The gut microbiota metabolism of pomegranate or walnut ellagitannins yields two urolithin-metabotypes that correlate with cardiometabolic risk biomarkers: Comparison between normoweight, overweight-obesity and metabolic syndrome

Clinical Nutrition

Volumn 37, Issue 3, 2018, Pages 897-905

  Selma, María V ^a   González Sarrías, Antonio ^a   Salas Salvadó, Jordi ^b,c   Andrés Lacueva, Cristina ^d   Alasalvar, Cesarettin ^e   Örem, Asım ^f   Tomás Barberán, Francisco A ^a   Espín, Juan C ^a  

^a RESEARCH GROUP ON QUALITY   (Spain)

^b HOSPITAL UNIVERSITARI SANT JOAN DE REUS   (Spain)

^c Instituto de Salud Carlos III   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e MATERIALS INSTITUTE   (Turkey)

^f KARADENIZ TECHNICAL UNIVERSITY   (Turkey)

Author keywords

Cardiovascular; Ellagic acid; Gut microbiota; Metabotype; Obesity; Polyphenols

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN B; ELLAGITANNIN; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; OXIDIZED LOW DENSITY LIPOPROTEIN; POMEGRANATE EXTRACT; UNCLASSIFIED DRUG; UROLITHIN A; UROLITHIN B; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL; 3,8-DIHYDROXY-6H-DIBENZO(B,D)PYRAN-6-ONE; BIOLOGICAL MARKER; COUMARIN DERIVATIVE; LIPID; PLANT EXTRACT; TANNIN;

ACTINOBACTERIA; ADULT; ALMOND; ARTICLE; BODY MASS; CLINICAL ARTICLE; CONTROLLED STUDY; DIETARY INTAKE; ELECTROSPRAY MASS SPECTROMETRY; FEMALE; GORDONIBACTER; HAZELNUT; HEALTH STATUS; HUMAN; INTESTINE FLORA; LIMIT OF QUANTITATION; MALE; METABOLIC SYNDROME X; NONHUMAN; OBESITY; POMEGRANATE; PROSPECTIVE STUDY; REAL TIME POLYMERASE CHAIN REACTION; RISK FACTOR; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; WALNUT; BLOOD; BODY WEIGHT; CARDIOVASCULAR DISEASE; CHEMISTRY; COMPARATIVE STUDY; FRUIT; LYTHRACEAE; METABOLISM; MIDDLE AGED; NUT; PHYSIOLOGY;

ADULT; BIOMARKERS; BODY MASS INDEX; BODY WEIGHT; CARDIOVASCULAR DISEASES; COUMARINS; FEMALE; FRUIT; GASTROINTESTINAL MICROBIOME; HUMANS; HYDROLYZABLE TANNINS; JUGLANS; LIPIDS; MALE; METABOLIC SYNDROME; MIDDLE AGED; NUTS; OBESITY; OVERWEIGHT; PLANT EXTRACTS; PUNICACEAE; RISK FACTORS;

EID: 85017175612     PISSN: 02615614     EISSN: 15321983     Source Type: Journal    
DOI: 10.1016/j.clnu.2017.03.012     Document Type: Article

References (30)

1. Wong, J.M.W., Gut microbiota and cardiometabolic outcomes: influence of dietary patterns and their associated components. Am J Clin Nutr 100:Suppl. (2014), 369S–377S.
2. Wang, Z., Klipfell, E., Bennett, B.J., Koeth, R., Levison, B.S., Dugar, B., et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472:7341 (2011), 57–63.
3. Collins, H.L., Drazul-Schrader, D., Sulpizio, A.C., Koster, P.D., Williamson, Y., Adelman, S.J., et al. L-Carnitine intake and high trimethylamine N-oxide plasma levels correlate with low aortic lesions in ApoE-/- transgenic mice expressing CETP. Atherosclerosis 244 (2016), 29–37.
4. Liu, W., Ma, H., Frost, L., Yuan, T., Dain, J.A., Seeram, N.P., Pomegranate phenolics inhibit formation of advanced glycation endproducts by scavenging reactive carbonyl species. Food Funct 5:11 (2014), 2996–3004.
5. Frankenfeld, C.L., Atkinson, C., Wähälä, K., Lampe, J.W., Obesity prevalence in relation to gut microbial environments capable of producing equol or O-desmethylangolensin from the isoflavone daidzein. Eur J Clin Nutr 68:4 (2014), 526–530.
6. Frankenfeld, C.L., Atkinson, C., Thomas, W.K., Gonzalez, A., Jokela, T., Wähälä, K., et al. High concordance of daidzein-metabolizing phenotypes in individuals measured 1 to 3 years apart. Br J Nutr, 94(6), 2007, 873.
7. Hazim, S., Curtis, P.J., Schär, M.Y., Ostertag, L.M., Kay, C.D., Minihane, A.-M., et al. Acute benefits of the microbial-derived isoflavone metabolite equol on arterial stiffness in men prospectively recruited according to equol producer phenotype: a double-blind randomized controlled trial. Am J Clin Nutr 103:3 (2016), 694–702.
8. Espín, J.C., Larrosa, M., García-Conesa, M.T., Tomás-Barberán, F., Biological significance of urolithins, the gut microbial ellagic acid-derived metabolites: the evidence so far. Evid Based Complement Altern Med, 2013, 2013, 270418.
9. Cerdá, B., Tomás-Barberán, F.A., Espín, J.C., Metabolism of antioxidant and chemopreventive ellagitannins from strawberries, raspberries, walnuts, and oak-aged wine in humans: identification of biomarkers and Individual variability. J Agric Food Chem 53:2 (2005), 227–235.
10. González-Sarrías, A., Giménez-Bastida, J.A., García-Conesa, M.T., Gómez-Sánchez, M.B., García-Talavera, N.V., Gil-Izquierdo, A., et al. Occurrence of urolithins, gut microbiota ellagic acid metabolites and proliferation markers expression response in the human prostate gland upon consumption of walnuts and pomegranate juice. Mol Nutr Food Res 54:3 (2010), 311–322.
11. Larrosa, M., González-Sarrías, A., Yáñez-Gascón, M.J., Selma, M.V., Azorín-Ortuño, M., Toti, S., et al. Anti-inflammatory properties of a pomegranate extract and its metabolite urolithin-A in a colitis rat model and the effect of colon inflammation on phenolic metabolism. J Nutr Biochem 21:8 (2010), 717–725.
12. Ishimoto, H., Shibata, M., Myojin, Y., Ito, H., Sugimoto, Y., Tai, A., et al. In vivo anti-inflammatory and antioxidant properties of ellagitannin metabolite urolithin A. Bioorg Med Chem Lett 21:19 (2011), 5901–5904.
13. Larrosa, M., García-Conesa, M.T., Espín, J.C., Tomás-Barberán, F.A., Ellagitannins, ellagic acid and vascular health. Mol Asp Med 31:6 (2010), 513–539.
14. Tomás-Barberán, F.A., García-Villalba, R., González-Sarrías, A., Selma, M.V., Espín, J.C., Ellagic acid metabolism by human gut microbiota: consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status. J Agric Food Chem 62:28 (2014), 6535–6538.
15. Selma, M.V., Romo-Vaquero, M., García-Villalba, R., González-Sarrías, A., Tomás-Barberán, F.A., Espín, J.C., The human gut microbial ecology associated with overweight and obesity determines ellagic acid metabolism. Food Funct 7 (2016), 1769–1774.
16. Selma, M.V., Beltrán, D., García-Villalba, R., Espín, J.C., Tomás-Barberán, F.A., Description of urolithin production capacity from ellagic acid of two human intestinal Gordonibacter species. Food Funct 5:8 (2014), 1779–1784.
17. Selma, M.V., Tomás-Barberán, F.A., Beltran, D., García-Villalba, R., Espín, J.C., Gordonibacter urolithinfaciens sp. nov., a urolithin-producing bacterium isolated from the human gut. Int J Syst Evol Microbiol 64:Pt 7 (2014), 2346–2352.
18. Romo-Vaquero, M., García-Villalba, R., González-Sarrías, A., Beltrán, D., Tomás-Barberán, F.A., Espín, J.C., et al. Interindividual variability in the human metabolism of ellagic acid: contribution of Gordonibacter to urolithin production. J Funct Foods 17 (2015), 785–791.
19. Mora-Cubillos, X., Tulipani, S., Garcia-Aloy, M., Bulló, M., Tinahones, F.J., Andrés-Lacueva, C., Plasma metabolomic biomarkers of mixed nuts exposure inversely correlate with severity of metabolic syndrome. Mol Nutr Food Res 59 (2015), 2480–2490.
20. Tulipani, S., Urpi-Sarda, M., García-Villalba, R., Rabassa, M., López-Uriarte, P., Bulló, M., et al. Urolithins are the main urinary microbial-derived phenolic metabolites discriminating a moderate consumption of nuts in free-living subjects with diagnosed metabolic syndrome. J Agric Food Chem 60:36 (2012), 8930–8940.
21. López-Uriarte, P., Nogués, R., Saez, G., Bulló, M., Romeu, M., Masana, L., et al. Effect of nut consumption on oxidative stress and the endothelial function in metabolic syndrome. Clin Nutr 29 (2010), 373–380.
22. Sharma, S., Roberts, L.S., Hudes, M.L., Lustig, R.H., Fleming, S.E., Macronutrient intakes and cardio metabolic risk factors in high BMI African American children. Nutr Metab 6:41 (2009), 1–8.
23. Vega, G.L., Ma, P.T.S., Cater, N.B., Filipchuk, N., Meguro, S., Garcia-Garcia, A.B., et al. Effects of adding fenofibrate (200 mg/day) to simvastatin (10 mg/day) in patients with combined hyperlipidemia and metabolic syndrome. Am J Cardiol 91:8 (2003), 956–960.
24. García-Villalba, R., Espín, J.C., Tomás-Barberán, F.A., Chromatographic and spectroscopic characterization of urolithins for their determination in biological samples after the intake of foods containing ellagitannins and ellagic acid. J Chromatogr A 1428 (2016), 162–175.
25. Arsenault, B.J., Boekholdt, S.M., Kastelein, J.J.P., Lipid parameters for measuring risk of cardiovascular disease. Nat Rev Cardiol 8:4 (2011), 197–206.
26. Miele, L., Giorgio, V., Alberelli, M.A., De Candia, E., Gasbarrini, A., Grieco, A., Impact of gut microbiota on obesity, diabetes, and cardiovascular disease risk. Curr Cardiol Rep, 17(12), 2015, 120.
27. Tomás-Barberán, F.A., González-Sarrías, A., García-Villalba, R., Núñez, M.A., Selma, M.V., García-Conesa, M.T., et al. Urolithins, the rescue of “old” metabolites to understand a “new” concept : metabotypes as a nexus between phenolic metabolism, microbiota dysbiosis and host health status. Mol Nutr Food Res 61:1 (2017), 1–35.
28. Frankenfeld, C.L., Atkinson, C., Thomas, W.K., Gonzalez, A., Jokela, T., Wähälä, K., et al. High concordance of daidzein-metabolizing phenotypes in individuals measured 1 to 3 years apart. Br J Nutr 94:6 (2005), 873–876.
29. Tomé-Carneiro, J., Gonzálvez, M., Larrosa, M., García-Almagro, F.J., Avilés-Plaza, F., Parra, S., et al. Consumption of a grape extract supplement containing resveratrol decreases oxidized LDL and ApoB in patients undergoing primary prevention of cardiovascular disease: a triple-blind, 6-month follow-up, placebo-controlled, randomized trial. Mol Nutr Food Res 56:5 (2012), 810–821.
30. Lamarche, B., Moorjani, S., Lupien, P.J., Cantin, B., Bernard, P.M., Dagenais, G.R., et al. Apolipoprotein A-I and B levels and the risk of ischemic heart disease during a five-year follow-up of men in the Quebec cardiovascular study. Circulation 94:3 (1996), 273–278.