Plasma urolithin metabolites correlate with improvements in endothelial function after red raspberry consumption: A double-blind randomized controlled trial

Archives of Biochemistry and Biophysics

Volumn 651, Issue , 2018, Pages 43-51

  Istas, Geoffrey ^a,b   Feliciano, Rodrigo P ^b   Weber, Timon ^b   Garcia Villalba, Rocio ^c   Tomas Barberan, Francisco ^c   Heiss, Christian ^b,d,e   Rodriguez Mateos, Ana ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c RESEARCH GROUP ON QUALITY   (Spain)

^d UNIVERSITY OF SURREY   (United Kingdom)

^e SURREY AND SUSSEX HEALTHCARE NHS TRUST   (United Kingdom)

Author keywords

(Poly)phenols; Ellagittanins; Endothelial function; Raspberries; Urolithins

Indexed keywords

ELLAGIC ACID; ELLAGITANNIN; GLUCOSE; GLUCURONIDE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PHENOL DERIVATIVE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UROLITHIN; UROLITHIN A 3 GLUCURONIDE; UROLITHIN A SULFATE; 3,8-DIHYDROXY-6H-DIBENZO(B,D)PYRAN-6-ONE; COUMARIN DERIVATIVE; POLYPHENOL;

ADULT; ARTICLE; BIOCHEMICAL COMPOSITION; BLOOD LEVEL; BLOOD PRESSURE; CONTROLLED STUDY; FOOD COMPOSITION; FOOD INTAKE; HUMAN; MALE; MASS SPECTROMETRY; METABOLITE; NORMAL HUMAN; PRIORITY JOURNAL; PULSE WAVE; RASPBERRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; URINALYSIS; URINE LEVEL; VASCULAR ENDOTHELIUM; ANALYSIS; ARTERY; BLOOD; DOUBLE BLIND PROCEDURE; FRUIT AND VEGETABLE JUICE; METABOLISM; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; RUBUS; YOUNG ADULT;

ADULT; ARTERIES; COUMARINS; DOUBLE-BLIND METHOD; ELLAGIC ACID; ENDOTHELIUM, VASCULAR; FRUIT AND VEGETABLE JUICES; HUMANS; MALE; POLYPHENOLS; PULSE WAVE ANALYSIS; RUBUS; YOUNG ADULT;

EID: 85048475774     PISSN: 00039861     EISSN: 10960384     Source Type: Journal    
DOI: 10.1016/j.abb.2018.05.016     Document Type: Article

References (36)

1. Ding, Y., Zhang, B., Zhou, K., et al. Dietary ellagic acid improves oxidant-induced endothelial dysfunction and atherosclerosis: role of Nrf2 activation. Int. J. Cardiol. 175:3 (2014), 508–514.
2. Mullen, W., McGinn, J., Lean, M.E., et al. Ellagitannins, flavonoids, and other phenolics in red raspberries and their contribution to antioxidant capacity and vasorelaxation properties. J. Agric. Food Chem. 50:18 (2002), 5191–5196.
3. Yu, Y.M., Wang, Z.H., Liu, C.H., Chen, C.S., Ellagic acid inhibits IL-1beta-induced cell adhesion molecule expression in human umbilical vein endothelial cells. Br. J. Nutr. 97:4 (2007), 692–698.
4. Chang, W.C., Yu, Y.M., Chiang, S.Y., Tseng, C.Y., Ellagic acid suppresses oxidised low-density lipoprotein-induced aortic smooth muscle cell proliferation: studies on the activation of extracellular signal-regulated kinase 1/2 and proliferating cell nuclear antigen expression. Br. J. Nutr. 99:4 (2008), 709–714.
5. Mullen, W., Yokota, T., Lean, M.E., Crozier, A., Analysis of ellagitannins and conjugates of ellagic acid and quercetin in raspberry fruits by LC-MSn. Phytochemistry 64:2 (2003), 617–624.
6. Mullen, W., Lean, M.E., Crozier, A., Rapid characterization of anthocyanins in red raspberry fruit by high-performance liquid chromatography coupled to single quadrupole mass spectrometry. J. Chromatogr. A 966:1–2 (2002), 63–70.
7. Huang, H., Chen, G., Liao, D., et al. Effects of berries consumption on cardiovascular risk factors: a meta-analysis with trial sequential analysis of randomized controlled trials. Sci. Rep., 6, 2016, 23625.
8. Zhu, Y., Miao, Y., Meng, Z., Zhong, Y., Effects of vaccinium berries on serum lipids: a meta-analysis of randomized controlled trials. Evid. Based Compl. Alternat. Med., 2015, 2015, 790329.
9. Basu, A., Betts, N.M., Nguyen, A., Newman, E.D., Fu, D., Lyons, T.J., Freeze-dried strawberries lower serum cholesterol and lipid peroxidation in adults with abdominal adiposity and elevated serum lipids. J. Nutr. 144:6 (2014), 830–837.
10. Burton-Freeman, B., Linares, A., Hyson, D., Kappagoda, T., Strawberry modulates LDL oxidation and postprandial lipemia in response to high-fat meal in overweight hyperlipidemic men and women. J. Am. Coll. Nutr. 29:1 (2010), 46–54.
11. Kerimi, A., Nyambe-Silavwe, H., Gauer, J.S., Tomas-Barberan, F.A., Williamson, G., Pomegranate juice, but not an extract, confers a lower glycemic response on a high-glycemic index food: randomized, crossover, controlled trials in healthy subjects. Am. J. Clin. Nutr. 106:6 (2017 Dec), 1384–1393.
12. Asgary, S., Sahebkar, A., Afshani, M.R., Keshvari, M., Haghjooyjavanmard, S., Rafieian-Kopaei, M., Clinical evaluation of blood pressure lowering, endothelial function improving, hypolipidemic and anti-inflammatory effects of pomegranate juice in hypertensive subjects. Phytother. Res. 28:2 (2014), 193–199.
13. Berryman, C.E., Grieger, J.A., West, S.G., et al. Acute consumption of walnuts and walnut components differentially affect postprandial lipemia, endothelial function, oxidative stress, and cholesterol efflux in humans with mild hypercholesterolemia. J. Nutr. 143:6 (2013), 788–794.
14. Jeong, H.S., Hong, S.J., Lee, T.-B., et al. Effects of black raspberry on lipid profiles and vascular endothelial function in patients with metabolic syndrome. Phytother. Res. 28:10 (2014), 1492–1498.
15. Seeram, N.P., Henning, S.M., Zhang, Y., Suchard, M., Li, Z., Heber, D., Pomegranate juice ellagitannin metabolites are present in human plasma and some persist in urine for up to 48 hours. J. Nutr. 136:10 (2006), 2481–2485.
16. Selma, M.V., Beltran, D., Garcia-Villalba, R., Espin, J.C., Tomas-Barberan, F.A., Description of urolithin production capacity from ellagic acid of two human intestinal Gordonibacter species. Food Funct. 5:8 (2014), 1779–1784.
17. González-Sarrías, A., Espín, J.C., Tomás-Barberán, F.A., Non-extractable polyphenols produce gut microbiota metabolites that persist in circulation and show anti-inflammatory and free radical-scavenging effects. Trends Food Sci. Technol. 69:Part B (2017), 281–288.
18. Ludwig, I.A., Mena, P., Calani, L., et al. New insights into the bioavailability of red raspberry anthocyanins and ellagitannins. Free Radic. Biol. Med. 89 (2015), 758–769.
19. Rodriguez-Mateos, A., Rendeiro, C., Bergillos-Meca, T., et al. Intake and time dependence of blueberry flavonoid-induced improvements in vascular function: a randomized, controlled, double-blind, crossover intervention study with mechanistic insights into biological activity. Am. J. Clin. Nutr. 98:5 (2013), 1179–1191.
20. Czank, C., Cassidy, A., Zhang, Q., et al. Human metabolism and elimination of the anthocyanin, cyanidin-3-glucoside: a (13)C-tracer study. Am. J. Clin. Nutr. 97:5 (2013), 995–1003.
21. Ludwig, I.A., Mena, P., Calani, L., et al. New insights into the bioavailability of red raspberry anthocyanins and ellagitannins. Free Radic. Biol. Med. 89 (2015), 758–769.
22. García-Villalba, R., Espín, J.C., Aaby, K., et al. Validated method for the characterization and quantification of extractable and nonextractable ellagitannins after acid hydrolysis in pomegranate fruits, juices, and extracts. J. Agric. Food Chem. 63:29 (2015), 6555–6566.
23. Rodriguez-Mateos, A., Hezel, M., Aydin, H., et al. Interactions between cocoa flavanols and inorganic nitrate: additive effects on endothelial function at achievable dietary amounts. Free Radic. Biol. Med. 80 (2015), 121–128.
24. Heiss, C., Sansone, R., Karimi, H., et al. Impact of cocoa flavanol intake on age-dependent vascular stiffness in healthy men: a randomized, controlled, double-masked trial. Age (Dordr.), 37(3), 2015, 9794.
25. Feliciano, R.P., Boeres, A., Massacessi, L., et al. Identification and quantification of novel cranberry-derived plasma and urinary (poly)phenols. Arch. Biochem. Biophys. 599 (2016 Jun 1), 31–41.
26. 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.
27. Rodriguez-Mateos, A., Cifuentes-Gomez, T., Gonzalez-Salvador, I., et al. Influence of age on the absorption, metabolism, and excretion of cocoa flavanols in healthy subjects. Mol. Nutr. Food Res. 59:8 (2015 Aug), 1504–1512.
28. Preik, M., Lauer, T., Heiss, C., Tabery, S., Strauer, B.E., Kelm, M., Automated ultrasonic measurement of human arteries for the determination of endothelial function. Ultraschall der Med. 21:5 (2000), 195–198 (Stuttgart, Germany: 1980).
29. Rodriguez-Mateos, A., Feliciano, R.P., Boeres, A., et al. Cranberry (poly)phenol metabolites correlate with improvements in vascular function: a double-blind, randomized, controlled, dose-response, crossover study. Mol. Nutr. Food Res., 2016, 1–11.
30. Spigoni, V., Mena, P., Cito, M., et al. Effects on nitric oxide production of urolithins, gut-derived ellagitannin metabolites, in human aortic endothelial cells. Molecules, 21(8), 2016.
31. Gimenez-Bastida, J.A., Gonzalez-Sarrias, A., Larrosa, M., Tomas-Barberan, F., Espin, J.C., Garcia-Conesa, M.T., Ellagitannin metabolites, urolithin A glucuronide and its aglycone urolithin A, ameliorate TNF-alpha-induced inflammation and associated molecular markers in human aortic endothelial cells. Mol. Nutr. Food Res. 56:5 (2012), 784–796.
32. 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.
33. Gonzalez-Sarrias, A., Garcia-Villalba, R., Romo-Vaquero, M., et al. Clustering according to urolithin metabotype explains the interindividual variability in the improvement of cardiovascular risk biomarkers in overweight-obese individuals consuming pomegranate: a randomized clinical trial. Mol. Nutr. Food Res., 61(5), 2017.
34. Selma, M.V., Romo-Vaquero, M., Garcia-Villalba, R., Gonzalez-Sarrias, A., Tomas-Barberan, F.A., Espin, J.C., The human gut microbial ecology associated with overweight and obesity determines ellagic acid metabolism. Food Funct. 7:4 (2016), 1769–1774.
35. Ras, R.T., Streppel, M.T., Draijer, R., Zock, P.L., Flow-mediated dilation and cardiovascular risk prediction: a systematic review with meta-analysis. Int. J. Cardiol. 168:1 (2013), 344–351.
36. Inaba, Y., Chen, J.A., Bergmann, S.R., Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a meta-analysis. Int. J. Cardiovasc. Imag. 26:6 (2010), 631–640.