, Ueland PM (2009) Choline and risk of neural tube defects in a folate-fortified population. Epidemiology 20(5):714–719CrossRef Shaw GM, Finnell RH, Blom HJ, Carmichael SL, Vollset SE, Yang W, Ueland PM (2009) Choline and risk of neural tube defects in a folate-fortified population. Epidemiology 20(5):714–719CrossRef
12.
Zurück zum Zitat Bae S, Ulrich CM, Neuhouser ML, Malysheva O, Bailey LB, Xiao L, Brown EC, Cushing-Haugen KL, Zheng Y, Cheng TY et al (2014) Plasma choline metabolites and colorectal cancer risk in the Women’s Health Initiative Observational Study. Cancer Res 74(24):7442–7452CrossRef Bae S, Ulrich CM, Neuhouser ML, Malysheva O, Bailey LB, Xiao L, Brown EC, Cushing-Haugen KL, Zheng Y, Cheng TY et al (2014) Plasma choline metabolites and colorectal cancer risk in the Women’s Health Initiative Observational Study. Cancer Res 74(24):7442–7452CrossRef
13.
Zurück zum Zitat Dalmeijer GW, Olthof MR, Verhoef P, Bots ML, van der Schouw YT (2008) Prospective study on dietary intakes of folate, betaine, and choline and cardiovascular disease risk in women. Eur J Clin Nutr 62(3):386–394CrossRef Dalmeijer GW, Olthof MR, Verhoef P, Bots ML, van der Schouw YT (2008) Prospective study on dietary intakes of folate, betaine, and choline and cardiovascular disease risk in women. Eur J Clin Nutr 62(3):386–394CrossRef
14.
Zurück zum Zitat Zeisel SH (2013) Metabolic crosstalk between choline/1-carbon metabolism and energy homeostasis. Clin Chem Lab Med 51(3):467–475CrossRef Zeisel SH (2013) Metabolic crosstalk between choline/1-carbon metabolism and energy homeostasis. Clin Chem Lab Med 51(3):467–475CrossRef
15.
Zurück zum Zitat Detopoulou P, Panagiotakos DB, Antonopoulou S, Pitsavos C, Stefanadis C (2008) Dietary choline and betaine intakes in relation to concentrations of inflammatory markers in healthy adults: the ATTICA study. Am J Clin Nutr 87(2):424–430CrossRef Detopoulou P, Panagiotakos DB, Antonopoulou S, Pitsavos C, Stefanadis C (2008) Dietary choline and betaine intakes in relation to concentrations of inflammatory markers in healthy adults: the ATTICA study. Am J Clin Nutr 87(2):424–430CrossRef
16.
Zurück zum Zitat Bidulescu A, Chambless LE, Siega-Riz AM, Zeisel SH, Heiss G (2007) Usual choline and betaine dietary intake and incident coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) study. BMC Cardiovasc Disord 7:20CrossRef Bidulescu A, Chambless LE, Siega-Riz AM, Zeisel SH, Heiss G (2007) Usual choline and betaine dietary intake and incident coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) study. BMC Cardiovasc Disord 7:20CrossRef
17.
Zurück zum Zitat Taylor HA Jr (2005) The Jackson Heart Study: an overview. Ethn Dis 15(4 Suppl 6):S6-1–S6-3 Taylor HA Jr (2005) The Jackson Heart Study: an overview. Ethn Dis 15(4 Suppl 6):S6-1–S6-3
18.
Zurück zum Zitat Taylor HA Jr, Wilson JG, Jones DW, Sarpong DF, Srinivasan A, Garrison RJ, Nelson C, Wyatt SB (2005) Toward resolution of cardiovascular health disparities in African Americans: design and methods of the Jackson Heart Study. Ethn Dis 15(4 Suppl 6):S6-4–S6-17 Taylor HA Jr, Wilson JG, Jones DW, Sarpong DF, Srinivasan A, Garrison RJ, Nelson C, Wyatt SB (2005) Toward resolution of cardiovascular health disparities in African Americans: design and methods of the Jackson Heart Study. Ethn Dis 15(4 Suppl 6):S6-4–S6-17
19.
Zurück zum Zitat Carithers T, Dubbert PM, Crook E, Davy B, Wyatt SB, Bogle ML, Taylor HA Jr, Tucker KL (2005) Dietary assessment in African Americans: methods used in the Jackson Heart Study. Ethn Dis 15(4 Suppl 6):S6-49–S6-55 Carithers T, Dubbert PM, Crook E, Davy B, Wyatt SB, Bogle ML, Taylor HA Jr, Tucker KL (2005) Dietary assessment in African Americans: methods used in the Jackson Heart Study. Ethn Dis 15(4 Suppl 6):S6-49–S6-55
20.
Zurück zum Zitat Zeisel SH, Mar MH, Howe JC, Holden JM (2003) Concentrations of choline-containing compounds and betaine in common foods. J Nutr 133(5):1302–1307 Zeisel SH, Mar MH, Howe JC, Holden JM (2003) Concentrations of choline-containing compounds and betaine in common foods. J Nutr 133(5):1302–1307
21.
Zurück zum Zitat Newell A (2006) USDA launches searchable database of foods. AWHONN Lifelines 10(2):167–169CrossRef Newell A (2006) USDA launches searchable database of foods. AWHONN Lifelines 10(2):167–169CrossRef
22.
Zurück zum Zitat Miller PE, Mitchell DC, Harala PL, Pettit JM, Smiciklas-Wright H, Hartman TJ (2011) Development and evaluation of a method for calculating the Healthy Eating Index-2005 using the nutrition data system for research. Public Health Nutr 14(2):306–313CrossRef Miller PE, Mitchell DC, Harala PL, Pettit JM, Smiciklas-Wright H, Hartman TJ (2011) Development and evaluation of a method for calculating the Healthy Eating Index-2005 using the nutrition data system for research. Public Health Nutr 14(2):306–313CrossRef
23.
Zurück zum Zitat Bidulescu A, Chambless LE, Siega-Riz AM, Zeisel SH, Heiss G (2009) Repeatability and measurement error in the assessment of choline and betaine dietary intake: the Atherosclerosis Risk in Communities (ARIC) study. Nutr J 8:14CrossRef Bidulescu A, Chambless LE, Siega-Riz AM, Zeisel SH, Heiss G (2009) Repeatability and measurement error in the assessment of choline and betaine dietary intake: the Atherosclerosis Risk in Communities (ARIC) study. Nutr J 8:14CrossRef
24.
Zurück zum Zitat Keku E, Rosamond W, Taylor HA Jr, Garrison R, Wyatt SB, Richard M, Jenkins B, Reeves L, Sarpong D (2005) Cardiovascular disease event classification in the Jackson Heart Study: methods and procedures. Ethn Dis 15(4 Suppl 6):S6-62–S6-70 Keku E, Rosamond W, Taylor HA Jr, Garrison R, Wyatt SB, Richard M, Jenkins B, Reeves L, Sarpong D (2005) Cardiovascular disease event classification in the Jackson Heart Study: methods and procedures. Ethn Dis 15(4 Suppl 6):S6-62–S6-70
25.
Zurück zum Zitat Taylor HA Jr (2003) Establishing a foundation for cardiovascular disease research in an African-American community: the Jackson Heart Study. Ethn Dis 13(4):411–413 Taylor HA Jr (2003) Establishing a foundation for cardiovascular disease research in an African-American community: the Jackson Heart Study. Ethn Dis 13(4):411–413
26.
Zurück zum Zitat Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612CrossRef Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612CrossRef
27.
Zurück zum Zitat Foppa M, Duncan BB, Rohde LE (2005) Echocardiography-based left ventricular mass estimation: how should we define hypertrophy? Cardiovasc Ultrasound 3(1):1–13CrossRef Foppa M, Duncan BB, Rohde LE (2005) Echocardiography-based left ventricular mass estimation: how should we define hypertrophy? Cardiovasc Ultrasound 3(1):1–13CrossRef
28.
Zurück zum Zitat Gatto NM, Henderson VW, St John JA, McCleary C, Detrano R, Hodis HN, Mack WJ (2009) Subclinical atherosclerosis is weakly associated with lower cognitive function in healthy hyperhomocysteinemic adults without clinical cardiovascular disease. Int J Geriatr Psychiatry 24(4):390–399CrossRef Gatto NM, Henderson VW, St John JA, McCleary C, Detrano R, Hodis HN, Mack WJ (2009) Subclinical atherosclerosis is weakly associated with lower cognitive function in healthy hyperhomocysteinemic adults without clinical cardiovascular disease. Int J Geriatr Psychiatry 24(4):390–399CrossRef
29.
Zurück zum Zitat Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M Jr, Detrano R (1990) Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15(4):827–832CrossRef Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M Jr, Detrano R (1990) Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15(4):827–832CrossRef
30.
Zurück zum Zitat Fernandez-Sola J (2015) Cardiovascular risks and benefits of moderate and heavy alcohol consumption. Nat Rev Cardiol 12(10):576–587CrossRef Fernandez-Sola J (2015) Cardiovascular risks and benefits of moderate and heavy alcohol consumption. Nat Rev Cardiol 12(10):576–587CrossRef
31.
Zurück zum Zitat Marshall TA (2011) Dietary guidelines for Americans, 2010: an update. J Am Dent Assoc 142(6):654–656CrossRef Marshall TA (2011) Dietary guidelines for Americans, 2010: an update. J Am Dent Assoc 142(6):654–656CrossRef
32.
Zurück zum Zitat Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N (1986) Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 57(6):450–458CrossRef Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N (1986) Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 57(6):450–458CrossRef
33.
Zurück zum Zitat Haring B, Wang W, Lee ET, Jhamnani S, Howard BV, Devereux RB (2015) Effect of dietary sodium and potassium intake on left ventricular diastolic function and mass in adults</=40 years (from the Strong Heart Study). Am J Cardiol 115(9):1244–1248CrossRef Haring B, Wang W, Lee ET, Jhamnani S, Howard BV, Devereux RB (2015) Effect of dietary sodium and potassium intake on left ventricular diastolic function and mass in adults</=40 years (from the Strong Heart Study). Am J Cardiol 115(9):1244–1248CrossRef
34.
Zurück zum Zitat Institute SAS: SAS/STAT user’s guide, version 8. 1999 Institute SAS: SAS/STAT user’s guide, version 8. 1999
35.
Zurück zum Zitat Institute of Medicine, Food and Nutrition Board (1998) Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid, biotin, and choline. The National Academies Press, Washington. doi:10.17226/6015 Institute of Medicine, Food and Nutrition Board (1998) Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid, biotin, and choline. The National Academies Press, Washington. doi:10.​17226/​6015
36.
Zurück zum Zitat Craig SA (2004) Betaine in human nutrition. Am J Clin Nutr 80(3):539–549CrossRef Craig SA (2004) Betaine in human nutrition. Am J Clin Nutr 80(3):539–549CrossRef
37.
Zurück zum Zitat Milani RV, Lavie CJ (2008) Homocysteine: the Rubik’s cube of cardiovascular risk factors. Mayo Clin Proc 83(11):1200–1202CrossRef Milani RV, Lavie CJ (2008) Homocysteine: the Rubik’s cube of cardiovascular risk factors. Mayo Clin Proc 83(11):1200–1202CrossRef
38.
Zurück zum Zitat Medina M, Urdiales JL, Amores-Sanchez MI (2001) Roles of homocysteine in cell metabolism: old and new functions. Eur J Biochem/FEBS 268(14):3871–3882CrossRef Medina M, Urdiales JL, Amores-Sanchez MI (2001) Roles of homocysteine in cell metabolism: old and new functions. Eur J Biochem/FEBS 268(14):3871–3882CrossRef
39.
Zurück zum Zitat Finkelstein JD, Harris BJ, Kyle WE (1972) Methionine metabolism in mammals: kinetic study of betaine-homocysteine methyltransferase. Arch Biochem Biophys 153(1):320–324CrossRef Finkelstein JD, Harris BJ, Kyle WE (1972) Methionine metabolism in mammals: kinetic study of betaine-homocysteine methyltransferase. Arch Biochem Biophys 153(1):320–324CrossRef
40.
Zurück zum Zitat Steenge GR, Verhoef P, Katan MB (2003) Betaine supplementation lowers plasma homocysteine in healthy men and women. J Nutr 133(5):1291–1295 Steenge GR, Verhoef P, Katan MB (2003) Betaine supplementation lowers plasma homocysteine in healthy men and women. J Nutr 133(5):1291–1295
41.
Zurück zum Zitat Cho E, Zeisel SH, Jacques P, Selhub J, Dougherty L, Colditz GA, Willett WC (2006) Dietary choline and betaine assessed by food-frequency questionnaire in relation to plasma total homocysteine concentration in the Framingham Offspring Study. Am J Clin Nutr 83(4):905–911CrossRef Cho E, Zeisel SH, Jacques P, Selhub J, Dougherty L, Colditz GA, Willett WC (2006) Dietary choline and betaine assessed by food-frequency questionnaire in relation to plasma total homocysteine concentration in the Framingham Offspring Study. Am J Clin Nutr 83(4):905–911CrossRef
42.
Zurück zum Zitat Ide T, Shimano H, Yahagi N, Matsuzaka T, Nakakuki M, Yamamoto T, Nakagawa Y, Takahashi A, Suzuki H, Sone H et al (2004) SREBPs suppress IRS-2-mediated insulin signalling in the liver. Nat Cell Biol 6(4):351–357CrossRef Ide T, Shimano H, Yahagi N, Matsuzaka T, Nakakuki M, Yamamoto T, Nakagawa Y, Takahashi A, Suzuki H, Sone H et al (2004) SREBPs suppress IRS-2-mediated insulin signalling in the liver. Nat Cell Biol 6(4):351–357CrossRef
43.
Zurück zum Zitat Purohit V, Abdelmalek MF, Barve S, Benevenga NJ, Halsted CH, Kaplowitz N, Kharbanda KK, Liu Q-Y, Lu SC, McClain CJ et al (2007) Role of S-adenosylmethionine, folate, and betaine in the treatment of alcoholic liver disease: summary of a symposium. Am J Clin Nutr 86(1):14–24CrossRef Purohit V, Abdelmalek MF, Barve S, Benevenga NJ, Halsted CH, Kaplowitz N, Kharbanda KK, Liu Q-Y, Lu SC, McClain CJ et al (2007) Role of S-adenosylmethionine, folate, and betaine in the treatment of alcoholic liver disease: summary of a symposium. Am J Clin Nutr 86(1):14–24CrossRef
44.
Zurück zum Zitat Muraoka T, Aoki K, Iwasaki T, Shinoda K, Nakamura A, Aburatani H, Mori S, Tokuyama K, Kubota N, Kadowaki T et al (2011) Ezetimibe decreases SREBP-1c expression in liver and reverses hepatic insulin resistance in mice fed a high-fat diet. Metab, Clin Exp 60(5):617–628CrossRef Muraoka T, Aoki K, Iwasaki T, Shinoda K, Nakamura A, Aburatani H, Mori S, Tokuyama K, Kubota N, Kadowaki T et al (2011) Ezetimibe decreases SREBP-1c expression in liver and reverses hepatic insulin resistance in mice fed a high-fat diet. Metab, Clin Exp 60(5):617–628CrossRef
45.
Zurück zum Zitat Bertoia ML, Pai JK, Cooke JP, Joosten MM, Mittleman MA, Rimm EB, Mukamal KJ (2014) Plasma homocysteine, dietary B vitamins, betaine, and choline and risk of peripheral artery disease. Atherosclerosis 235(1):94–101CrossRef Bertoia ML, Pai JK, Cooke JP, Joosten MM, Mittleman MA, Rimm EB, Mukamal KJ (2014) Plasma homocysteine, dietary B vitamins, betaine, and choline and risk of peripheral artery disease. Atherosclerosis 235(1):94–101CrossRef
46.
Zurück zum Zitat Cho E, Holmes MD, Hankinson SE, Willett WC (2010) Choline and betaine intake and risk of breast cancer among post-menopausal women. Br J Cancer 102(3):489–494CrossRef Cho E, Holmes MD, Hankinson SE, Willett WC (2010) Choline and betaine intake and risk of breast cancer among post-menopausal women. Br J Cancer 102(3):489–494CrossRef
47.
Zurück zum Zitat Cho E, Willett WC, Colditz GA, Fuchs CS, Wu K, Chan AT, Zeisel SH, Giovannucci EL (2007) Dietary choline and betaine and the risk of distal colorectal adenoma in women. J Natl Cancer Inst 99(16):1224–1231CrossRef Cho E, Willett WC, Colditz GA, Fuchs CS, Wu K, Chan AT, Zeisel SH, Giovannucci EL (2007) Dietary choline and betaine and the risk of distal colorectal adenoma in women. J Natl Cancer Inst 99(16):1224–1231CrossRef
48.
Zurück zum Zitat Kotsopoulos J, Hankinson SE, Tworoger SS (2010) Dietary betaine and choline intake are not associated with risk of epithelial ovarian cancer. Eur J Clin Nutr 64(1):111–114CrossRef Kotsopoulos J, Hankinson SE, Tworoger SS (2010) Dietary betaine and choline intake are not associated with risk of epithelial ovarian cancer. Eur J Clin Nutr 64(1):111–114CrossRef
49.
Zurück zum Zitat Lee JE, Giovannucci E, Fuchs CS, Willett WC, Zeisel SH, Cho E (2010) Choline and betaine intake and the risk of colorectal cancer in men. Cancer Epidemiol, Biomark Prev 19(3):884–887CrossRef Lee JE, Giovannucci E, Fuchs CS, Willett WC, Zeisel SH, Cho E (2010) Choline and betaine intake and the risk of colorectal cancer in men. Cancer Epidemiol, Biomark Prev 19(3):884–887CrossRef
50.
Zurück zum Zitat Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM et al (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472(7341):57–63CrossRef Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM et al (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472(7341):57–63CrossRef
Metadaten
Titel
Dietary choline and betaine; associations with subclinical markers of cardiovascular disease risk and incidence of CVD, coronary heart disease and stroke: the Jackson Heart Study
verfasst von
Heather R. Millard
Solomon K. Musani
Daniel T. Dibaba
Sameera A. Talegawkar
Herman A. Taylor
Katherine L. Tucker
Aurelian Bidulescu
Publikationsdatum
22.08.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 1/2018
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-016-1296-8

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