Plasma methionine, choline, betaine, and dimethylglycine in relation to colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC)
Open accessAbstract
Background Disturbances in one carbon metabolism may contribute to carcinogenesis by affecting methylation and synthesis of DNA. Choline and its oxidation product betaine are involved in this metabolism and can serve as alternative methyl group donors when folate status is low.Patients and methods We conducted a case-control study nested within the European Prospective Investigation into Cancer and Nutrition (EPIC), to investigate plasma concentrations of the methyl donors methionine, choline, betaine (trimethylglycine), and dimethylglycine (DMG) in relation to colorectal cancer (CRC) risk. Our study included 1367 incident CRC cases (965 colon and 402 rectum) and 2323 controls matched by gender, age group, and study center. Multivariate-adjusted odds ratios (ORs) and 95% confidence intervals (95% CIs) for CRC risk were estimated by conditional logistic regression, comparing the fifth to the first quintile of plasma concentrations.Results Overall, methionine (OR: 0.79, 95% CI: 0.63-0.99, P-trend = 0.05), choline (OR: 0.77, 95% CI: 0.60-0.99, P-trend = 0.07), and betaine (OR: 0.85, 95% CI: 0.66-1.09, P-trend = 0.06) concentrations were inversely associated with CRC risk of borderline significance. In participants with folate concentration below the median of 11.3 nmol/l, high betaine concentration was associated with reduced CRC risk (OR: 0.71, 95% CI: 0.50-1.00, P-trend = 0.02), which was not observed for those having a higher folate status. Among women, but not men, high choline concentration was associated with decreased CRC risk (OR: 0.62, 95% CI: 0.43-0.88, P-trend = 0.01). Plasma DMG was not associated with CRC risk.Conclusions Individuals with high plasma concentrations of methionine, choline, and betaine may be at reduced risk of CRC.
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?
Some but not all prospective studies associated higher dietary and plasma levels of choline with increased risk of colorectal neoplasia.
“Some,147, 148 but not all,149–151 prospective studies have associated higher dietary and plasma levels of choline with increased risk of colorectal neoplasia.”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [147]
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
Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008
Ferlay, J., Shin, H.-R., Bray, F., Forman, D., Mathers, C., & Parkin, D. M. (2010) · International Journal of Cancer · doi:10.1002/ijc.25516 · Cited by 22,207 · see citing works
Cancer incidence and mortality patterns in Europe: Estimates for 40 countries in 2012
Ferlay, J., Steliarova‐Foucher, E., Lortet‐Tieulent, J., Rosso, S., Coebergh, J. W. W., Comber, H., Forman, D., & Bray, F. (2013) · European Journal of Cancer · doi:10.1016/j.ejca.2012.12.027 · Cited by 5,243 · see citing works
Riboli, E., Hunt, K., Slimani, N., Ferrari, P., Norat, T., Fahey, M., Charrondière, U., Hémon, B., Casagrande, C., Vignat, J., et al. (2002) · Public Health Nutrition · doi:10.1079/phn2002394 · Cited by 1,866 · see citing works
Self-citationCraig, S. A. (2004) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.3.539 · Cited by 1,062 · see citing works
Ríboli, E. (1997) · International Journal of Epidemiology · doi:10.1093/ije/26.suppl_1.s6 · Cited by 944 · see citing works
Ma, J., Stampfer, M. J., Giovannucci, E. L., Artigas, C., Hunter, D. J., Fuchs, C. S., Willett, W. C., Selhub, J., Hennekens, C. H., & Rozen, R. R. (1997) · PubMed · Cited by 774 · see citing works
Choline: Critical Role During Fetal Development and Dietary Requirements in Adults
Zeisel, S. H. (2006) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.26.061505.111156 · Cited by 741 · see citing works
Choline and betaine in health and disease
Ueland, P. M. (2010) · Journal of Inherited Metabolic Disease · doi:10.1007/s10545-010-9088-4 · Cited by 577 · see citing works
Self-citationOgino, S., Chan, A. T., Fuchs, C. S., & Giovannucci, E. L. (2010) · Gut · doi:10.1136/gut.2010.217182 · Cited by 521 · see citing works
The EPIC Project: Rationale and study design
Ríboli, E., & Kaaks, R. (1997) · International Journal of Epidemiology · Cited by 475 · see citing works
Self-citationEpidemiologic Studies of Folate and Colorectal Neoplasia: a Review
Giovannucci, E. L. (2002) · Journal of Nutrition · doi:10.1093/jn/132.8.2350s · Cited by 451 · see citing works
Molloy, A. M., & Scott, J. M. (1997) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(97)81007-5 · Cited by 433 · see citing works
Diet and cancer — the European Prospective Investigation into Cancer and Nutrition
Bingham, S. A., & Ríboli, E. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1298 · Cited by 387 · see citing works
Holm, P. I., Ueland, P. M., Kvalheim, G., & Lien, E. A. (2003) · Clinical Chemistry · doi:10.1373/49.2.286 · Cited by 318 · see citing works
Self-citationResseguie, M., Song, J., Niculescu, M. D., da Costa, K.-A., Randall, T. A., & Zeisel, S. H. (2007) · The FASEB Journal · doi:10.1096/fj.07-8227com · Cited by 246 · see citing works
Low folate levels may protect against colorectal cancer
Guelpen, B. R. V., Hultdin, J., Johansson, I., Hallmans, G., Stenling, R., Riboli, E., Winkvist, A., & Palmqvist, R. (2006) · Gut · doi:10.1136/gut.2005.085480 · Cited by 222 · see citing works
Self-citationSerum folate, homocysteine and colorectal cancer risk in women: a nested case–control study
Kato, I., Dnistrian, A. M., Schwartz, M. K., Toniolo, P. G., Koenig, K. L., Shore, R. E., Akhmedkhanov, A., Zeleniuch‐Jacquotte, A., & Ríboli, E. (1999) · British Journal of Cancer · doi:10.1038/sj.bjc.6690305 · Cited by 212 · see citing works
Colorectal cancer and folate status: a nested case-control study among male smokers.
Glynn, S. A., Albanes, D., Pietinen, P., Brown, C. C., Rautalahti, M. T., Tangrea, J. A., Gunter, E. W., Barrett, M. J., Virtamo, J. R. K., & Taylor, P. R. (1996) · PubMed · Cited by 195 · see citing works
Fredriksen, Å., Meyer, K., Ueland, P. M., Vollset, S. E., Grotmol, T., & Schneede, J. (2007) · Human Mutation · doi:10.1002/humu.20522 · Cited by 188 · see citing works
Self-citationB-vitamin intake, metabolic genes, and colorectal cancer risk (United States)
Marchand, L. L., Donlon, T. A., Hankin, J. H., Kolonel, L. N., Wilkens, L. R., & Seifried, A. (2002) · Cancer Causes & Control · doi:10.1023/a:1015057614870 · Cited by 176 · see citing works
Kune, G. A., & Watson, L. (2006) · Nutrition and Cancer · doi:10.1207/s15327914nc5601_3 · Cited by 156 · see citing works
Harnack, L., Jacobs, D. R., Nicodemus, K. K., Lazovich, D., Anderson, K. E., & Folsom, A. R. (2002) · Nutrition and Cancer · doi:10.1207/s15327914nc432_5 · Cited by 145 · see citing works
Dietary choline requirements of women: effects of estrogen and genetic variation
Fischer, L. M., da Costa, K.-A., Kwock, L., Galanko, J. A., & Zeisel, S. H. (2010) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2010.30064 · Cited by 136 · see citing works
Dietary intake of selected B vitamins in relation to risk of major cancers in women
Kabat, G. C., Miller, A. B., Jain, M., & Rohan, T. E. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604540 · Cited by 128 · see citing works
Choline deficiency increases lymphocyte apoptosis and DNA damage in humans
da Costa, K.-A., Niculescu, M. D., Craciunescu, C. N., Fischer, L. M., & Zeisel, S. H. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.1.88 · Cited by 128 · see citing works
Hustad, S., Midttun, Ø., Schneede, J., Vollset, S. E., Grotmol, T., & Ueland, P. M. (2007) · The American Journal of Human Genetics · doi:10.1086/513520 · Cited by 127 · see citing works
Self-citationRed cell and plasma folate, folate consumption, and the risk of colorectal adenomatous polyps.
Bird, C. L., Swendseid, M. E., Witte, J. S., Shikany, J. M., Hunt, I. F., Frankl, H. D., Lee, E. R., Longnecker, M. P., & Haile, R. W. (1995) · PubMed · Cited by 125 · see citing works
Hustad, S., Eussen, S. J. P. M., Midttun, Ø., Ulvik, A., van de Kant, P. M., Mørkrid, L., Gislefoss, R. E., & Ueland, P. M. (2011) · Clinical Chemistry · doi:10.1373/clinchem.2011.174490 · Cited by 118 · see citing works
Self-citationDietary Folate, Methionine, Riboflavin, and Vitamin B-6 and Risk of Sporadic Colorectal Cancer
de Vogel, S., Dindore, V., van Engeland, M., Goldbohm, R. A., van den Brandt, P. A., & Weijenberg, M. P. (2008) · Journal of Nutrition · doi:10.3945/jn.108.091157 · Cited by 109 · see citing works
Dietary choline and betaine and the risk of distal colorectal adenoma in women
Cho, E., Willett, W. C., Colditz, G. A., Fuchs, C. S., Wu, K., Chan, A. T., Zeisel, S. H., & Giovannucci, E. L. (2007) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djm082 · Cited by 108 · see citing works
Dietary choline deficiency causes DNA strand breaks and alters epigenetic marks on DNA and histones
Zeisel, S. H. (2011) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2011.10.008 · Cited by 106 · see citing works
High intakes of choline and betaine reduce breast cancer mortality in a population‐based study
Xu, X., Gammon, M. D., Zeisel, S. H., Bradshaw, P. T., Wetmur, J. G., Teitelbaum, S. L., Neugut, A. I., Santella, R. M., & Chen, J. (2009) · The FASEB Journal · doi:10.1096/fj.09-136507 · Cited by 91 · see citing works
Zschäbitz, S., Cheng, T. D., Neuhouser, M. L., Zheng, Y., Ray, R. M., Miller, J. W., Song, X., Maneval, D. R., Beresford, S. A. A., Lane, D. S., et al. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.034736 · Cited by 83 · see citing works
Plasma Folate, Related Genetic Variants, and Colorectal Cancer Risk in EPIC
Eussen, S. J. P. M., Vollset, S. E., Igland, J., Meyer, K., Fredriksen, Å., Ueland, P. M., Jenab, M., Slimani, N., Boffetta, P., Overvad, K., et al. (2010) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-09-0841 · Cited by 83 · see citing works
Self-citationEussen, S. J. P. M., Vollset, S. E., Hustad, S., Midttun, Ø., Meyer, K., Fredriksen, Å., Ueland, P. M., Jenab, M., Slimani, N., Boffetta, P., et al. (2010) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-10-0407 · Cited by 72 · see citing works
Self-citationCholine and betaine intake and the risk of colorectal cancer in men
Lee, J. E., Giovannucci, E., Fuchs, C. S., Willett, W. C., Zeisel, S. H., & Cho, E. (2010) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-09-1295 · Cited by 67 · see citing works
Murtaugh, M. A., Curtin, K., Sweeney, C., Wolff, R. K., Holubkov, R., Caan, B. J., & Slattery, M. L. (2007) · Cancer Causes & Control · doi:10.1007/s10552-006-0099-2 · Cited by 62 · see citing works
Flood, A. P., Caprario, L. C., Chaterjee, N., Lacey, J. V., Schairer, C., & Schatzkin, A. G. (2002) · Cancer Causes & Control · doi:10.1023/a:1016330609603 · Cited by 52 · see citing works
Associations between dietary intake of choline and betaine and lung cancer risk
Ying, J., Rahbar, M. H., Hallman, D. M., Hernandez, L. M., Spitz, M. R., Forman, M. R., & Gorlova, O. Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054561 · Cited by 50 · see citing works
Shrubsole, M. J., Yang, G., Gao, Y., Chow, W.-H., Shu, X. O., Cai, Q., Rothman, N., Gao, J. H., Wagner, C., & Zheng, W. (2009) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-1200 · Cited by 45 · see citing works
5-Methyltetrahydrofolate can be photodegraded by endogenous photosensitizers
Juzeniene, A., Tam, T. T. T., Iani, V., & Moan, J. E. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.07.030 · Cited by 43 · see citing works
Otani, T., Iwasaki, M., Sasazuki, S., Inoue, M., & Tsugane, S. (2007) · Cancer Causes & Control · doi:10.1007/s10552-007-9071-z · Cited by 41 · see citing works
Biomarkers Related to One-Carbon Metabolism as Potential Risk Factors for Distal Colorectal Adenomas
de Vogel, S., Schneede, J., Ueland, P. M., Vollset, S. E., Meyer, K., Fredriksen, Å., Midttun, Ø., Bjørge, T., Kampman, E., Bretthauer, M., et al. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0359 · Cited by 39 · see citing works
Self-citationLinking Epidemiology to Epigenomics—Where Are We Today?
Ulrich, C. M., & Grady, W. M. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-10-0298 · Cited by 18 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Eussen SJ, Vollset SE, Hustad S et al. Plasma vitamins B2, B6, and B12, and related genetic variants as predictors of colorectal cancer risk. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 2010; 19: 2549-2561.
Cited by
Sorted by citations
Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer
Song, M., Chan, A. T., & Sun, J. (2020) · Gastroenterology · doi:10.1053/j.gastro.2019.06.048 · Cited by 752 · see citing works
Nutrients, foods, and colorectal cancer prevention
Song, M., Garrett, W. S., & Chan, A. T. (2015) · Gastroenterology · doi:10.1053/j.gastro.2014.12.035 · Cited by 700 · see citing works
Bae, S., Ulrich, C. M., Neuhouser, M. L., Malysheva, O., Bailey, L. B., Xiao, L., Brown, E. C., Cushing-Haugen, K. L., Zheng, Y., Cheng, T.-Y. D., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-1835 · Cited by 253 · see citing works
Methyl Donor Micronutrients that Modify DNA Methylation and Cancer Outcome
Mahmoud, A. M., & Ali, M. M. (2019) · Nutrients · doi:10.3390/nu11030608 · Cited by 249 · see citing works
Ubago‐Guisado, E., Rodríguez‐Barranco, M., Ching-López, A., Petrova, D., Molina‐Montes, E., Amiano, P., Barricarte, A., Chirlaque, M., Agudo, A., & Sánchez, M. (2021) · Nutrients · doi:10.3390/nu13103582 · Cited by 158 · see citing works
Self-citationColon Carcinogenesis: The Interplay Between Diet and Gut Microbiota
Loke, Y. L., Chew, M. T., Ngeow, Y. F., Lim, W. W.-D., & Peh, S. C. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.603086 · Cited by 129 · see citing works
Guertin, K. A., Li, X. S., Graubard, B. I., Albanes, D., Weinstein, S. J., Goedert, J. J., Wang, Z., Hazen, S. L., & Sinha, R. (2017) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-16-0948 · Cited by 96 · see citing works
Blocking glycine utilization inhibits multiple myeloma progression by disrupting glutathione balance
Xia, J., Zhang, J., Wu, X., Du, W., Zhu, Y., Liu, X., Liu, Z., Meng, B., Guo, J., Yang, Q. Z., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31248-w · Cited by 81 · see citing works
Pancreatic and mucosal enzymes in choline phospholipid digestion
Nilsson, Å., & Duan, R. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00320.2018 · Cited by 68 · see citing works
Betaine is a positive regulator of mitochondrial respiration
Lee, I. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.12.005 · Cited by 66 · see citing works
Liu, Z., Tan, X., Li, Q., Liao, G., Fang, A., Zhang, D., Chen, P., Wang, X., Luo, Y., Long, J., et al. (2018) · Nutrition & Metabolism · doi:10.1186/s12986-018-0319-2 · Cited by 64 · see citing works
Wang, Z.-N., Lin, Y., Liang, J., Huang, Y., Ma, C., Liu, X., & Yang, J. (2017) · Oncotarget · doi:10.18632/oncotarget.22402 · Cited by 61 · see citing works
Association of choline and betaine levels with cancer incidence and survival: A meta-analysis
Youn, J., Cho, E., & Lee, J. E. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2018.01.042 · Cited by 58 · see citing works
Huang, J., Weinstein, S. J., Moore, S. C., Derkach, A., Hua, X., Liao, L. M., Gu, F., Mondul, A. M., Sampson, J. N., & Albanes, D. (2018) · American Journal of Epidemiology · doi:10.1093/aje/kwy017 · Cited by 54 · see citing works
The Impact of Natural Dietary Compounds and Food-Borne Mycotoxins on DNA Methylation and Cancer
Ghazi, T., Arumugam, T., Foolchand, A., & Chuturgoon, A. A. (2020) · Cells · doi:10.3390/cells9092004 · Cited by 51 · see citing works
Yuan, B., Wu, W., Chen, M., Gu, H., Tang, Q., Guo, D., Chen, T., Chen, Y., Lu, C., Song, L., et al. (2017) · Toxicological Sciences · doi:10.1093/toxsci/kfx092 · Cited by 49 · see citing works
Redefining environmental exposure for disease etiology
Rappaport, S. M. (2018) · npj Systems Biology and Applications · doi:10.1038/s41540-018-0065-0 · Cited by 48 · see citing works
Rosas‐Rodríguez, J. A., & Valenzuela-Soto, E. M. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119943 · Cited by 46 · see citing works
Gao, X., Randell, E. W., Zhou, H., & Sun, G. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193114 · Cited by 44 · see citing works
Choline metabolism and its implications in cancer
Yao, N., Li, W., Xu, G., Duan, N., Yu, G., & Qu, J. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1234887 · Cited by 39 · see citing works
Zhou, R.-F., Chen, X., Zhou, Z., Zhang, Y., Lan, Q.-Y., Liao, G., Chen, Y., & Zhu, H. (2017) · Scientific Reports · doi:10.1038/s41598-017-00773-w · Cited by 39 · see citing works
Barberini, L., Restivo, A., Noto, A., Deidda, S., Fattuoni, C., Fanos, V., Saba, L., Zorcolo, L., & Mussap, M. (2019) · Annals of Translational Medicine · doi:10.21037/atm.2019.12.34 · Cited by 39 · see citing works
Myte, R., Gylling, B., Häggström, J., Schneede, J., Ueland, P. M., Hallmans, G., Johansson, I., Palmqvist, R., & Guelpen, B. R. V. (2017) · Scientific Reports · doi:10.1038/srep43434 · Cited by 33 · see citing works
Self-citationDeng, Y., Yao, H., Chen, W., Wei, H., Li, X., Zhang, F., Gao, S., Man, H., Chen, J., Tao, X., et al. (2020) · Journal of Cancer · doi:10.7150/jca.47631 · Cited by 32 · see citing works
Untargeted lipidomic features associated with colorectal cancer in a prospective cohort
Perttula, K., Schiffman, C., Edmands, W. M. B., Petrick, L. M., Grigoryan, H., Cai, X., Gunter, M. J., Naccarati, A., Polidoro, S., Dudoit, S., et al. (2018) · BMC Cancer · doi:10.1186/s12885-018-4894-4 · Cited by 30 · see citing works
Self-citationComponents of one-carbon metabolism other than folate and colorectal cancer risk
Myte, R., Gylling, B., Schneede, J., Ueland, P. M., Häggström, J., Hultdin, J., Hallmans, G., Johansson, I., Palmqvist, R., & Van Guelpen, B. (2016) · Epidemiology · doi:10.1097/ede.0000000000000529 · Cited by 29 · see citing works
Self-citationHarewood, R., Rothwell, J. A., Bešević, J., Viallon, V., Achaintre, D., Gicquiau, A., Rinaldi, S., Wedekind, R., Prehn, C. P., Adamski, J., et al. (2024) · EBioMedicine · doi:10.1016/j.ebiom.2024.105024 · Cited by 25 · see citing works
Self-citationModulation of Colitis-associated Colon Tumorigenesis by Baicalein and Betaine
Kim, D. H., Sung, B., Chung, H. Y., & Kim, N. D. (2014) · Journal of Cancer Prevention · doi:10.15430/jcp.2014.19.3.152 · Cited by 24 · see citing works
Byrd, D. A., Zouiouich, S., Karwa, S., Li, X. S., Wang, Z., Sampson, J. N., Loftfield, E., Huang, W., Hazen, S. L., & Sinha, R. R. (2024) · Cancer · doi:10.1002/cncr.35219 · Cited by 22 · see citing works
Chen, S., Lu, X., He, T., Yishake, D., Tan, X., Hou, M., Luo, Y., Long, J., Tang, Z., Zhong, R., et al. (2021) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202100157 · Cited by 17 · see citing works
Han, P., Bidulescu, A., Barber, J. R., Zeisel, S. H., Joshu, C. E., Prizment, A. E., Vitolins, M. Z., & Platz, E. A. (2019) · Cancer Causes & Control · doi:10.1007/s10552-019-01148-4 · Cited by 17 · see citing works
Keaveney, E. M., Price, R. K., Hamill, L. L., Wallace, J. M. W., McNulty, H., Ward, M., Strain, J., Ueland, P. M., Molloy, A. M., Piironen, V. I., et al. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114514003778 · Cited by 17 · see citing works
Self-citationClavenna, M. G., Vecchia, M. L., Sculco, M., Joseph, S., Barberis, E., Amede, E., Mellai, M., Brossa, S., Borgonovi, G., Occhipinti, P., et al. (2023) · Cancers · doi:10.3390/cancers15123065 · Cited by 14 · see citing works
Changes in Choline Metabolites and Ceramides in Response to a DASH-Style Diet in Older Adults
Tate, B. N., Guilder, G. P. V., Aly, M., Spence, L., Diaz-Rubio, M. E., Le, H. H., Johnson, E. L., McFadden, J. W., & Perry, C. A. (2023) · Nutrients · doi:10.3390/nu15173687 · Cited by 14 · see citing works
Novel metabolomic predictors of incident colorectal cancer in men and women
Downie, J. M., Joshi, A. D., Geraghty, C. M., Guercio, B. J., Zeleznik, O. A., Song, M., Bever, A. M., Drew, D. A., Tabung, F. K., Zhang, X., et al. (2024) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djae270 · Cited by 11 · see citing works
Su, H., Gu, X., Zhang, W., Lin, F., Lu, X., Zeng, X., Wang, C., Chen, W., Liu, W., Tan, P. H., et al. (2025) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5c00091 · Cited by 10 · see citing works
Du, Y., Lin, F., Long, W., Luo, W., Yan, B., Xu, M. T., Mo, X., & Zhang, C. (2016) · European Journal of Nutrition · doi:10.1007/s00394-016-1183-3 · Cited by 9 · see citing works
Gómez-Cebrián, N., Rojas‐Benedicto, A., Albors-Vaquer, A., Bellosillo, B., Besses, C., Martínez‐López, J., Pineda‐Lucena, A., & Puchades‐Carrasco, L. (2021) · Cancers · doi:10.3390/cancers13030482 · Cited by 8 · see citing works
Guerra, G., Segrado, F., Pasanisi, P., Bruno, E., Lopez, S., Raspagliesi, F., Bianchi, M., & Venturelli, E. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e21921 · Cited by 8 · see citing works
Rossi, M., Khalifeh, M., Fiori, F., Parpinel, M. T., Serraino, D., Pelucchi, C., Negri, E., Giacosa, A., Crispo, A., Collatuzzo, G., et al. (2023) · European Journal of Clinical Nutrition · doi:10.1038/s41430-023-01298-4 · Cited by 7 · see citing works
Microbiome in Colonic Carcinogenesis
Sun, J., & Xia, Y. (2023) · Comprehensive physiology · doi:10.1002/cphy.c210052 · Cited by 10 · see citing works
Yang, P., Tsai, E., Hou, M., Lee, Y.-J., & Wang, T. (2024) · Breast Cancer · doi:10.1007/s12282-024-01579-1 · Cited by 6 · see citing works
Li, W., Li, C., Liu, T., Song, Y., Chen, P., Liu, L., Wang, B., & Qu, J. (2023) · Scientific Reports · doi:10.1038/s41598-023-49610-3 · Cited by 5 · see citing works
Microbiota and detrimental protein derived metabolites in colorectal cancer
González, A., Odriozola, I., Fullaondo, A., & Odriozola, A. (2024) · Advances in genetics · doi:10.1016/bs.adgen.2024.06.001 · Cited by 7 · see citing works
Kiss, E., Forika, G., Dank, M., Krenács, T., & Németh, Z. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052546 · Cited by 5 · see citing works
Martín-Fernández-de-Labastida, S., Alegría-Lertxundi, I., de Pancorbo, M. M., & Arroyo‐Izaga, M. (2023) · European Journal of Nutrition · doi:10.1007/s00394-023-03229-2 · Cited by 4 · see citing works
Chen, A. Y., Matich, E. K., Laryea, J. A., Hsu, P.-C., & Su, L. J. (2024) · Nutrients · doi:10.3390/nu16234200 · Cited by 4 · see citing works
Nicken, P., Empl, M. T., Gerhard, D., Hausmann, J., & Steinberg, P. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.07.014 · Cited by 4 · see citing works
The Double-Edged Nature of Methyl Donors in Cancer Development from Prevention to Progression
Pan, D., Wang, S., & Sun, G. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms27010323 · Cited by 3 · see citing works
Genome‐wide association study of circulating folate one‐carbon metabolites
Wang, J., Asante, I., Baron, J. A., Figueiredo, J. C., Haile, R. W., Levine, A. J., Newcomb, P. A., Templeton, A. S., Schumacher, F. R., Louie, S. G., et al. (2019) · Genetic Epidemiology · doi:10.1002/gepi.22249 · Cited by 3 · see citing works
Microbiome in Colonic Carcinogenesis
Sun, J., & Xia, Y. (2023) · Comprehensive physiology · doi:10.1002/j.2040-4603.2023.tb00265.x · Cited by 2 · see citing works
Shi, C., Liu, X., Han, S., Tang, Y., Zeng, H.-L., Du, M.-L., Yang, Y., Jia, J.-N., Shi, Q. W., & Hou, F. (2024) · Current Pharmaceutical Design · doi:10.2174/0113816128294401240523092259 · Cited by 1 · see citing works
Differentiation of Exposure and Disease-Related Biomarkers Associated with Colorectal Cancer
Perttula, K. (2017) · eScholarship (California Digital Library)
Metabolic Risk Factors and Molecular Subtypes of Colorectal Cancer
Myte, R. (2018) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Choline status and related health outcomes in humans: A scoping review
Yoo, S., Aoun, A., Montazeri, A., Collins, É., & Little, J. (2026) · Nutrition and Health · doi:10.1177/02601060261430655
Lin, H., Deng, X., Yang, Y., Zhang, R., Wang, Y.-D., & Chen, W.-D. (2026) · Gut Microbes · doi:10.1080/19490976.2026.2719116
Li, Y., Fan, Y., Yin, Y., Feng, X., Zhu, D., & Dai, L. (2026) · Mucosal Immunology · doi:10.1016/j.mucimm.2026.100407
- Authors
- Nitter, M., Norgård, B., de Vogel, S., Eussen, S. J. P. M., Meyer, K., Ulvik, A., Ueland, P. M., Nygård, O., Vollset, S. E., Bjørge, T., Tjønneland, A., Hansen, L., Boutron-Ruault, M., Racine, A., Cottet, V., Kaaks, R., Kühn, T., Trichopoulou, A., Bamia, C., Naska, A., Grioni, S., Palli, D., Panico, S., Tumino, R., Vineis, P., Bueno-de-Mesquita, H. B., van Kranen, H., Peeters, P. H., Weiderpass, E., Dorronsoro, M., Jakszyn, P., Sánchez, M., Argüelles, M., Huerta, J. M., Barricarte, A., Johansson, M., Ljuslinder, I., Khaw, K., Wareham, N., Freisling, H., Duarte-Salles, T., Stepien, M., Gunter, M. J., & Riboli, E.
- Affiliations
- Maastricht University (NL)
- Bevital (Norway) (NO)
- Haukeland University Hospital (NO)
- Norwegian Institute of Public Health (NO)
- Danish Cancer Society (DK)
- Université Paris-Sud (FR)
- Inserm (FR)
- German Cancer Research Center (DE)
- National and Kapodistrian University of Athens (GR)
- Fondazione IRCCS Istituto Nazionale dei Tumori (IT)
- Istituto per lo Studio e la Prevenzione Oncologica (IT)
- Federico II University Hospital (IT)
- Azienda Usl 8 Arezzo (IT)
- Italian institute for Genomic Medicine (IT)
- National Institute for Public Health and the Environment (NL)
- University Medical Center Utrecht (NL)
- Karolinska Institutet (SE)
- Biogipuzkoa Health Research Institute (ES)
- Institut Català d'Oncologia (ES)
- Universidad de Granada (ES)
- Gobierno del Principado de Asturias (ES)
- Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (ES)
- Instituto de Salud Pública de Navarra (ES)
- Centre international de recherche sur le cancer (FR)
- Umeå University (SE)
- University of Cambridge (GB)
- Imperial College London (GB)
- ORCID
- Eussen, S.J.P.M.
- Meyer, K.
- Ulvik, A.
- Ueland, P.M.
- Bjørge, T.
- Tjønneland, A.
- Hansen, L.
- Racine, A.
- Cottet, V.
- Kaaks, R.
- Trichopoulou, A.
- Naska, A.
- Grioni, S.
- Palli, D.
- Panico, S.
- Tumino, R.
- Vineis, P.
- Peeters, P.H.
- Weiderpass, E.
- Jakszyn, P.
- Sánchez, M.
- Huerta, J.M.
- Barricarte, A.
- Johansson, M.
- Ljuslinder, I.
- Khaw, K.
- Wareham, N.
- Freisling, H.
- Gunter, M.J.
- Venue
- Annals of Oncology
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 25
- Issue
- 8
- Pages
- 1609-1615
- ISSN
- 0923-7534 (ISSN-L)
- OpenAlex
- W2158110124
- Cited by
- 57
- References
- 44
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 7 · 2023: 9 · 2022: 2 · 2021: 4 · 2020: 3 · 2019: 5 · 2018: 8 · 2017: 6 · 2016: 3 · 2015: 2 · 2014: 3
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Annals of Oncology (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
- BIBSYS Brage (BIBSYS (Norway)) (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Rivm (National Institute for Public Health and the Environment) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Funders
- World Health Organization
- Wellcome Trust
- Cancer Research UK
- National Institute for Health and Care Research (NF-SI-0512-10135)
- British Heart Foundation
- Medical Research Council (MC_UU_12015/1)
- Topics
- Health Sciences › Medicine › Rheumatology › Folate and B Vitamins Research
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Keywords
- colorectal cancer risk, plasma methionine, choline, betaine, dimethylglycine, one-carbon metabolism, methyl donors, folate status, DNA methylation, colon cancer, rectal cancer, sex differences, EPIC cohort, cancer risk biomarkers, chemoprevention
- MeSH terms
- Aged, Betaine, Choline, Europe, Female, Humans, Male, Methionine, Middle Aged, Nutritional Status, Prospective Studies, Risk Factors, Sarcosine, Colorectal Neoplasms, Case-Control Studies
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
