Effect of egg ingestion on trimethylamine-N-oxide production in humans: a randomized, controlled, dose-response study , , ,
Open accessAbstract
Background It is important to understand whether eating eggs, which are a major source of dietary choline, results in increased exposure to trimethylamine-N-oxide (TMAO), which is purported to be a risk factor for developing heart disease.Objective We determined whether humans eating eggs generate TMAO and, if so, whether there is an associated increase in a marker for inflammation [ie, high-sensitivity C-reactive protein (hsCRP)] or increased oxidation of low-density lipoprotein (LDL).Design In a longitudinal, double-blind, randomized dietary intervention, 6 volunteers were fed breakfast doses of 0, 1, 2, 4, or 6 egg yolks. Diets were otherwise controlled on the day before and day of each egg dose with a standardized low-choline menu. Plasma TMAO at timed intervals (immediately before and 1, 2, 4, 8, and 24 h after each dose), 24-h urine TMAO, predose and 24-h postdose serum hsCRP, and plasma oxidized LDL were measured. Volunteers received all 5 doses with each dose separated by >2-wk washout periods.Results The consumption of eggs was associated with increased plasma and urine TMAO concentrations (P < 0.01), with ∼14% of the total choline in eggs having been converted to TMAO. There was considerable variation between individuals in the TMAO response. There was no difference in hsCRP or oxidized LDL concentrations after egg doses.Conclusions The consumption of ≥2 eggs results in an increased formation of TMAO. Choline is an essential nutrient that is required for normal human liver and muscle functions and important for normal fetal development. Additional study is needed to both confirm the association between TMAO and atherosclerosis and identify factors, microbiota and genetic, that influence the generation of TMAO before policy and medical recommendations are made that suggest reduced dietary choline intake.
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Studies have shown dose-dependent TMA/TMAO formation with egg ingestion.
“Studies have also shown dose-dependent TMA/TMAO formation with egg ingestion.2,18”
From Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women (2019) · cites this paper as [18]
About 15% of egg PtdCho was converted to TMA, and peak plasma TMA occurred 6 to 8 h after egg ingestion.
“About 15% of the PtdCho in eggs was converted to TMA, and peak plasma TMA concentrations were achieved between 6 and 8 h after ingestion of the eggs (79).”
From Trimethylamine <i>N</i> -Oxide, the Microbiome, and Heart and Kidney Disease (2017) · cites this paper as [79]
Consuming at least two eggs, which contain mostly PtdCho, increases TMAO formation.
“However, consumption of ≥2 eggs, which contain mostly PtdCho, results in increased formation of TMAO (79,110).”
From Trimethylamine <i>N</i> -Oxide, the Microbiome, and Heart and Kidney Disease (2017) · cites this paper as [79]
After an egg-containing meal, plasma TMAO peaks at 6 to 8 h and returns to baseline by 24 h.
“After people consume a meal containing eggs, TMAO concentrations in plasma peak at 6 to 8 h and return to baseline by 24 h after the meal (79).”
From Trimethylamine <i>N</i> -Oxide, the Microbiome, and Heart and Kidney Disease (2017) · cites this paper as [79]
Other factors, such as host genotype, besides the abundance of TMA-producing bacteria may account for differences in TMAO accumulation.
“suggest that other factors (e.g., host genotype) besides the abundance of TMA-producing bacteria may account for differences in TMAO accumulation (25).”
Cites
A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/o59-099 · Cited by 54,751 · see citing works
Toprak, Ö., Kurt, H., Sarı, Y., Şarkış, C., Us, H., & Kırık, A. (2017) · Kidney & Blood Pressure Research · doi:10.1159/000468530 · Cited by 29,769 · see citing works
A New Equation to Estimate Glomerular Filtration Rate
Levey, A. S., Stevens, L. A., Schmid, C. H., Zhang, Y. (., Castro, A. F., Feldman, H. I., Kusek, J. W., Eggers, P., Van Lente, F., Greene, T., et al. (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-150-9-200905050-00006 · Cited by 25,603 · see citing works
Obesity alters gut microbial ecology
Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., & Gordon, J. I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504978102 · Cited by 6,176 · 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
Self-citationIntestinal 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
Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk
Tang, W. H. W., Wang, Z., Levison, B. S., Koeth, R. A., Britt, E. B., Fu, X., Wu, Y., & Hazen, S. L. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1109400 · Cited by 3,402 · see citing works
Bennett, B. J., Vallim, T. Q. D. A., Wang, Z., Shih, D. M., Meng, Y., Gregory, J., Allayee, H., Lee, R., Graham, M., Crooke, R., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2012.12.011 · Cited by 1,070 · see citing works
Self-citationThe core gut microbiome, energy balance and obesity
Turnbaugh, P. J., & Gordon, J. I. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.174136 · Cited by 993 · see citing works
He, K., Song, Y., Daviglus, M. L., Liu, K., Van Horn, L., Dyer, A. R., & Greenland, P. (2004) · Circulation · doi:10.1161/01.cir.0000132503.19410.6b · Cited by 764 · see citing works
Concentrations 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
Self-citationSex and menopausal status influence human dietary requirements for the nutrient choline
Fischer, L. M., Costa, K. A. D., Kwock, L., Stewart, P. W., Lu, T.-S., Stabler, S. P., Allen, R. H., & Zeisel, S. H. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.5.1275 · Cited by 347 · see citing works
Self-citationSvanborg, A., Svennerholm, L. T., Myrén, I., Soomägi, M. R., CLAESSON, B. O., & Rohman, S. (1961) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1961.tb17091.x · Cited by 326 · see citing works
Koç, H., Mar, M.-H. H., Ranasinghe, A., Swenberg, J. A., & Zeisel, S. H. (2002) · Analytical Chemistry · doi:10.1021/ac025624x · Cited by 294 · see citing works
Self-citationFish consumption and cardiovascular disease in the physicians’ health study: A prospective study
Morris, M. C., Manson, J. E., Rosner, B., Buring, J. E., Willett, W. C., & Hennekens, C. H. (1995) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a117615 · Cited by 268 · cited 1× · see citing works
“However, no evidence of an association between dietary intake of fish and any cardiovascular endpoint was observed in the Physicians’ Health Study (20), and a meta-analysis of 11 available cohort studies concluded that fish consumption is inversely associated with fatal coronary heart disease (21).”
BackgroundFormation of methylamines from ingested choline and lecithin.
Zeisel, S. H., Wishnok, J. S., & Blusztajn, J. K. (1983) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)33590-1 · Cited by 253 · see citing works
Self-citationBidulescu, 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
Self-citationBlesso, C. N., Andersen, C. J., Barona, J., Volek, J. S., & Fernández, M. L. (2012) · Metabolism · doi:10.1016/j.metabol.2012.08.014 · Cited by 142 · see citing works
Dalmeijer, 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
daCosta, K.-A., Vrbanac, J. J., & Zeisel, S. H. (1990) · Analytical Biochemistry · doi:10.1016/0003-2697(90)90449-j · Cited by 93 · see citing works
Self-citationMorley, J. E. (2010) · Clinics in Geriatric Medicine · doi:10.1016/j.cger.2009.11.005 · Cited by 87 · see citing works
Nutrition in pregnancy: the argument for including a source of choline
Zeisel, S. H. (2013) · International Journal of Women s Health · doi:10.2147/ijwh.s36610 · Cited by 84 · see citing works
Self-citationIncrease in human exposure to methylamine precursors of N-nitrosamines after eating fish.
Zeisel, S. H., & daCosta, K. A. (1986) · PubMed · Cited by 70 · see citing works
Self-citationMALIGNANT MELANOMA AND FLUORESCENT LIGHTING
Carlton-Foss, J., Beral, V., & Evans, S. (1982) · The Lancet · doi:10.1016/s0140-6736(82)92704-0 · Cited by 65 · see citing works
Yamazaki, H., & Shimizu, M. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.03.020 · Cited by 65 · see citing works
AMINE METABOLISM AND THE SMALL BOWEL IN URqMIA
Simenhoff, M. L. (1976) · The Lancet · doi:10.1016/s0140-6736(76)91207-1 · Cited by 62 · see citing works
Growdon, J. H., Cohen, E. L., & Wurtman, R. J. (1977) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1977.tb07732.x · Cited by 60 · see citing works
Katz, D. L., Gnanaraj, J., Treu, J. A., Ma, Y., Kavak, Y., & Njike, V. Y. (2014) · American Heart Journal · doi:10.1016/j.ahj.2014.10.001 · Cited by 49 · see citing works
An in Vitro Study of Choline Uptake by Intestine from Neonatal and Adult Rats
Sheard, N. F., & Zeisel, S. H. (1986) · Pediatric Research · doi:10.1203/00006450-198608000-00014 · Cited by 44 · see citing works
Self-citationCholine and lecithin administration to patients with tardive dyskinesia.
Growdon, J. H., & Gelenberg, A. J. (1978) · PubMed · Cited by 7 · see citing works
Katz, D. L., Ma, Y., Kavak, Y., & Njike, V. Y. (2013) · The FASEB Journal · doi:10.1096/fasebj.27.1_supplement.225.6 · Cited by 2 · see citing works
Flagged first, then by citations
1 of the 32 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
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
The Gut Microbiota and Inflammation: An Overview
Bander, Z. A., Nitert, M. D., Mousa, A., & Naderpoor, N. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17207618 · Cited by 783 · see citing works
Bechthold, A., Boeing, H., Schwedhelm, C., Hoffmann, G., Knüppel, S., Iqbal, K., De Henauw, S., Michels, N., Devleesschauwer, B., Schlesinger, S., et al. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2017.1392288 · Cited by 693 · see citing works
“Eggs are a major source of dietary choline and consumption results in increased exposure to trimethylamine-N -oxide, a metabolite linked to atherosclerosis (Miller et al. 2014; Senthong et al. 2016).”
The contributory role of gut microbiota in cardiovascular disease
Tang, W. H. W., & Hazen, S. L. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72331 · Cited by 641 · see citing works
Wang, Z., Bergeron, N., Levison, B. S., Li, X. S., Chiu, S., Jia, X., Koeth, R. A., Li, L., Wu, Y., Tang, W. H. W., et al. (2019) · European Heart Journal · doi:10.1093/eurheartj/ehy799 · Cited by 496 · 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
Self-citationFennema, D., Phillips, I. R., & Shephard, E. A. (2016) · Drug Metabolism and Disposition · doi:10.1124/dmd.116.070615 · Cited by 355 · see citing works
Missailidis, C., Hällqvist, J., Qureshi, A. R., Barany, P., Heimbürger, O., Lindholm, B., Stenvinkel, P., & Bergman, P. (2016) · PLOS ONE · doi:10.1371/journal.pone.0141738 · Cited by 338 · see citing works
Gut reactions: Breaking down xenobiotic–microbiome interactions
Clarke, G., Sandhu, K. V., Griffin, B. T., Dinan, T. G., Cryan, J. F., & Hyland, N. P. (2019) · Pharmacological Reviews · doi:10.1124/pr.118.015768 · Cited by 319 · 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
Dietary Choline Intake: Current State of Knowledge Across the Life Cycle
Wiedeman, A. M., Barr, S. I., Green, T., Xu, Z., Innis, S. M., & Kitts, D. D. (2018) · Nutrients · doi:10.3390/nu10101513 · Cited by 318 · see citing works
TMAO: how gut microbiota contributes to heart failure
Zhang, Y., Wang, Y., Ke, B., & Du, J. (2020) · Translational research · doi:10.1016/j.trsl.2020.08.007 · Cited by 306 · see citing works
Senthong, V., Wang, Z., Li, X. S., Fan, Y., Wu, Y., Wilson Tang, W. H., & Hazen, S. L. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.115.002816 · Cited by 270 · 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
Diabetes is Associated with Higher Trimethylamine N-oxide Plasma Levels
Dambrova, M., Latkovskis, G., Kuka, J., Strele, I., Konrade, I., Grinberga, S., Hartmane, D., Pugovics, O., Erglis, A., & Liepinsh, E. (2016) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0035-1569330 · Cited by 229 · see citing works
Metabolic, Epigenetic, and Transgenerational Effects of Gut Bacterial Choline Consumption
Romano, K. A., Martinez-del Campo, A., Kasahara, K., Chittim, C. L., Vivas, E. I., Amador-Noguez, D., Balskus, E. P., & Rey, F. E. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.07.021 · Cited by 224 · see citing works
Hoyles, L., Pontifex, M. G., Rodriguez-Ramiro, I., Anis-Alavi, M. A., Jelane, K. S., Snelling, T., Solito, E., Fonseca, S., Carvalho, A. L., Carding, S. R., et al. (2021) · Microbiome · doi:10.1186/s40168-021-01181-z · Cited by 221 · see citing works
Trimethylamine N-oxide (TMAO) in human health
Gątarek, P., & Kałużna-Czaplińska, J. (2020) · EXCLI journal · doi:10.17179/excli2020-3239 · Cited by 233 · 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
Sánchez-Rodríguez, E., Egea-Zorrilla, A., Plaza‐Díaz, J., Aragón‐Vela, J., Muñoz‐Quezada, S., Tercedor‐Sánchez, L., & Abadía‐Molina, F. (2020) · Nutrients · doi:10.3390/nu12030605 · Cited by 220 · see citing works
A metabolomic study of biomarkers of meat and fish intake
Cheung, W., Keski-Rahkonen, P., Assi, N., Ferrari, P., Freisling, H., Rinaldi, S., Slimani, N., Zamora-Ros, R., Rundle, M., Frost, G., et al. (2017) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.146639 · Cited by 206 · 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
Gut microbiota in atherosclerosis: focus on trimethylamine N‐oxide
Zhu, Y., Li, Q., & Jiang, H. (2020) · Apmis · doi:10.1111/apm.13038 · Cited by 204 · see citing works
Ge, X., Zheng, L., Zhuang, R., Yu, P., Xu, Z., Liu, G., Xi, X., Zhou, X., & Fan, H. (2019) · Advances in Nutrition · doi:10.1093/advances/nmz064 · Cited by 194 · see citing works
Sherriff, J. L., O’Sullivan, T. A., Properzi, C., Oddo, J.-L., & Adams, L. A. (2016) · Advances in Nutrition · doi:10.3945/an.114.007955 · Cited by 191 · see citing works
Zhuang, R., Ge, X., Han, L., Yu, P., Gong, X., Meng, Q., Zhang, Y., Fan, H., Zheng, L., Liu, Z., et al. (2019) · Obesity Reviews · doi:10.1111/obr.12843 · Cited by 184 · see citing works
Heianza, Y., Sun, D., Li, X., DiDonato, J. A., Bray, G. A., Sacks, F. M., & Qi, L. (2019) · Gut · doi:10.1136/gutjnl-2018-316155 · Cited by 177 · see citing works
Gut Microbiota and Ischemic Stroke: The Role of Trimethylamine N-Oxide
Nam, H. S. (2019) · Journal of Stroke · doi:10.5853/jos.2019.00472 · Cited by 176 · 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
“For TMAO quantification, before the analysis, each sample was added with TMAO-d9 as internal standard and then extracted with acidified acetonitrile, as previously described [6].”
MethodMeyer, K. A., Benton, T. Z., Bennett, B. J., Jacobs, D. R., Lloyd‐Jones, D. M., Gross, M. D., Carr, J. J., Gordon‐Larsen, P., & Zeisel, S. H. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.116.003970 · Cited by 167 · see citing works
Self-citationDietary Reference Values for choline
EFSA Panel on Dietetic Products, N. A. A. (. (2016) · EFSA Journal · doi:10.2903/j.efsa.2016.4484 · Cited by 163 · see citing works
Egg Phospholipids and Cardiovascular Health
Blesso, C. N. (2015) · Nutrients · doi:10.3390/nu7042731 · Cited by 157 · see citing works
Bioactive Egg Components and Inflammation
Andersen, C. J. (2015) · Nutrients · doi:10.3390/nu7095372 · Cited by 150 · 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
Wozniak, J. R., Fuglestad, A. J., Eckerle, J. K., Fink, B. A., Hoecker, H. L., Boys, C. J., Radke, J. P., Kroupina, M., Miller, N. C., Brearley, A. M., et al. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.099168 · Cited by 131 · see citing works
Self-citationBarrea, L., Annunziata, G., Muscogiuri, G., Laudisio, D., Somma, C. D., Maisto, M., Tenore, G. C., Colao, A., & Savastano, S. (2018) · Nutrition · doi:10.1016/j.nut.2018.11.015 · Cited by 131 · 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
Spence, J. D. (2019) · Nutrients · doi:10.3390/nu11030647 · Cited by 130 · see citing works
Qin, C., Lv, J., Yu, C., Bian, Z., Si, J., Yang, L., Chen, Y., Zhou, Y., Zhang, H., Liu, J., et al. (2018) · Heart · doi:10.1136/heartjnl-2017-312651 · Cited by 127 · see citing works
The Impact of Egg Nutrient Composition and Its Consumption on Cholesterol Homeostasis
Kuang, H., Yang, F., Zhang, Y., Wang, T., & Chen, G. (2018) · Cholesterol · doi:10.1155/2018/6303810 · Cited by 128 · see citing works
Obeid, R., Awwad, H. M., Rabagny, Y., Graeber, S., Herrmann, W., & Geisel, J. (2016) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.121269 · Cited by 117 · see citing works
Meyer, K. A., & Shea, J. (2017) · Nutrients · doi:10.3390/nu9070711 · Cited by 115 · see citing works
Krüger, R., Merz, B., Rist, M. J., Ferrario, P. G., Bub, A., Kulling, S. E., & Watzl, B. (2017) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201700363 · Cited by 114 · 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
Simó, C., & García‐Cañas, V. (2020) · Food & Function · doi:10.1039/d0fo01237h · Cited by 110 · see citing works
Nutrients Turned into Toxins: Microbiota Modulation of Nutrient Properties in Chronic Kidney Disease
Fernández-Prado, R., Esteras, R., Pérez-Gómez, M., Gracia-Iguacel, C., González-Parra, E., Sanz, A., Ortiz, A., & Sánchez-Niño, M. (2017) · Nutrients · doi:10.3390/nu9050489 · Cited by 89 · see citing works
Sankowski, B., Księżarczyk, K., Raćkowska, E., Szlufik, S., Koziorowski, D., & Giebułtowicz, J. (2020) · Clinica Chimica Acta · doi:10.1016/j.cca.2019.10.038 · Cited by 105 · see citing works
Usual Choline Intakes Are Associated with Egg and Protein Food Consumption in the United States
Wallace, T. C., & Fulgoni, V. L. I. (2017) · Nutrients · doi:10.3390/nu9080839 · Cited by 101 · see citing works
Bergeron, N., Williams, P. T., Lamendella, R., Faghihnia, N., Grube, A., Li, X., Wang, Z., Knight, R. D., Jansson, J. K., Hazen, S. L., et al. (2016) · British Journal Of Nutrition · doi:10.1017/s0007114516004165 · Cited by 101 · see citing works
Gut Microbiota and Atherosclerosis—Focusing on the Plaque Stability
Shen, X., Li, L., Sun, Z., Zang, G., Zhang, L., Shao, C., & Wang, Z. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.668532 · Cited by 99 · see citing works
Trimethylamine-N-oxide: A Novel Biomarker for the Identification of Inflammatory Bowel Disease
Wilson, A. S., Teft, W. A., Morse, B. L., Choi, Y., Woolsey, S., DeGorter, M. K., Hegele, R. A., Tirona, R. G., & Kim, R. B. (2015) · Digestive Diseases and Sciences · doi:10.1007/s10620-015-3797-3 · Cited by 97 · 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
Aldana-Hernández, P., Leonard, K.-A., Zhao, Y.-Y., Curtis, J. M., Field, C. J., & Jacobs, R. L. (2020) · The Journal of Nutrition · doi:10.1093/jn/nxz214 · Cited by 91 · see citing works
DiMarco, D. M., Missimer, A., Murillo, A. G., Lemos, B. S., Malysheva, O., Caudill, M. A., Blesso, C. N., & Fernández, M. L. (2017) · Lipids · doi:10.1007/s11745-017-4230-9 · Cited by 91 · see citing works
Zeng, Y., Guo, M., Xia, F., Teng, F., Tan, X., Li, X., Wang, M., Long, Y., & Xu, Y. (2021) · Advances in Nutrition · doi:10.1093/advances/nmab010 · Cited by 88 · see citing works
Egg consumption and risk of type 2 diabetes: a meta-analysis of prospective studies
Djoussé, L., Khawaja, O. A., & Gaziano, J. M. (2016) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.119933 · Cited by 83 · see citing works
Iannotti, L. L., Lutter, C. K., Waters, W. F., Gallegos-Riofrío, C. A., Malo, C., Reinhart, G. A., Palacios, A. M., Karp, C. A., Chapnick, M., Cox, K. L., et al. (2017) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.117.160515 · Cited by 83 · see citing works
Koppe, L., Fouque, D., & Soulage, C. (2018) · Toxins · doi:10.3390/toxins10040155 · Cited by 83 · see citing works
Egg consumption, cardiovascular diseases and type 2 diabetes
Geiker, N. R. W., Larsen, M. L., Dyerberg, J., Stender, S., & Astrup, A. V. (2017) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2017.153 · Cited by 80 · see citing works
Heianza, Y., Sun, D., Smith, S. R., Bray, G. A., Sacks, F. M., & Qi, L. (2018) · Diabetes Care · doi:10.2337/dc17-2108 · Cited by 80 · see citing works
Carey, J. N., Mettert, E. L., Roggiani, M., Myers, K. S., Kiley, P. J., & Goulian, M. (2018) · Cell · doi:10.1016/j.cell.2018.02.005 · Cited by 77 · see citing works
Cho, C. E., Aardema, N. D. J., Bunnell, M. L., Larson, D. P., Aguilar, S., Bergeson, J., Malysheva, O., Caudill, M. A., & Lefevre, M. (2020) · Nutrients · doi:10.3390/nu12082220 · Cited by 76 · see citing works
Egg consumption and heart health: A review
Clayton, Z. S., Fusco, E., & Kern, M. (2016) · Nutrition · doi:10.1016/j.nut.2016.12.014 · Cited by 75 · see citing works
Ottiger, M., Nickler, M., Steuer, C., Bernasconi, L., Huber, A., Christ‐Crain, M., Henzen, C., Hoess, C., Thomann, R., Zimmerli, W., et al. (2017) · Nutrition · doi:10.1016/j.nut.2017.07.001 · Cited by 75 · see citing works
Trimethylamine N -oxide: heart of the microbiota–CVD nexus?
Naghipour, S., Cox, A. J., Peart, J. N., Toit, E. F. D., & Headrick, J. P. (2020) · Nutrition Research Reviews · doi:10.1017/s0954422420000177 · Cited by 75 · see citing works
Eggs: Healthy or Risky? A Review of Evidence from High Quality Studies on Hen’s Eggs
Myers, M., & Ruxton, C. H. S. (2023) · Nutrients · doi:10.3390/nu15122657 · Cited by 82 · see citing works
Phillips, I. R., & Shephard, E. A. (2019) · Xenobiotica · doi:10.1080/00498254.2019.1643515 · Cited by 71 · see citing works
Chan, M. M.-Y., Yang, X., Wang, H., Saaoud, F., Sun, Y., & Fong, D. (2019) · Nutrients · doi:10.3390/nu11081821 · Cited by 68 · see citing works
Biomarker of food intake for assessing the consumption of dairy and egg products
Münger, L. H., Garcia‐Aloy, M., Vázquez‐Fresno, R., Gille, D., Rosana, A. R. R., Passerini, A., Soria-Florido, M. T., Pimentel, G., Sajed, T., Wishart, D. S., et al. (2018) · Genes & Nutrition · doi:10.1186/s12263-018-0615-5 · Cited by 68 · 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
Costabile, G., Vetrani, C., Bozzetto, L., Giacco, R., Bresciani, L., Rio, D. D., Vitale, M., Pepa, G. D., Brighenti, F., Riccardi, G., et al. (2021) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqab188 · Cited by 67 · see citing works
Virtanen, J. K., Mursu, J., Virtanen, H. E., Fogelholm, M., Salonen, J. T., Koskinen, T. T., Voutilainen, S., & Tuomainen, T. (2016) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.122317 · Cited by 67 · see citing works
Gurven, M., Trumble, B. C., Stieglitz, J., Blackwell, A. D., Michalik, D. E., Finch, C. E., & Kaplan, H. S. (2016) · Evolution Medicine and Public Health · doi:10.1093/emph/eow028 · Cited by 67 · see citing works
Emerging roles of flavin monooxygenase 3 in cholesterol metabolism and atherosclerosis
Schugar, R. C., & Brown, J. M. (2015) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000215 · Cited by 65 · see citing works
Egg consumption and cardiovascular risk: a dose–response meta-analysis of prospective cohort studies
Godos, J., Micek, A., Brzostek, T., Toledo, E., Iacoviello, L., Astrup, A. V., Franco, O. H., Galvano, F., Martínez‐González, M. Á., & Grosso, G. (2020) · European Journal of Nutrition · doi:10.1007/s00394-020-02345-7 · Cited by 65 · see citing works
Zhao, X., Zeisel, S. H., & Zhang, S. (2015) · Electrophoresis · doi:10.1002/elps.201500055 · Cited by 63 · see citing works
Self-citationDietary reference values for chloride
EFSA Panel on Nutrition, N. F. A. F. A. (., Turck, D., Castenmiller, J. J. M., Henauw, S. D., Hirsch‐Ernst, K. I., Kearney, J., Knutsen, H. K., Maciuk, A., Mangelsdorf, I., McArdle, H. J., et al. (2019) · EFSA Journal · doi:10.2903/j.efsa.2019.5779 · Cited by 65 · 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
Diet‐derived microbial metabolites in health and disease
Roager, H. M., & Dragsted, L. O. (2019) · Nutrition Bulletin · doi:10.1111/nbu.12396 · Cited by 60 · see citing works
Mei, Z., Chen, G., Wang, Z., Usyk, M., Yu, B., Baeza, Y. V., Humphrey, G. C., Benítez, R. A. S., Li, J., Williams-Nguyen, J. S., et al. (2021) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqab001 · Cited by 60 · see citing works
Farhangi, M. A., & Vajdi, M. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1770199 · Cited by 59 · see citing works
Trimethylamine-N-Oxide Pathway: A Potential Target for the Treatment of MAFLD
Li, X., Hong, J. W., Wang, Y., Pei, M., Wang, L., & Gong, Z. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.733507 · Cited by 58 · see citing works
Trimethylamine N-Oxide From Gut Microbiota in Chronic Kidney Disease Patients: Focus on Diet
Moraes, C., Fouque, D. P., Amaral, A. C. F., & Mafra, D. (2015) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2015.06.004 · Cited by 57 · see citing works
Pignanelli, M., Bogiatzi, C., Gloor, G. B., Allen‐Vercoe, E., Reid, G., Urquhart, B. L., Ruetz, K. N., Velenosi, T. J., & Spence, J. D. (2018) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2018.05.007 · Cited by 57 · see citing works
Association of Urinary and Plasma Levels of Trimethylamine N-Oxide (TMAO) with Foods
Lombardo, M., Aulisa, G., Marcon, D., Rizzo, G., Tarsisano, M. G., Renzo, L. D., Federici, M., Caprio, M., & LORENZO, A. D. (2021) · Nutrients · doi:10.3390/nu13051426 · Cited by 55 · see citing works
Chen, S. X., Jiang, P., Yu, D., Liao, G., Wu, S., Fang, A., Chen, P., Wang, X., Luo, Y., Long, J., et al. (2020) · European Journal of Nutrition · doi:10.1007/s00394-020-02278-1 · Cited by 56 · see citing works
Zhu, C., Sawrey‐Kubicek, L., Bardagjy, A. S., Houts, H. E., Tang, X., Sacchi, R., Randolph, J., Steinberg, F. M., & Zivkovic, A. M. (2020) · Nutrition Research · doi:10.1016/j.nutres.2020.04.002 · Cited by 54 · see citing works
Association of diet with circulating trimethylamine-N-oxide concentration
Hamaya, R., Ivey, K. L., Lee, D. H., Wang, M., Li, J., Franke, A. A., Sun, Q., & Rimm, E. B. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa225 · Cited by 53 · see citing works
Gessner, A., di Giuseppe, R., Koch, M., Fromm, M. F., Lieb, W., & Maas, R. (2020) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2019-1146 · Cited by 51 · 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
Pignanelli, M., Just, C., Bogiatzi, C., Dinculescu, V., Gloor, G. B., Allen‐Vercoe, E., Reid, G., Urquhart, B. L., Ruetz, K. N., Velenosi, T. J., et al. (2018) · Nutrients · doi:10.3390/nu10060779 · Cited by 48 · see citing works
Richard, C., Cristall, L., Fleming, E., Lewis, E. D., Ricupero, M., Jacobs, R. L., & Field, C. J. (2017) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2016.12.002 · Cited by 48 · see citing works
Malinowska, A. M., Szwengiel, A., & Chmurzyńska, A. (2016) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637486.2016.1256379 · Cited by 47 · see citing works
Yu, Z., Zhang, L., Jiang, X., Xue, C., Chi, N., Zhang, T., & Wang, Y. (2020) · Journal of Food Science · doi:10.1111/1750-3841.15186 · Cited by 47 · see citing works
Wiese, G. N., Biruete, A., Moorthi, R. N., Moe, S. M., Lindemann, S. R., & Gallant, K. M. H. (2020) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2020.04.007 · Cited by 46 · see citing works
Lemos, B. S., Vera, I., Malysheva, O., Caudill, M. A., & Fernández, M. L. (2018) · Journal of the American College of Nutrition · doi:10.1080/07315724.2018.1466213 · Cited by 46 · see citing works
Drouin‐Chartier, J., Schwab, A. L., Chen, S., Li, Y., Sacks, F. M., ROSNER, B. A., Manson, J. E., Willett, W. C., Stampfer, M. J., Hu, F. B., et al. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa115 · Cited by 46 · see citing works
Prenatal and Postnatal Choline Supplementation in Fetal Alcohol Spectrum Disorder
Ernst, A. M., Gimbel, B. A., de Water, E., Eckerle, J. K., Radke, J. P., Georgieff, M., & Wozniak, J. R. (2022) · Nutrients · doi:10.3390/nu14030688 · Cited by 46 · see citing works
Argyridou, S., Davies, M. J., Biddle, G. J. H., Bernieh, D., Suzuki, T., Dawkins, N. P., Rowlands, A. V., Khunti, K. K., Yates, T. E., & Smith, A. C. (2021) · Journal of Nutrition · doi:10.1093/jn/nxab046 · Cited by 44 · see citing works
Smallwood, T., Allayee, H., & Bennett, B. J. (2015) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000259 · Cited by 42 · see citing works
Self-citation
- Authors
- Miller, C. A., Corbin, K. D., da Costa, K.-A., Zhang, S., Zhao, X., Galanko, J. A., Blevins, T., Bennett, B. J., O’Connor, A., & Zeisel, S. H.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Venue
- The American Journal of Clinical Nutrition
- Publisher
- Elsevier BV
- Published
- 2014-09
- Volume
- 100
- Issue
- 3
- Pages
- 778-786
- ISSN
- 0002-9165 (ISSN-L)
- PMC
- PMC4135488
- OpenAlex
- W2073054952
- Cited by
- 240
- References
- 32
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 11 · 2023: 14 · 2022: 16 · 2021: 27 · 2020: 30 · 2019: 25 · 2018: 29 · 2017: 23 · 2016: 24 · 2015: 16 · 2014: 3
- FWCI
- 21.89
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal of Clinical Nutrition (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (DK56350, P30DK034987, P30DK056350)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- trimethylamine N-oxide, dietary choline, dietary cholesterol, gut microbiota, C-reactive protein, inflammation, oxidized LDL, atherosclerosis risk, dose-response relationship
- MeSH terms
- Adult, C-Reactive Protein, Choline, Double-Blind Method, Egg Yolk, Eggs, Female, Heart Diseases, Humans, Lipoproteins, LDL, Longitudinal Studies, Male, Methylamines, Middle Aged, North Carolina, Pilot Projects, Risk Factors, Biomarkers, Up-Regulation, Cross-Over Studies
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