Dietary choline and betaine intakes in relation to concentrations of inflammatory markers in healthy adults: the ATTICA study
Open accessAbstract
Background Choline and betaine are found in a variety of plant and animal foods and were recently shown to be associated with decreased homocysteine concentrations.Objective The scope of this work was to investigate the associations between dietary choline and betaine consumption and various markers of low-grade systemic inflammation.Design Under the context of a cross-sectional survey that enrolled 1514 men (18-87 y of age) and 1528 women (18-89 y of age) with no history of cardiovascular disease (the ATTICA Study), fasting blood samples were collected and inflammatory markers were measured. Dietary habits were evaluated with a validated food-frequency questionnaire, and the intakes of choline and betaine were calculated from food-composition tables.Results Compared with the lowest tertile of choline intake (<250 mg/d), participants who consumed >310 mg/d had, on average, 22% lower concentrations of C-reactive protein (P < 0.05), 26% lower concentrations of interleukin-6 (P < 0.05), and 6% lower concentrations of tumor necrosis factor-alpha (P < 0.01). Similarly, participants who consumed >360 mg/d of betaine had, on average, 10% lower concentrations of homocysteine (P < 0.01), 19% lower concentrations of C-reactive protein (P < 0.1), and 12% lower concentrations of tumor necrosis factor-alpha (P < 0.05) than did those who consumed <260 mg/d. These findings were independent of various sociodemographic, lifestyle, and clinical characteristics of the participants.Conclusions Our results support an association between choline and betaine intakes and the inflammation process in free-eating and apparently healthy adults. However, further studies are needed to confirm or refute our findings.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The connection between dietary choline and betaine and heart disease in human subjects is unclear.
“The connection between dietary choline and betaine and heart disease in subjects is unclear.”
From Prognostic value of choline and betaine depends on intestinal microbiota-generated metabolite trimethylamine-N-oxide (2014) · cites this paper as [8]
One study found that greater choline and betaine consumption was linked to less inflammation.
“High intake of choline and betaine was associated with diminished inflammation in one study (66,67).”
From The contributory role of gut microbiota in cardiovascular disease (2014) · cites this paper as [66]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Atherosclerosis--an inflammatory disease
Ross, R. (1999) · New England Journal of Medicine · doi:10.1056/nejm199901143400207 · Cited by 21,725 · see citing works
Institute of Medicine (1998) · National Academies Press eBooks · doi:10.17226/6015 · Cited by 2,464 · see citing works
Homocysteine and Atherothrombosis
Welch, G. N., & Loscalzo, J. (1998) · New England Journal of Medicine · doi:10.1056/nejm199804093381507 · Cited by 1,997 · see citing works
The Sulfur-Containing Amino Acids: An Overview
Brosnan, J. T., & Brosnan, M. E. (2006) · The Journal of Nutrition · doi:10.1093/jn/136.6.1636s · Cited by 1,220 · see citing works
Craig, S. A. (2004) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.3.539 · Cited by 1,062 · see citing works
Ridker, P. M., Glynn, R. J., & Hennekens, C. H. (1998) · Circulation · doi:10.1161/01.cir.97.20.2007 · Cited by 1,012 · see citing works
Inflammatory Markers and Onset of Cardiovascular Events: Results From the Health ABC Study
Cesari, M., Penninx, B. W. J. H., Newman, A. B., Kritchevsky, S. B., Nicklas, B. J., Sutton-Tyrrell, K., Rubin, S. M., Ding, J., Simonsick, E. M., Harris, T. B., et al. (2003) · Circulation · doi:10.1161/01.cir.0000097109.90783.fc · Cited by 978 · see citing works
Chrysohoou, C. A., Panagiotakos, D. B., Pitsavos, C. E., Das, U. N., & Stefanadis, C. (2004) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2004.03.039 · Cited by 770 · see citing works
Self-citationConcentrations of Choline-Containing Compounds and Betaine in Common Foods
Zeisel, S. H., Mar, M.-H., Howe, J. C., & Holden, J. M. (2003) · The Journal of Nutrition · doi:10.1093/jn/133.5.1302 · Cited by 744 · see citing works
Finglas, P. M. (2000) · Trends in Food Science & Technology · doi:10.1016/s0924-2244(01)00010-3 · Cited by 652 · see citing works
Choline, an essential nutrient for humans
Zeisel, S. H., da Costa, K.-A., Franklin, P. D., ALEXANDER, E. A., LaMont, J. T., Sheard, N. F., & Beiser, A. (1991) · The FASEB Journal · doi:10.1096/fasebj.5.7.2010061 · Cited by 623 · see citing works
RELIABILITY AND VALIDITY OF THE INTERNATIONAL PHYSICAL ACTIVITY QUESTIONNAIRE (IPAQ)
Hallal, P. C., & Victora, C. G. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000117161.66394.07 · Cited by 562 · see citing works
Refsum, H., Nurk, E., Smith, A. D., Ueland, P. M., Gjesdal, C. G., Bjelland, I., Tverdal, A., Tell, G. S., Nygard, O. K., & Vollset, S. E. (2006) · Journal of Nutrition · doi:10.1093/jn/136.6.1731s · Cited by 493 · see citing works
Homocysteine and other thiols in plasma and urine: automated determination and sample stability
Fiskerstrand, T., Refsum, H., Kvalheim, G., & Ueland, P. M. (1993) · Clinical Chemistry · doi:10.1093/clinchem/39.2.263 · Cited by 469 · see citing works
Bermudez, E. A., Rifai, N., Buring, J. E., Manson, J. E., & Ridker, P. M. (2002) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000029781.31325.66 · Cited by 469 · see citing works
López‐García, E., Schulze, M. B., Manson, J. E., Meigs, J. B., Albert, C. M., Rifai, N., Willett, W. C., & Hu, F. B. (2004) · Journal of Nutrition · doi:10.1093/jn/134.7.1806 · Cited by 378 · see citing works
Periconceptional Dietary Intake of Choline and Betaine and Neural Tube Defects in Offspring
Shaw, G. M., Carmichael, S. L., Yang, W., Selvin, S., & Schaffer, D. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh187 · Cited by 362 · see citing works
Katsouyanni, K. (1997) · International Journal of Epidemiology · doi:10.1093/ije/26.suppl_1.s118 · Cited by 347 · see citing works
Homocyst(e)ine and Risk of Cardiovascular Disease in the Multiple Risk Factor Intervention Trial
Evans, R. G., Shaten, B. J., Hempel, J. D., Cutler, J. A., & Kuller, L. H. (1997) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.17.10.1947 · Cited by 342 · see citing works
Homocysteine and Risk of Cardiovascular Disease Among Postmenopausal Women
Ridker, P. M. (1999) · JAMA · doi:10.1001/jama.281.19.1817 · Cited by 255 · see citing works
Wener, M. H., Daum, P., & McQuillan, G. M. (2000) · PubMed · Cited by 252 · see citing works
The Effects of Sulfur Amino Acid Intake on Immune Function in Humans
Grimble, R. F. (2006) · Journal of Nutrition · doi:10.1093/jn/136.6.1660s · Cited by 251 · see citing works
Friso, S., Jacques, P. F., Wilson, P. W. F., Rosenberg, I. H., & Selhub, J. (2001) · Circulation · doi:10.1161/01.cir.103.23.2788 · Cited by 243 · see citing works
Purohit, V., Abdelmalek, M. F., Barve, S. S., Benevenga, N. J., Halsted, C. H., Kaplowitz, N., Kharbanda, K. K., Liu, Q.-Y., Lu, S. C.-L., McClain, C. J., et al. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.1.14 · Cited by 221 · see citing works
Cho, E., Zeisel, S. H., Jacques, P. F., Selhub, J., Dougherty, L., Colditz, G. A., & Willett, W. C. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.4.905 · Cited by 217 · see citing works
Schwab, U., Törrönen, A., Toppinen, L., Alfthan, G., Saarinen, M., Aro, A., & Uusitupa, M. I. J. (2002) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/76.5.961 · Cited by 184 · see citing works
Betaine Supplementation Lowers Plasma Homocysteine in Healthy Men and Women
Steenge, G. R., Verhoef, P., & Katan, M. (2003) · Journal of Nutrition · doi:10.1093/jn/133.5.1291 · Cited by 157 · see citing works
USDA database for the choline content of common foods
Howe, J. C., Williams, J. R., & Holden, J. M. (2004) · Cited by 155 · see citing works
Bidulescu, A., Chambless, L. E., Siega-Riz, A. M., Zeisel, S. H., & Heiss, G. (2007) · BMC Cardiovascular Disorders · doi:10.1186/1471-2261-7-20 · Cited by 153 · see citing works
Status and management of hypertension in Greece
Panagiotakos, D. B., Pitsavos, C., Chrysohoou, C. A., Skoumas, J., Papadimitriou, L., Stefanadis, C., & TOUTOUZAS, P. K. (2003) · Journal of Hypertension · doi:10.1097/00004872-200308000-00011 · Cited by 137 · see citing works
Self-citationDalmeijer, G. W., Olthof, M. R., Verhoef, P., Bots, M. L., & van der Schouw, Y. T. (2008) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602725 · Cited by 131 · see citing works
Solini, A., Santini, E., & Ferrannini, E. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803265 · Cited by 130 · see citing works
Effects of Betaine Intake on Plasma Homocysteine Concentrations and Consequences for Health
Olthof, M. R., & Verhoef, P. (2005) · Current Drug Metabolism · doi:10.2174/1389200052997366 · Cited by 124 · see citing works
S-adenosylmethionine (SAMe) protects against acute alcohol induced hepatotoxicity in mice☆
Song, Z., Zhou, Z., Chen, T., et al. (2003) · The Journal of Nutritional Biochemistry · doi:10.1016/s0955-2863(03)00116-5 · Cited by 109 · see citing works
Olthof, M. R., Brink, E. J., Katan, M., & Verhoef, P. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/82.1.111 · Cited by 108 · see citing works
Olthof, M. R., van Vliet, T., Verhoef, P., Zock, P. L., & Katan, M. (2005) · PLoS Medicine · doi:10.1371/journal.pmed.0020135 · Cited by 101 · see citing works
Physiological Regulation of Phospholipid Methylation Alters Plasma Homocysteine in Mice
Jacobs, R. L., Stead, L. M., Devlin, C. M., Tabas, I. A., Brosnan, M. E., Brosnan, J. T., & Vance, D. E. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m501971200 · Cited by 95 · see citing works
S-adenosylmethionine deficiency and TNF-α in lipopolysaccharide-induced hepatic injury
Chawla, R. K., Watson, W. H., Eastin, C. E., Lee, E. Y., Schmidt, J., & McClain, C. J. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.275.1.g125 · Cited by 91 · see citing works
B-group vitamin supplementation mitigates oxidative damage after acute ischaemic stroke
Ullegaddi, R., Powers, H. J., & Gariballa, S. (2004) · Clinical Science · doi:10.1042/cs20040134 · Cited by 90 · see citing works
Shai, I., Stampfer, M. J., Ma, J., Manson, J. E., Hankinson, S. E., Cannuscio, C. C., Selhub, J., Curhan, G. C., & Rimm, E. B. (2004) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2004.07.020 · Cited by 84 · see citing works
Innis, S. M., Davidson, A. G. F., Melynk, S., et al. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.3.702 · Cited by 70 · see citing works
Fischer, L. M., Scearce, J. A., Mar, M.-H. H., Patel, J. R., Blanchard, R. T., MacIntosh, B., Busby, M. G., & Zeisel, S. H. (2005) · Journal of Nutrition · doi:10.1093/jn/135.4.826 · Cited by 66 · see citing works
Su, S.-J., Huang, L., Pai, L.-S., Liu, H., & Chang, K. (2005) · Nutrition · doi:10.1016/j.nut.2005.01.011 · Cited by 63 · see citing works
Bleie, Ø., Semb, A. G., Grundt, H., Nordrehaug, J. E., Vollset, S. E., Ueland, P. M., Nilsen, D. W. T., Bakken, A. M., Refsum, H., & Nygard, O. K. (2007) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01810.x · Cited by 55 · see citing works
Majano, P. L., García‐Monzón, C., García–Trevijano, E. R., Corrales, F. J., Cámara, J., Ortiz, P., Mato, J. M., Avila, M. A., & Moreno‐Otero, R. (2001) · Journal of Hepatology · doi:10.1016/s0168-8278(01)00208-2 · Cited by 53 · see citing works
Jonasson, T., Öhlin, A.-K., Gottsäter, A., Hultberg, B. L., & Öhlin, H. (2005) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2005.108 · Cited by 40 · see citing works
Ward, M., McNulty, H., Pentieva, K. D., et al. (2000) · Journal of Nutrition · doi:10.1093/jn/130.11.2653 · Cited by 35 · see citing works
A choline-rich diet improves survival in a rat model of endotoxin shock
Rivera, C. A., Wheeler, M. D., Enomoto, N., et al. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.275.4.g862 · Cited by 35 · see citing works
The effect of homocysteine reduction by B-vitamin supplementation on inflammatory markers
Peeters, A. C. T. M., van Aken, B. E., Blom, H. J., Reitsma, P. H., & den Heijer, M. (2007) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2007.021 · Cited by 23 · see citing works
Schernthaner, G.-H., Plank, C. M., Minar, E., Bieglmayer, C., Koppensteiner, R., & Schernthaner, G.-H. (2006) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2006.01639.x · Cited by 17 · see citing works
Effect of betaine administration on metabolism of hepatic glutathione in rats
Kim, S. K., Kim, S. Y., & Kim, Y. C. (1998) · Archives of Pharmacal Research · doi:10.1007/bf02976780 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Choline: an essential nutrient for public health
Zeisel, S. H., & da Costa, K.-A. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.2009.00246.x · Cited by 1,062 · see citing works
New hypotheses for the health-protective mechanisms of whole-grain cereals: what is beyond fibre?
Fardet, A. (2010) · Nutrition Research Reviews · doi:10.1017/s0954422410000041 · Cited by 1,030 · see citing works
Wang, Z., Tang, W. H. W., Buffa, J. A., Fu, X., Britt, E. B., Koeth, R. A., Levison, B. S., Fan, Y., Wu, Y., & Hazen, S. L. (2014) · European Heart Journal · doi:10.1093/eurheartj/ehu002 · Cited by 559 · see citing works
Song, T., Song, X., Zhu, C., Patrick, R., Skurla, M., Santangelo, I., Green, M., Harper, D., Ren, B., Forester, B. P., et al. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101503 · Cited by 346 · see citing works
Tolkien, K., Bradburn, S., & Murgatroyd, C. (2019) · Clinical Nutrition · doi:10.1016/j.clnu.2018.11.007 · Cited by 215 · see citing works
Fargnoli, J. L., Fung, T. T., Olenczuk, D. M., Chamberland, J. P., Hu, F. B., & Mantzoros, C. S. (2008) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26480 · Cited by 124 · see citing works
Red Beetroot and Betalains as Cancer Chemopreventative Agents
Lechner, J. F., & Stoner, G. D. (2019) · Molecules · doi:10.3390/molecules24081602 · Cited by 122 · see citing works
Millard, H. R., Musani, S. K., Dibaba, D. T., Talegawkar, S. A., Taylor, H. A., Tucker, K. L., & Bidulescu, A. (2018) · European Journal of Nutrition · doi:10.1007/s00394-016-1296-8 · Cited by 101 · see citing works
Zheng, Y., Li, Y., Rimm, E. B., Hu, F. B., Albert, C. M., Rexrode, K. M., Manson, J. E., & Qi, L. (2016) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.131771 · Cited by 100 · see citing works
Lechner, J. F., Wang, L.-S., Rocha, C. M., Larue, B., Henry, C., McIntyre, C. M., Riedl, K. M., Schwartz, S. J., & Stoner, G. D. (2010) · Journal of Medicinal Food · doi:10.1089/jmf.2008.0280 · Cited by 95 · see citing works
Montenegro, C. F., Kwong, D. A., Minow, Z. A., Davis, B. A., Lozada, C. F., & Casazza, G. A. (2017) · Applied Physiology Nutrition and Metabolism · doi:10.1139/apnm-2016-0452 · Cited by 58 · see citing works
Dietary cholesterol, heart disease risk and cognitive dissonance
McNamara, D. J. (2014) · Proceedings of the Nutrition Society · doi:10.1017/s0029665113003844 · Cited by 30 · see citing works
- Authors
- Detopoulou, P., Panagiotakos, D. B., Antonopoulou, S., Pitsavos, C., & Stefanadis, C.
- Affiliations
- National and Kapodistrian University of Athens (GR)
- Corresponding author
- Panagiotakos, Demosthenes B
- ORCID
- Venue
- The American Journal of Clinical Nutrition
- Publisher
- Elsevier BV
- Published
- 2008-02
- Volume
- 87
- Issue
- 2
- Pages
- 424-430
- ISSN
- 0002-9165 (ISSN-L)
- OpenAlex
- W2158828556
- Cited by
- 286
- References
- 51
- Citations by year
- 2026: 12 · 2025: 14 · 2024: 20 · 2023: 20 · 2022: 19 · 2021: 20 · 2020: 9 · 2019: 19 · 2018: 16 · 2017: 15 · 2016: 18 · 2015: 17 · 2014: 15 · 2013: 12 · 2012: 13
- FWCI
- 15.50
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal of Clinical Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Medicine › Rheumatology › Folate and B Vitamins Research
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Keywords
- dietary choline, dietary betaine, low-grade inflammation, C-reactive protein, interleukin-6, TNF-α, homocysteine, healthy adults, ATTICA study
- MeSH terms
- Adult, Aged, Aged, 80 and over, Analysis of Variance, Betaine, C-Reactive Protein, Choline, Cross-Sectional Studies, Diet Surveys, Fasting, Feeding Behavior, Female, Greece, Homocysteine, Humans, Inflammation, Life Style, Lipotropic Agents, Male, Middle Aged, Tumor Necrosis Factor-alpha, Biomarkers, Interleukin-6
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review