Plasma Choline Metabolites and Colorectal Cancer Risk in the Women's Health Initiative Observational Study
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Abstract
Few studies have examined associations between plasma choline metabolites and risk of colorectal cancer. Therefore, we investigated associations between plasma biomarkers of choline metabolism [choline, betaine, dimethylglycine, and trimethylamine N-oxide (TMAO)] and colorectal cancer risk among postmenopausal women in a case–control study nested within the Women's Health Initiative Observational Study. We selected 835 matched case–control pairs, and cases were further stratified by tumor site (proximal, distal, or rectal) and stage (local/regional or metastatic). Colorectal cancer was assessed by self-report and confirmed by medical records over the mean of 5.2 years of follow-up. Baseline plasma choline metabolites were measured by LC/MS-MS. In multivariable-adjusted conditional logistic regression models, plasma choline tended to be positively associated with rectal cancer risk [OR (95% confidence interval, CI)highest vs. lowest quartile = 2.44 (0.93–6.40); P trend = 0.08], whereas plasma betaine was inversely associated with colorectal cancer overall [0.68 (0.47–0.99); P trend = 0.01] and with local/regional tumors [0.64 (0.42–0.99); P trend = 0.009]. Notably, the plasma betaine:choline ratio was inversely associated with colorectal cancer overall [0.56 (0.39–0.82); P trend = 0.004] as well as with proximal [0.66 (0.41–1.06); P trend = 0.049], rectal [0.27 (0.10–0.78); P trend = 0.02], and local/regional [0.50 (0.33–0.76); P trend = 0.001] tumors. Finally, plasma TMAO, an oxidative derivative of choline produced by intestinal bacteria, was positively associated with rectal cancer [3.38 (1.25–9.16); P trend = 0.02] and with overall colorectal cancer risk among women with lower (vs. higher) plasma vitamin B12 levels (P interaction = 0.003). Collectively, these data suggest that alterations in choline metabolism, which may arise early in disease development, may be associated with higher risk of colorectal cancer. The positive association between plasma TMAO and colorectal cancer risk is consistent with an involvement of the gut microbiome in colorectal cancer pathogenesis. Cancer Res; 74(24); 7442–52. ©2014 AACR.
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The association between plasma trimethylamine N-oxide level and colorectal cancer risk was restricted to patients with low plasma vitamin B12 levels.
“In support of this hypothesis, the association between plasma level of TMAO and risk of CRC was restricted to patients with low plasma levels of vitamin B12.151”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [151]
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 [151]
The Women's Health Initiative and ATBC studies reported that alterations in choline metabolism and plasma TMAO predicted risk factors for colorectal cancer.
“The Women's Health Initiative and the alpha-tocopherol, beta-carotene cancer prevention observational studies reported that alterations in choline metabolism and plasma TMAO concentrations were predicted risk factors for colorectal cancer (7,83).”
From Trimethylamine <i>N</i> -Oxide, the Microbiome, and Heart and Kidney Disease (2017) · cites this paper as [7]
Serum TMAO levels are positively correlated with cardiovascular disease in humans.
“Recent human studies have established that the levels of TMAO in serum are positively correlated with impaired renal function, colorectal cancer, and cardiovascular disease (CVD) (8, 10, 17, 18).”
Serum TMAO levels are positively correlated with colorectal cancer in humans.
“Recent human studies have established that the levels of TMAO in serum are positively correlated with impaired renal function, colorectal cancer, and cardiovascular disease (CVD) (8, 10, 17, 18).”
Serum TMAO levels are positively correlated with impaired renal function in humans.
“Recent human studies have established that the levels of TMAO in serum are positively correlated with impaired renal function, colorectal cancer, and cardiovascular disease (CVD) (8, 10, 17, 18).”
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Cites
An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444 · see citing works
Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease
Wang, Z., Klipfell, E., Bennett, B. J., Koeth, R., Levison, B. S., DuGar, B., Feldstein, A. E., Britt, E. B., Fu, X., Chung, Y.-M., et al. (2011) · Nature · doi:10.1038/nature09922 · Cited by 5,597 · see citing works
Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis
Koeth, R. A., Wang, Z., Levison, B. S., Buffa, J. A., Org, E., Sheehy, B. T., Britt, E. B., Fu, X., Wu, Y., Li, L., et al. (2013) · Nature Medicine · doi:10.1038/nm.3145 · Cited by 4,386 · see citing works
Design of the Women’s Health Initiative Clinical Trial and Observational Study
The Women’s Health Initiative Study Group (1998) · Controlled Clinical Trials · doi:10.1016/s0197-2456(97)00078-0 · Cited by 2,580 · see citing works
Colorectal Cancer Epidemiology: Incidence, Mortality, Survival, and Risk Factors
Haggar, F. A., & Boushey, R. P. (2009) · Clinics in Colon and Rectal Surgery · doi:10.1055/s-0029-1242458 · Cited by 2,018 · see citing works
Bacteria as vitamin suppliers to their host: A gut microbiota perspective
LeBlanc, J. G., Milani, C., de Giori, G. S., Sesma, F., van Sinderen, D., & Ventura, M. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2012.08.005 · Cited by 1,613 · cited 1× · see citing works
“Certain groups of intestinal bacteria can synthesize (45, 46) and consume (47, 48) vitamin B12, 291 which may impact the vitamin B12 requirement/status of the host.”
Dumas, M.-E., Barton, R. H., Toye, A., Cloarec, O., Blancher, C., Rothwell, A., Fearnside, J., Tatoud, R., Blanc, V., Lindon, J. C., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601056103 · Cited by 1,042 · see citing works
Folate and DNA Methylation: A Review of Molecular Mechanisms and the Evidence for Folate's Role
Crider, K. S., Yang, T. P., Berry, R. J., & Bailey, L. B. (2012) · Advances in Nutrition · doi:10.3945/an.111.000992 · Cited by 1,022 · see citing works
Self-citationCholine metabolism in malignant transformation
Glunde, K., Bhujwalla, Z. M., & Ronen, S. M. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3162 · Cited by 826 · see citing works
Outcomes ascertainment and adjudication methods in the women's health initiative
Curb, J. D., McTiernan, A., Heckbert, S. R., Kooperberg, C. L., Stanford, J. L., Nevitt, M. C., Johnson, K., Proulx-Burns, L., Pastore, L. M., Criqui, M. H., et al. (2003) · Annals of Epidemiology · doi:10.1016/s1047-2797(03)00048-6 · Cited by 700 · see citing works
Estrogen plus Progestin and Colorectal Cancer in Postmenopausal Women
Chlebowski, R. T., Wactawski‐Wende, J., Ritenbaugh, C., Hubbell, F. A., Ascensão, J. L., Rodabough, R. J., Rosenberg, C. A., Taylor, V. M., Harris, R. E., Chen, C., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa032071 · Cited by 663 · see citing works
Bailey, L. B. (2009) · CRC Press eBooks · doi:10.1201/9781420071252 · Cited by 636 · see citing works
Self-citationLanger, R. D., White, E., Lewis, C. E., Kotchen, J. M., Hendrix, S. L., & Trevisan, M. (2003) · Annals of Epidemiology · doi:10.1016/s1047-2797(03)00047-4 · Cited by 630 · see citing works
Postmenopausal hormone therapy and the risk of colorectal cancer: a review and meta-analysis
Grodstein, F., Newcomb, P. A., & Stampfer, M. J. (1999) · The American Journal of Medicine · doi:10.1016/s0002-9343(99)00063-7 · Cited by 580 · see citing works
Krueger, S. K., & Williams, D. E. (2005) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.01.001 · Cited by 570 · see citing works
Aboagye, E. O., & Bhujwalla, Z. M. (1999) · PubMed · Cited by 546 · see citing works
Epidemiologic 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
Vitamin B12 deficiency in the elderly.
Baik, H.-W., & Russell, R. M. (1999) · Annual review of nutrition · doi:10.1146/annurev.nutr.19.1.357 · Cited by 415 · see citing works
Folate Status: Effects on Pathways of Colorectal Carcinogenesis
Choi, S., & Mason, J. B. (2002) · Journal of Nutrition · doi:10.1093/jn/132.8.2413s · Cited by 398 · see citing works
DNA Methylation, Cancer Susceptibility, and Nutrient Interactions
Davis, C. D., & Uthus, E. O. (2004) · Experimental Biology and Medicine · doi:10.1177/153537020422901002 · Cited by 390 · see citing works
Folate and DNA Methylation: A Mechanistic Link between Folate Deficiency and Colorectal Cancer?
Kim, Y. (2004) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.511.13.4 · Cited by 350 · see citing works
Gastrointestinal microflora, food components and colon cancer prevention
Davis, C. D., & Milner, J. A. (2009) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.06.001 · Cited by 335 · see citing works
Holtan, S. G., Creedon, D. J., Haluska, P., & Markovic, S. N. (2009) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(11)60669-1 · Cited by 306 · see citing works
The role of hyperosmotic stress in inflammation and disease
Brocker, C. N., Thompson, D. C., & Vasiliou, V. (2012) · BioMolecular Concepts · doi:10.1515/bmc-2012-0001 · Cited by 302 · see citing works
Pufulete, M., Abbadi, R. A.-G., Leather, A. J. M., Appleby, P. N., Gout, S., Terry, C., Emery, P. W., & Sanders, T. A. B. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00279-8 · Cited by 268 · see citing works
Culture‐independent analysis of the gut microbiota in colorectal cancer and polyposis
Scanlan, P. D., Shanahan, F., Clune, Y., Collins, J. K., O'Sullivan, G. C., O'Riordan, M., Holmes, E., Wang, Y., & Marchesi, J. R. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01503.x · Cited by 245 · see citing works
Dietary Precursors of Trimethylamine in Man: A Pilot Study
Zhang, A. Q., Mitchell, S. C., & Smith, R. L. (1999) · Food and Chemical Toxicology · doi:10.1016/s0278-6915(99)00028-9 · Cited by 232 · see citing works
Biomarkers of Nutrient Exposure and Status in One-Carbon (Methyl) Metabolism
Mason, J. B. (2003) · Journal of Nutrition · doi:10.1093/jn/133.3.941s · Cited by 226 · see citing works
Gunter, M. J., Hoover, D. R., Yu, H., Wassertheil-Smoller, S. W., Rohan, T. E., Manson, J. E., Howard, B. V., Wylie‐Rosett, J., Anderson, G. L., Ho, G., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-2946 · Cited by 224 · see citing works
The role of gut microbiota in the pathogenesis of colorectal cancer
Zhu, Q., Gao, R., Wu, W., & Qin, H. (2013) · Tumor Biology · doi:10.1007/s13277-013-0684-4 · Cited by 210 · see citing works
Screening Colonoscopy in Very Elderly Patients
Lin, O. S. T., Kozarek, R. A., Schembre, D. B., Ayub, K., Glück, M., Drennan, F. M., Soon, M., & Rabeneck, L. (2006) · JAMA · doi:10.1001/jama.295.20.2357 · Cited by 183 · see citing works
Maternal choline intake modulates maternal and fetal biomarkers of choline metabolism in humans
Yan, J., Jiang, X., West, A. A., Perry, C. A., Malysheva, O., Devapatla, S., Pressman, E. K., Vermeylen, F., Stabler, S. P., Allen, R. H., et al. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.022772 · Cited by 173 · see citing works
Self-citationVitamin B12 synthesis by human small intestinal bacteria
Albert, M. J., Mathan, V. I., & Baker, S. J. (1980) · Nature · doi:10.1038/283781a0 · Cited by 171 · see citing works
Novel Reductant for Determination of Total Plasma Homocysteine
Gilfix, B. M., Blank, D. W., & Rosenblatt, D. S. (1997) · Clinical Chemistry · doi:10.1093/clinchem/43.4.687 · Cited by 163 · see citing works
Zeisel, S. H., daCosta, K. A., Youssef, M., & Hensey, S. (1989) · The Journal of Nutrition · doi:10.1093/jn/119.5.800 · Cited by 151 · see citing works
Therapeutic Targets and Biomarkers Identified in Cancer Choline Phospholipid Metabolism
Glunde, K., & Serkova, N. J. (2006) · Pharmacogenomics · doi:10.2217/14622416.7.7.1109 · Cited by 148 · see citing works
Pandrea, I. V., & LANDAY, A. L. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-387715-4.00003-4 · Cited by 127 · see citing works
Increased Choline Kinase Activity and Elevated Phosphocholine Levels in Human Colon Cancer†
NAKAGAMI, K., Uchida, T., Ohwada, S., Koibuchi, Y., Suda, Y., Sekine, T., & Morishita, Y. (1999) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.1999.tb00764.x · Cited by 124 · see citing works
Microvessel quantification and its possible relation with liver metastasis in colorectal cancer
Tomisaki, S., Ohno, S., Ichiyoshi, Y., Kuwano, H., Maehara, Y., & Sugimachi, K. (1996) · Cancer · doi:10.1002/(sici)1097-0142(19960415)77:8 · Cited by 118 · see citing works
Yan, J., Jiang, X., West, A. A., Perry, C. A., Malysheva, O., Brenna, J. T., Stabler, S. P., Allen, R. H., Gregory, J. F., & Caudill, M. A. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.066092 · Cited by 111 · see citing works
Self-citationTalwar, D. K., Quasim, T., McMillan, D. C., Kinsella, J., Williamson, C., & O’Reilly, D. S. J. (2003) · Journal of Chromatography B · doi:10.1016/s1570-0232(03)00320-9 · Cited by 110 · see citing works
Miller, J. W., Beresford, S. A. A., Neuhouser, M. L., Cheng, T. D., Song, X., Brown, E. C., Zheng, Y., Rodríguez, B. L., Green, R., & Ulrich, C. M. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.049932 · Cited by 86 · see citing works
Self-citationToriola, A. T., Cheng, T. D., Neuhouser, M. L., Wener, M. H., Zheng, Y., Brown, E. C., Miller, J. W., Song, X., Beresford, S. A. A., Gunter, M. J., et al. (2012) · International Journal of Cancer · doi:10.1002/ijc.27942 · Cited by 86 · see citing works
Self-citationZschäbitz, 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
Self-citationAge-Related Changes in Cobalamin (Vitamin B12) Handling
Nilsson‐Ehle, H. (1998) · Drugs & Aging · doi:10.2165/00002512-199812040-00003 · Cited by 79 · see citing works
Giannella, R. A., Broitman, S. A., & Zamcheck, N. (1971) · Journal of Clinical Investigation · doi:10.1172/jci106581 · Cited by 77 · see citing works
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., et al. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu185 · Cited by 57 · see citing works
Lipid Metabolism by Gut Microbes and Atherosclerosis
Loscalzo, J. (2011) · Circulation Research · doi:10.1161/res.0b013e3182290620 · Cited by 54 · see citing works
Meat-metabolizing bacteria in atherosclerosis
Bäckhed, F. (2013) · Nature Medicine · doi:10.1038/nm.3178 · Cited by 53 · see citing works
Degradation of various amine compounds by mesophilic clostridia
M�ller, B., Hippe, H., & Gottschalk, G. (1986) · Archives of Microbiology · doi:10.1007/bf00413032 · Cited by 50 · see citing works
Studies of the small-intestinal bacterial flora and of intestinal absorption in pernicious anemia
Sherwood, W. C., Goldstein, F., Haurani, F. I., & Wirts, C. W. (1964) · Digestive Diseases and Sciences · doi:10.1007/bf02239334 · Cited by 46 · 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
Yan, J., Winter, L. B., Burns‐Whitmore, B., Vermeylen, F., & Caudill, M. A. (2012) · Nutrition and Diabetes · doi:10.1038/nutd.2012.23 · Cited by 35 · see citing works
Self-citationCulture‐independent analysis of the gut microbiota in colorectal cancer and polyposis
Scanlan, P. D., Shanahan, F., Clune, Y., Collins, J. K., O’Sullivan, G. C., O'Riordan, M., Holmes, E. C., Wang, Y., & Marchesi, J. R. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01622.x · Cited by 29 · see citing works
Folate and Choline Interrelationships
Caudill, M. A. (2009) · CRC Press eBooks · doi:10.1201/9781420071252-c18 · Cited by 18 · see citing works
Self-citationKanazawa (1996) · doi:10.1002/(sici)1097-0142(19960415)77:8+
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Thomas, A. M., Manghi, P., Asnicar, F., Pasolli, E., Armanini, F., Zolfo, M., Beghini, F., Manara, S., Karcher, N., Pozzi, C., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0405-7 · Cited by 1,030 · see citing works
Self-citationInfluence 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
Romano, K. A., Vivas, E. I., Amador-Noguez, D., & Rey, F. E. (2015) · mBio · doi:10.1128/mbio.02481-14 · Cited by 777 · see citing works
Gut microbes and metabolites as modulators of blood-brain barrier integrity and brain health
Parker, A., Fonseca, S., & Carding, S. R. (2019) · Gut Microbes · doi:10.1080/19490976.2019.1638722 · Cited by 722 · see citing works
Trimethylamine <i>N</i> -Oxide, the Microbiome, and Heart and Kidney Disease
Zeisel, S. H., & Warrier, M. (2017) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071816-064732 · Cited by 475 · see citing works
Kerfeld, C. A., Aussignargues, C., Zarzycki, J., Cai, F., & Sutter, M. (2018) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2018.10 · Cited by 445 · see citing works
Cho, C. E., Taesuwan, S., Malysheva, O. V., Bender, E., Tulchinsky, N. F., Yan, J., Sutter, J. L., & Caudill, M. A. (2017) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201600324 · Cited by 405 · see citing works
Self-citationMirji, G., Worth, A., Bhat, S. A., El Sayed, M., Kannan, T., Goldman, A. R., Tang, H.-Y., Liu, Q., Auslander, N., Dang, C. V., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.abn0704 · Cited by 327 · see citing works
TMAO: A small molecule of great expectations
Ufnal, M., Żądło‐Dobrowolska, A., & Ostaszewski, R. (2015) · Nutrition · doi:10.1016/j.nut.2015.05.006 · Cited by 319 · see citing works
Role of the Gut Microbiota and Its Metabolites in Tumorigenesis or Development of Colorectal Cancer
Qu, R., Zhang, Y., Ma, Y., Zhou, X., Sun, L., Jiang, C., Zhang, Z., & Fu, W. (2023) · Advanced Science · doi:10.1002/advs.202205563 · Cited by 303 · see citing works
Dysbiosis of gut microbiota in promoting the development of colorectal cancer
Zou, S., Fang, L., & Lee, M. (2017) · Gastroenterology report · doi:10.1093/gastro/gox031 · Cited by 279 · see citing works
Genetic Factors Are Not the Major Causes of Chronic Diseases
Rappaport, S. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154387 · Cited by 250 · see citing works
Gut microbiota: A target for heavy metal toxicity and a probiotic protective strategy
Duan, H., Yu, L., Tian, F., Zhai, Q., Fan, L., & Chen, W. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.140429 · Cited by 247 · see citing works
Martínez-del Campo, A., Bodea, S., Hamer, H. A., Marks, J. A., Haiser, H. J., Turnbaugh, P. J., & Balskus, E. P. (2015) · mBio · doi:10.1128/mbio.00042-15 · Cited by 224 · see citing works
Trimethylamine- N -Oxide: Friend, Foe, or Simply Caught in the Cross-Fire?
Cho, C. E., & Caudill, M. A. (2016) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2016.10.005 · Cited by 218 · see citing works
Self-citationMueller, D. M., Allenspach, M., Othman, A., Saely, C. H., Muendlein, A., Vonbank, A., Drexel, H., & von Eckardstein, A. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.10.091 · Cited by 217 · see citing works
Rohrmann, S., Linseisen, J., Allenspach, M., von Eckardstein, A., & Müller, D. (2016) · The Journal of Nutrition · doi:10.3945/jn.115.220103 · Cited by 197 · see citing works
Phosphatidylcholine-Derived Lipid Mediators: The Crosstalk Between Cancer Cells and Immune Cells
Saito, R. D. F., Andrade, L. N. D. S., Bustos, S. O., & Chammas, R. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.768606 · Cited by 183 · see citing works
Li, D., Lu, Y., Yuan, S., Cai, X., He, Y., Chen, J., Wu, Q., He, D., Fang, A., Bo, Y., et al. (2022) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqac074 · Cited by 185 · see citing works
Mondul, A. M., Moore, S. C., Weinstein, S. J., Karoly, E. D., Sampson, J. N., & Albanes, D. (2015) · International Journal of Cancer · doi:10.1002/ijc.29576 · Cited by 179 · see citing works
The Gut Microbial Metabolite Trimethylamine-N-Oxide Is Present in Human Cerebrospinal Fluid
Del Rio, D., Zimetti, F., Caffarra, P., Tassotti, M., Bernini, F., Brighenti, F., Zini, A., & Zanotti, I. (2017) · Nutrients · doi:10.3390/nu9101053 · Cited by 172 · see citing works
“Similarly, it has been associated with other chronic diseases, such as diabetes [10] and cancer [11], further strengthening the pathological implications of this microbiota metabolite.”
BackgroundFu, B. C., Hullar, M. A. J., Randolph, T. W., Franke, A. A., Monroe, K. R., Cheng, I. C., Wilkens, L. R., Shepherd, J., Madeleine, M. M., Marchand, L. L., et al. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa015 · Cited by 171 · see citing works
Trimethylamine N‐oxide: breathe new life
Subramaniam, S., & Fletcher, C. (2018) · British Journal of Pharmacology · doi:10.1111/bph.13959 · Cited by 171 · see citing works
Bekhit, A. E. A., Giteru, S. G., Holman, B. W. B., & Hopkins, D. L. (2021) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12764 · Cited by 169 · see citing works
Gut Microbiota in Colorectal Cancer: Biological Role and Therapeutic Opportunities
Pandey, H., Tang, D. W. T., Wong, S. H., & Lal, D. (2023) · Cancers · doi:10.3390/cancers15030866 · Cited by 165 · see citing works
Choline metabolism-based molecular diagnosis of cancer: an update
Glunde, K., Penet, M., Jiang, L., Jacobs, M. A., & Bhujwalla, Z. M. (2015) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.2015.1039515 · Cited by 161 · see citing works
Alisson-Silva, F., Kawanishi, K., & Varki, A. (2016) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2016.07.002 · Cited by 156 · see citing works
Wu, J., Wen, X., Faulk, C. D., Boehnke, K. F., Zhang, H., Dolinoy, D. C., & Xi, C. (2016) · Toxicological Sciences · doi:10.1093/toxsci/kfw046 · Cited by 149 · see citing works
Trimethylamine N-Oxide in Relation to Cardiometabolic Health—Cause or Effect?
Papandreou, C., Moré, M. I., & Bellamine, A. (2020) · Nutrients · doi:10.3390/nu12051330 · Cited by 150 · see citing works
Tsiaoussis, J., Antoniou, M. N., Koliarakis, I., Mesnage, R., Vardavas, C. I., Izotov, B. N., Psaroulaki, A., & Tsatsakis, A. M. (2019) · Toxicology Letters · doi:10.1016/j.toxlet.2019.04.014 · Cited by 134 · see citing works
Bist, P., & Choudhary, S. (2022) · Biological Trace Element Research · doi:10.1007/s12011-021-03092-4 · Cited by 132 · see citing works
Trimethylamine N -oxide: A harmful, protective or diagnostic marker in lifestyle diseases?
Nowiński, A., & Ufnal, M. (2017) · Nutrition · doi:10.1016/j.nut.2017.08.001 · Cited by 130 · see citing works
Colon 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
Milk Polar Lipids: Underappreciated Lipids with Emerging Health Benefits
Anto, L., Warykas, S. W., Torres‐Gonzalez, M., & Blesso, C. N. (2020) · Nutrients · doi:10.3390/nu12041001 · Cited by 117 · see citing works
Sánchez‐Alcoholado, L., Ordóñez, R., Otero, A. P., Plaza-Andrades, I. J., Laborda-Illanes, A., Medina, J. A., Ramos‐Molina, B., Gómez‐Millán, J., & Queipo‐Ortuño, M. I. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186782 · Cited by 117 · see citing works
Gut Microbiota-Derived Metabolites in Colorectal Cancer: The Bad and the Challenges
Zhang, W., An, Y., Qin, X., Wu, X., Wang, X., Hou, H., Song, X., Liu, T., Wang, B., Huang, X., et al. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.739648 · Cited by 119 · see citing works
The roles of microbial products in the development of colorectal cancer: a review
Fang, Y., Yan, C., Zhao, Q., Xu, J., Liu, Z., Gao, J., Zhu, H., Dai, Z., Wang, D., & Tang, D. (2021) · Bioengineered · doi:10.1080/21655979.2021.1889109 · Cited by 119 · see citing works
Intra-individual variation of plasma trimethylamine-N-oxide (TMAO), betaine and choline over 1 year
Kühn, T., Rohrmann, S., Sookthai, D., Johnson, T., Katzke, V., Kaaks, R., von Eckardstein, A., & Müller, D. (2017) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2016-0374 · Cited by 110 · see citing works
Gut microbiota-derived metabolites in CRC progression and causation
Dalal, N., Jalandra, R., Bayal, N., Yadav, A. K., Harshulika, Sharma, M., Makharia, G. K., Kumar, P., Singh, R. K., Solanki, P. R., et al. (2021) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-021-03729-w · Cited by 102 · 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
Chan, C. W. H., Law, B. M. H., Waye, M. M. Y., Chan, J. Y., So, W. K. W., & Chow, K. M. (2019) · Journal of Cancer · doi:10.7150/jca.31737 · Cited by 96 · 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
Emerging role of trimethylamine-N-oxide (TMAO) in colorectal cancer
Jalandra, R., Dalal, N., Yadav, A. K., Verma, D., Sharma, M., Singh, R. K., Khosla, A., Kumar, A., & Solanki, P. R. (2021) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-021-11582-7 · Cited by 255 · see citing works
Toxic and essential metals: metabolic interactions with the gut microbiota and health implications
Zhu, Q., Chen, B., Zhang, F., Zhang, B., Guo, Y., Pang, M., Huang, L., & Wang, T. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1448388 · Cited by 100 · see citing works
The complex metabolism of trimethylamine in humans: endogenous and exogenous sources
Chhibber-Goel, J., Gaur, A., Singhal, V., Parakh, N., Bhargava, B., & Sharma, A. (2016) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2016.6 · Cited by 93 · see citing works
Tocchetti, C. G., Ameri, P., de Boer, R. A., D’Alessandra, Y., Russo, M., Sorriento, D., Ciccarelli, M., Kiss, B., Bertrand, L., Dawson, D. K., et al. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa222 · Cited by 90 · see citing works
Contribution of Trimethylamine N-Oxide (TMAO) to Chronic Inflammatory and Degenerative Diseases
Constantino-Jonapa, L. A., Espinoza-Palacios, Y., Escalona‐Montaño, A. R., Hernández-Ruiz, P., Amezcua-Guerra, L. M., Amedei, A., & Aguirre‐García, M. M. (2023) · Biomedicines · doi:10.3390/biomedicines11020431 · Cited by 97 · see citing works
Gurwara, S., Ajami, N. J., Jang, A., Hessel, F. C., Chen, L., Plew, S., Wang, Z., Graham, D. Y., Hair, C. D., White, D. L., et al. (2019) · Nutrients · doi:10.3390/nu11030613 · Cited by 89 · see citing works
Zhou, Y., Zhang, Y., Jin, S., Lv, J., Li, M., & Feng, N. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117031 · Cited by 92 · see citing works
Ocvirk, S., Wilson, A. S., Posma, J. M., Li, J. V., Koller, K. R., Day, G. M., Flanagan, C. A., Otto, E., Sacco, P. E., Sacco, F. D., et al. (2019) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqz301 · Cited by 81 · see citing works
Trimethylamine N-Oxide Promotes Cell Proliferation and Angiogenesis in Colorectal Cancer
Yang, S., Dai, H., Lu, Y., Li, R., Gao, C., & Pan, S. (2022) · Journal of Immunology Research · doi:10.1155/2022/7043856 · Cited by 85 · see citing works
Modesitt, S. C., Hallowell, P. T., Slack‐Davis, J. K., Michalek, R. D., Atkins, K. A., Kelley, S. L., Arapovic, S., Shupnik, M. A., & Hoehn, K. L. (2015) · Gynecologic Oncology · doi:10.1016/j.ygyno.2015.05.015 · Cited by 81 · see citing works
Pb Toxicity on Gut Physiology and Microbiota
Liu, W., Feng, H., Zheng, S., Xu, S., Massey, I. Y., Zhang, C., Wang, X., & Yang, F. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.574913 · Cited by 77 · see citing works
Microbial metabolites in colorectal tumorigenesis and cancer therapy
Liu, Y., Lau, H. C.-H., & Yu, J. Q. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2203968 · Cited by 80 · see citing works
Griffin, L. E., Djurić, Z., Angiletta, C. J., Mitchell, C. M., Baugh, M. E., Davy, K. P., & Neilson, A. P. (2019) · Food & Function · doi:10.1039/c9fo00333a · Cited by 77 · see citing works
Schugar, R. C., Gliniak, C. M., Osborn, L. J., Massey, W. J., Sangwan, N., Horak, A. J., Banerjee, R., Orabi, D., Helsley, R. N., Brown, A. L., et al. (2022) · eLife · doi:10.7554/elife.63998 · Cited by 73 · see citing works
Gut Microbiota-Derived Metabolite Trimethylamine N-Oxide as a Biomarker in Early Parkinson’s Disease
Chung, S. J., Rim, J. H., Ji, D., Lee, S., Yoo, H. S., Jung, J. H., Baik, K., Choi, Y., Ye, B. S., Sohn, Y. H., et al. (2021) · Nutrition · doi:10.1016/j.nut.2020.111090 · Cited by 74 · see citing works
Rombouts, C., Hemeryck, L., HECKE, T. V., SMET, S. D., Vos, W. H. D., & Vanhaecke, L. (2017) · Scientific Reports · doi:10.1038/srep42514 · Cited by 74 · see citing works
Changes in gut microbiota composition after bariatric surgery: a new balance to decode
Palmisano, S., Campisciano, G., Silvestri, M., Guerra, M., Giuricin, M., Casagranda, B., Comar, M., & de Manzini, N. (2020) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-019-04321-x · Cited by 72 · see citing works
Ilyas, A., Wijayasinghe, Y. S., Khan, I., Samaloty, N. M. E., Adnan, M., Dar, T. A., Poddar, N. K., Singh, L. R., Sharma, H., & Khan, S. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.964624 · Cited by 71 · see citing works
Yu, H., Geng, W., Zheng, Z., Gao, J., Guo, D., & Wang, Y. (2019) · Theranostics · doi:10.7150/thno.33459 · Cited by 68 · see citing works
Prospective study of blood metabolites associated with colorectal cancer risk
Shu, X., Xiang, Y., Rothman, N., Yu, D., Li, H., Yang, G., Cai, H., Ma, X., Qing Lan, B., Gao, Y., et al. (2018) · International Journal of Cancer · doi:10.1002/ijc.31341 · Cited by 67 · see citing works
Preoperative Serum TMAO Level is a New Prognostic Marker for Colorectal Cancer
Liu, X., Liu, H., Yuan, C., Zhang, Y., Wang, W., Hu, S., Liu, L., & Wang, Y. (2017) · Biomarkers in Medicine · doi:10.2217/bmm-2016-0262 · Cited by 67 · see citing works
Reichard, C. A., Naelitz, B. D., Wang, Z., Jia, X., Li, J., Stampfer, M. J., Klein, E. A., Hazen, S. L., & Sharifi, N. (2021) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-21-0766 · Cited by 64 · see citing works
Roe, A. J., Zhang, S., Bhadelia, R. A., Johnson, E. J., Lichtenstein, A. H., Rogers, G. T., Rosenberg, I. H., Smith, C. E., Zeisel, S. H., & Scott, T. M. (2017) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.137158 · Cited by 64 · 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
Balancing the Equation: A Natural History of Trimethylamine and Trimethylamine-N-oxide
Loo, R. L., Chan, Q. M., Nicholson, J. K., & Holmes, E. C. (2022) · Journal of Proteome Research · doi:10.1021/acs.jproteome.1c00851 · Cited by 60 · see citing works
Metabolomic epidemiology offers insights into disease aetiology
Fuller, H., Zhu, Y., Nicholas, J. C., Chatelaine, H., Drzymalla, E., Sarvestani, A. K., Julián‐Serrano, S., Tahir, U. A., Sinnott-Armstrong, N., Raffield, L. M., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00903-x · Cited by 61 · see citing works
Garcia, E., Wolak, J. E., Wang, Z., Li, X. S., Bennett, D. W., Connelly, M. A., Otvos, J. D., Hazen, S. L., & Jeyarajah, E. J. (2017) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2017.06.003 · Cited by 62 · see citing works
The metabolic fate of isotopically labeled trimethylamine-N-oxide (TMAO) in humans
Taesuwan, S., Cho, C. E., Malysheva, O. V., Bender, E., King, J. H., Yan, J., Thalacker-Mercer, A. E., & Caudill, M. A. (2017) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2017.02.010 · Cited by 62 · see citing works
Self-citationTacconi, E., Palma, G., Biase, D. D., Luciano, A., Barbieri, M., de Nigris, F., & Bruzzese, F. (2023) · Nutrients · doi:10.3390/nu15030563 · Cited by 62 · see citing works
A Bacterial Microcompartment Is Used for Choline Fermentation by Escherichia coli 536
Herring, T. I., Harris, T. N., Chowdhury, C., Mohanty, S. K., & Bobik, T. A. (2018) · Journal of Bacteriology · doi:10.1128/jb.00764-17 · Cited by 59 · 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
Ungvari, Z., Fekete, M., Varga, P., Lehoczki, A., Munkácsy, G., Fekete, J. T., Bianchini, G., Ocana, A., Buda, A., Ungvari, A., et al. (2025) · GeroScience · doi:10.1007/s11357-025-01646-1 · Cited by 56 · see citing works
Microbial Metabolite Dysbiosis and Colorectal Cancer
Niekamp, P., & Kim, C. H. (2023) · Gut and Liver · doi:10.5009/gnl220260 · Cited by 56 · 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
Microbiota of the gastrointestinal tract: Friend or foe?
Senchukova, M. A. (2023) · World Journal of Gastroenterology · doi:10.3748/wjg.v29.i1.19 · Cited by 55 · see citing works
Mechanisms shared between cancer, heart failure, and targeted anti-cancer therapies
de Wit, S., Glen, C., de Boer, R. A., & Lang, N. N. (2022) · Cardiovascular Research · doi:10.1093/cvr/cvac132 · Cited by 52 · see citing works
Ottiger, M., Nickler, M., Steuer, C., Odermatt, J., Huber, A., Christ‐Crain, M., Henzen, C., Hoess, C., Thomann, R., Zimmerli, W., et al. (2016) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2016.08.017 · Cited by 50 · 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
Mola, S., Pandolfo, C., Sica, A., & Porta, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186866 · Cited by 48 · see citing works
Raj, V., Bhadauria, A. S., Singh, A. K., Kumar, U., Rai, A., Keshari, A. K., Kumar, P., Kumar, D., Maity, B., Nath, S., et al. (2018) · Cytokine · doi:10.1016/j.cyto.2018.03.026 · Cited by 45 · see citing works
Folate and choline absorption and uptake: Their role in fetal development
Radziejewska, A., & Chmurzyńska, A. (2018) · Biochimie · doi:10.1016/j.biochi.2018.12.002 · Cited by 47 · see citing works
Wang, Q., & Xu, R. (2019) · BMC Genomics · doi:10.1186/s12864-019-5510-y · Cited by 46 · see citing works
The metabolic dialogue between intratumoural microbes and cancer: implications for immunotherapy
Situ, Y., Zhang, P., Zhang, C., Jiang, A., Zhang, N., Zhu, L., Mou, W., Liu, Z., Wong, H. Z. H., Zhang, J., et al. (2025) · eBioMedicine · doi:10.1016/j.ebiom.2025.105708 · Cited by 45 · see citing works
Advances in the World of Bacterial Microcompartments
Stewart, A. M., Stewart, K. L., Yeates, T. O., & Bobik, T. A. (2021) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.12.002 · Cited by 45 · see citing works
Mahmud, I., Pinto, F. G., Rubio, V. Y., Lee, B., Pavlovich, C. P., Perera, R. J., & Garrett, T. J. (2021) · Analytical Chemistry · doi:10.1021/acs.analchem.1c00943 · Cited by 44 · see citing works
Wu, Y., Rong, X., Pan, M., Wang, T., Yang, H., Chen, X., Xiao, Z., & Zhao, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.840171 · Cited by 42 · see citing works
Shi, C., de Wit, S., Učambarlić, E., Markousis‐Mavrogenis, G., Screever, E. M., Meijers, W. C., de Boer, R. A., & Aboumsallem, J. P. (2023) · Cancers · doi:10.3390/cancers15030729 · Cited by 42 · see citing works
De-coding the complex role of microbial metabolites in cancer
Escriva, P. P., Bernardino, C. C. T., & Letellier, E. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115358 · Cited by 45 · see citing works
Heaney, L. M., Jones, D. J. L., Mbasu, R. J., Ng, L. L., & Suzuki, T. (2015) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-015-9164-6 · Cited by 41 · see citing works
Enalapril decreases rat plasma concentration of TMAO, a gut bacteria-derived cardiovascular marker
Konop, M., Radkowski, M., Grochowska, M., Perlejewski, K., Samborowska, E., & Ufnal, M. (2018) · Biomarkers · doi:10.1080/1354750x.2018.1432689 · Cited by 41 · see citing works
Cheng, T. D., Makar, K. W., Neuhouser, M. L., Miller, J. W., Song, X., Brown, E. C., Beresford, S. A. A., Zheng, Y., Poole, E. M., Galbraith, R. L., et al. (2015) · Cancer · doi:10.1002/cncr.29465 · Cited by 40 · see citing works
Self-citationNeveu, V., Nicolas, G., Amara, A., Salek, R. M., & Scalbert, A. (2023) · Scientific Reports · doi:10.1038/s41598-022-26366-w · Cited by 40 · 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
Intestinal Macrophages at the Crossroad between Diet, Inflammation, and Cancer
Caprara, G., Allavena, P., & Erreni, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144825 · Cited by 38 · see citing works
Nutrigenomics at the Interface of Aging, Lifespan, and Cancer Prevention
Riscuta, G. (2016) · The Journal of Nutrition · doi:10.3945/jn.116.235119 · Cited by 37 · see citing works
Wang, Q., Huang, H., Yang, Y., Yang, X.-L., Li, X.-M., Zhong, W., Wen, B., He, F., & Li, J. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1491821 · Cited by 47 · see citing works
Huang, J. Y., Luu, H. N., Butler, L. M., Midttun, Ø., Ulvik, A., Wang, R., Jin, A., Gao, Y., Tan, Y., Ueland, P. M., et al. (2020) · International Journal of Cancer · doi:10.1002/ijc.32994 · Cited by 36 · see citing works
Cys34 Adductomics Links Colorectal Cancer with the Gut Microbiota and Redox Biology
Grigoryan, H., Schiffman, C., Gunter, M. J., Naccarati, A., Polidoro, S., Dagnino, S., Dudoit, S., Vineis, P., & Rappaport, S. M. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-1529 · Cited by 35 · see citing works
- Authors
- 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., Miller, J. W., Green, R., Lane, D. S., Beresford, S. A. A., & Caudill, M. A.
- Affiliations
- Cornell University (US)
- German Cancer Research Center (DE)
- Fred Hutch Cancer Center (US)
- University of Georgia (US)
- 2Fred Hutchinson Cancer Research Center, Seattle, Washington.
- Rutgers, The State University of New Jersey (US)
- University of California, Davis (US)
- Stony Brook School (US)
- Corresponding author
- Ulrich, Cornelia M.
- Caudill, Marie A.
- ORCID
- Venue
- Cancer Research
- Published
- 2014-12-14
- Volume
- 74
- Issue
- 24
- Pages
- 7442-7452
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- PMC
- PMC4268282
- OpenAlex
- W2092436074
- Cited by
- 253
- References
- 56
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 27 · 2023: 34 · 2022: 23 · 2021: 34 · 2020: 24 · 2019: 20 · 2018: 19 · 2017: 17 · 2016: 16 · 2015: 13
- FWCI
- 15.26
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Health and Human Services
- National Institutes of Health (HHSN268201100004C, n01wh22110-38-0-0, HHSN268201100001C, HHSN268201100002C, HHSN268201100003C, N01 WH022110)
- National Institute on Aging (HHSN-271-2011-00004C,)
- National Heart, Lung, and Blood Institute (HHSN2682011-00001I, HHSN2682011-00002I, HHSN2682011‐00004I, HHSN268201100046C, HHSN2682011-00003I)
- National Cancer Institute (R01CA120523)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Keywords
- colorectal cancer risk, choline metabolism, plasma choline, betaine, dimethylglycine, trimethylamine N-oxide, rectal cancer, postmenopausal women, vitamin B12, tumor location, tumor stage, plasma biomarkers, Women's Health Initiative Observational Study, gut microbiota, oxidative stress, inflammation
- MeSH terms
- Aged, Betaine, Choline, Female, Humans, Methylamines, Middle Aged, Risk Factors, Colorectal Neoplasms, Women's Health
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