Urolithins, the rescue of “old” metabolites to understand a “new” concept: Metabotypes as a nexus among phenolic metabolism, microbiota dysbiosis, and host health status
Abstract
Urolithins are dibenzo[b,d]pyran-6-one derivatives that are produced by the human gut microbiota from ellagitannins and ellagic acid (EA). These metabolites are much better absorbed than their precursors and have been suggested to be responsible for the health effects attributed to ellagitannins and EA that occur in food products as berries and nuts. In the present review, the role and potential of urolithins in human health are critically reviewed, and a perspective of the research approach needed to demonstrate these health effects is presented, based on the existing knowledge. The analytical methods available for urolithin analysis, their occurrence in different tissues and biological fluids, and their metabolism by human gut microbiota are considered. In addition, the interindividual variability observed for the production of urolithins (metabotypes) and its relationship with health status and dysbiosis are also reviewed. The potential mechanisms of action of urolithins are also critically discussed, paying attention to the concentration and the type of metabolites used in the in vitro and in vivo assays and the physiological significance of the results obtained. The gut microbiota metabolism of EA to urolithins and that of daidzein to equol, their individual variations, and the effects on health are also compared.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Among urolithins, urolithin A displays potent anti-inflammatory, antioxidative, and antiaging properties.
“Among urolithins, urolithin A (UroA) displays potent anti-inflammatory, antioxidative, and antiaging properties.130,133, 134, 135”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [133]
Cites
Lipinski, C. A., Lombardo, F., Dominy, B. W., & Feeney, P. J. (1997) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(96)00423-1 · Cited by 11,484 · see citing works
Enterotypes of the human gut microbiome
MetaHIT Consortium (additional members), Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., et al. (2011) · Nature · doi:10.1038/nature09944 · Cited by 7,548 · see citing works
Interaction between Phenolics and Gut Microbiota: Role in Human Health
Selma, M. V., Espín, J. C., & Tomás-Barberán, F. A. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf902107d · Cited by 1,324 · see citing works
Self-citationAnhê, F. F., Roy, D., Pilon, G., Dudonné, S., Matamoros, S., Varin, T. V., Garofalo, C., Moine, Q., Desjardins, Y., Levy, E., et al. (2015) · Gut · doi:10.1136/gutjnl-2014-307142 · Cited by 1,137 · see citing works
Aviram, M., Dornfeld, L., Rosenblat, M., Volkova, N., Kaplan, M., Coleman, R., Hayek, T., Presser, D., & Fuhrman, B. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.5.1062 · Cited by 866 · see citing works
Nutraceuticals: Facts and fiction
Espı́n, J. C., García‐Conesa, M., & Tomás-Barberán, F. A. (2007) · Phytochemistry · doi:10.1016/j.phytochem.2007.09.014 · Cited by 815 · see citing works
Self-citationTan, W., Verma, V., Jeong, K., Kim, S. Y., Jung, C., Lee, S. E., & Rhee, J. H. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00001 · Cited by 635 · see citing works
Espín, J. C., Larrosa, M., García-Conesa, M. T., & Tomás-Barberán, F. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/270418 · Cited by 576 · see citing works
Self-citationLarrosa, M., González‐Sarrías, A., Yáñez-Gascón, M. J., Selma, M. V., Azorín‐Ortuño, M., Toti, S., Tomás-Barberán, F. A., Dolara, P., & Espı́n, J. C. (2009) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.04.012 · Cited by 505 · see citing works
Self-citationSeeram, N. P., Henning, S. M., Zhang, Y., Suchard, M. A., Li, Z., & Heber, D. (2006) · Journal of Nutrition · doi:10.1093/jn/136.10.2481 · Cited by 477 · see citing works
Resveratrol and Clinical Trials: The Crossroad from In Vitro Studies to Human Evidence
Tomé‐Carneiro, J., Larrosa, M., González‐Sarrías, A., Tomás-Barberán, F. A., García‐Conesa, M., & Espı́n, J. C. (2013) · Current Pharmaceutical Design · doi:10.2174/13816128113199990407 · Cited by 451 · see citing works
Self-citationCerdá, B., Tomás-Barberán, F. A., & Espı́n, J. C. (2004) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf049144d · Cited by 448 · see citing works
Self-citationCerd�, B., Esp�n, J. C., Parra, S., Mart�nez, P., & Tom�s-Barber�n, F. A. (2004) · European Journal of Nutrition · doi:10.1007/s00394-004-0461-7 · Cited by 435 · see citing works
Self-citationTomás-Barberán, F. A., García-Villalba, R., González-Sarrías, A., Selma, M. V., & Espín, J. C. (2014) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf5024615 · Cited by 419 · see citing works
Self-citationIn vivo and in vitro metabolism of trans-resveratrol by human gut microbiota
Bode, L. M., Bunzel, D., Huch, M., Cho, G., Ruhland, D., Bunzel, M., Bub, A., Franz, C. M. A. P., & Kulling, S. E. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.049379 · Cited by 397 · see citing works
A survey of modulation of gut microbiota by dietary polyphenols
Dueñas, M., Muñoz-González, I., Cueva, C., Jiménez-Girón, A., Sánchez-Patán, F., Santos-Buelga, C., Moreno-Arribas, M. V., & Bartolomé, B. (2015) · BioMed Research International · doi:10.1155/2015/850902 · Cited by 396 · see citing works
Cerd�, B., Llorach, R., Cer�n, J. J., Espı́n, J. C., & Tomás-Barberán, F. A. (2003) · European Journal of Nutrition · doi:10.1007/s00394-003-0396-4 · Cited by 384 · see citing works
Self-citationEllagitannins, ellagic acid and vascular health
Larrosa, M., García‐Conesa, M., Espı́n, J. C., & Tomás-Barberán, F. A. (2010) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2010.09.005 · Cited by 378 · see citing works
Self-citationMertens‐Talcott, S. U., Jilma‐Stohlawetz, P., Rios, J., Hingorani, L., & Derendorf, H. (2006) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf061674h · Cited by 353 · see citing works
Espín, J. C., González-Barrio, R., Cerdá, B., López-Bote, C., Rey, A. I., & Tomás-Barberán, F. A. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf0723864 · Cited by 352 · see citing works
Self-citationPitts, S. J., Gustafson, A., Wu, Q., Mayo, M. L., Ward, R. K., McGuirt, J. T., Rafferty, A. P., Lancaster, M. F., Evenson, K. R., Keyserling, T. C., et al. (2014) · Nutrition Journal · doi:10.1186/1475-2891-13-1 · Cited by 330 · see citing works
Maruo, T., Sakamoto, M., Ito, C., Toda, T., & Benno, Y. (2008) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.65404-0 · Cited by 308 · see citing works
Selma, M. V., Beltrán, D., García-Villalba, R., Espín, J. C., & Tomás-Barberán, F. A. (2014) · Food Funct. · doi:10.1039/c4fo00092g · Cited by 304 · see citing works
Self-citationCerdá, B., Periago, P., Espín, J. C., & Tomás-Barberán, F. A. (2005) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf050384i · Cited by 301 · see citing works
Self-citationCerdá, B., Cerón, J. M. C., Tomás-Barberán, F. A., et al. (2003) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf020842c · Cited by 297 · see citing works
Self-citationSeeram, N. P., Aronson, W. J., Zhang, Y., Henning, S. M., Moro, A., Lee, R., Sartippour, M. R., Harris, D. M., Rettig, M. B., Suchard, M. A., et al. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf071303g · Cited by 293 · see citing works
González‐Barrio, R., Borges, G., Mullen, W., & Crozier, A. (2010) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf100315d · Cited by 283 · see citing works
Białońska, D., Ramnani, P., Kasimsetty, S. G., Muntha, K. R., Gibson, G. R., & Ferreira, D. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.03.038 · Cited by 280 · see citing works
Larrosa, M., González‐Sarrías, A., García‐Conesa, M., Tomás-Barberán, F. A., & Espı́n, J. C. (2006) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf0527403 · Cited by 261 · see citing works
Self-citationBiałońska, D., Kasimsetty, S. G., Khan, S. I., & Ferreira, D. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf9025794 · Cited by 258 · see citing works
Possemiers, S., Bolca, S., Grootaert, C., Heyerick, A., Decroos, K., Dhooge, W., Keukeleire, D. D., Rabot, S., Verstraete, W., & de Wiele, T. V. (2006) · Journal of Nutrition · doi:10.1093/jn/136.7.1862 · Cited by 258 · see citing works
Núñez‐Sánchez, M. Á., Garcı́a-Villalba, R., Monedero‐Saiz, T., Espin, N. V. G.-T., Gómez‐Sánchez, M. B., Sánchez‐Álvarez, C., García‐Albert, A. M., Rodríguez‐Gil, F. J., Ruiz‐Marín, M., Pastor-Quirante, F. A., et al. (2014) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300931 · Cited by 235 · see citing works
Self-citationLotito, S. B., & Frei, B. B. (2003) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2003.10.005 · Cited by 228 · see citing works
Adams, L. S., Zhang, Y., Seeram, N. P., Heber, D., & Chen, S. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-08-0225 · Cited by 219 · see citing works
Yuan, T., Ma, H., Liu, W., Niesen, D. B., Shah, N., Crews, R., Rose, K. N., Vattem, D. A., & Seeram, N. P. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00260 · Cited by 219 · see citing works
González‐Sarrías, A., Giménez‐Bastida, J. A., García‐Conesa, M. T., Gómez‐Sánchez, M. B., García‐Talavera, N. V., Gil‐Izquierdo, A., Sánchez‐Álvarez, C., Fontana‐Compiano, L. O., Morga‐Egea, J. P., Pastor‐Quirante, F. A., et al. (2010) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200900152 · Cited by 212 · see citing works
Self-citationClavel, T., Henderson, G., Alpert, C.-A., Philippe, C., Rigottier‐Gois, L., Dore, J. M., & Blaut, M. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.10.6077-6085.2005 · Cited by 208 · see citing works
González‐Sarrías, A., Larrosa, M., Tomás-Barberán, F. A., Dolara, P., & Espı́n, J. C. (2010) · British Journal Of Nutrition · doi:10.1017/s0007114510000826 · Cited by 207 · see citing works
Self-citationTime course production of urolithins from ellagic acid by human gut microbiota
García-Villalba, R., Beltrán, D., Espín, J. C., Selma, M. V., & Tomás-Barberán, F. A. (2013) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf402498b · Cited by 207 · see citing works
Self-citationHydroxycinnamic acid composition and in vitro antioxidant activity of selected grain fractions
Gallardo, C., Jiménez, L., & García‐Conesa, M. (2005) · Food Chemistry · doi:10.1016/j.foodchem.2005.07.053 · Cited by 204 · see citing works
Self-citationIn vitro transformation of chlorogenic acid by human gut microbiota
Tomás-Barberán, F. A., Garcı́a-Villalba, R., Quartieri, A., Raimondi, S., Amaretti, A., Leonardi, A., & Rossi, M. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300441 · Cited by 202 · see citing works
Self-citationNew insights into the bioavailability of red raspberry anthocyanins and ellagitannins
Ludwig, I. A., Mena, P. R., Calani, L., Borges, G., Pereira‐Caro, G., Bresciani, L., Rio, D. D., Lean, M. E. J., & Crozier, A. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.10.400 · Cited by 201 · see citing works
Colon Cancer Chemopreventive Activities of Pomegranate Ellagitannins and Urolithins
Kasimsetty, S. G., Białońska, D., Reddy, M. K., Ma, G., Khan, S. I., & Ferreira, D. (2010) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf903762h · Cited by 198 · see citing works
Wang, X.-L., Hur, H.-G., Lee, J. H., Kim, K. T., & Kim, S.-I. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.1.214-219.2005 · Cited by 196 · see citing works
González‐Barrio, R., Edwards, C. A., & Crozier, A. (2011) · Drug Metabolism and Disposition · doi:10.1124/dmd.111.039651 · Cited by 194 · see citing works
Antiglycative and neuroprotective activity of colon‐derived polyphenol catabolites
Verzelloni, E., Pellacani, C., Tagliazucchi, D., Tagliaferri, S., Calani, L., Costa, L. G., Brighenti, F., Borges, G., Crozier, A., Conte, A., et al. (2011) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201000525 · Cited by 190 · see citing works
González‐Sarrías, A., Garcı́a-Villalba, R., Núñez‐Sánchez, M. Á., Tomé‐Carneiro, J., Zafrilla, P., Mulero, J., Tomás-Barberán, F. A., & Espı́n, J. C. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.09.019 · Cited by 184 · see citing works
Self-citationTalking microbes: When gut bacteria interact with diet and host organs
Cani, P. D., & Everard, A. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500406 · Cited by 175 · see citing works
González‐Barrio, R., Truchado, P., Ito, H., Espı́n, J. C., & Tomás-Barberán, F. A. (2011) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf103894m · Cited by 171 · see citing works
Self-citationConcentrated Pomegranate Juice Improves Lipid Profiles in Diabetic Patients with Hyperlipidemia
Esmaillzadeh, A., Tahbaz, F., Gaieni, I., Majd, H. A., & Azadbakht, L. (2004) · Journal of Medicinal Food · doi:10.1089/jmf.2004.7.305 · Cited by 168 · see citing works
Giménez‐Bastida, J. A., González‐Sarrías, A., Larrosa, M., Tomás-Barberán, F. A., Espı́n, J. C., & García‐Conesa, M. (2012) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201100677 · Cited by 166 · see citing works
Self-citationSeeram, N. P., Zhang, Y., McKeever, R., Henning, S. M., Lee, R., Suchard, M. A., Li, Z., Chen, S., Thames, G., Zerlin, A., et al. (2008) · Journal of Medicinal Food · doi:10.1089/jmf.2007.650 · Cited by 164 · see citing works
Fate of Microbial Metabolites of Dietary Polyphenols in Rats: Is the Brain Their Target Destination?
Gasperotti, M., Passamonti, S., Tramer, F., Masuero, D., Guella, G., Mattivi, F., & Vrhovšek, U. (2015) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00051 · Cited by 163 · see citing works
Isolation of a human intestinal bacterium capable of daidzein and genistein conversion
Matthies, A., Blaut, M., & Braune, A. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.01795-08 · Cited by 161 · see citing works
González‐Sarrías, A., Espı́n, J. C., Tomás-Barberán, F. A., & García‐Conesa, M. (2009) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200800150 · Cited by 158 · see citing works
Self-citationGordonibacter urolithinfaciens sp. nov., a urolithin-producing bacterium isolated from the human gut
Selma, M. V., Tomás-Barberán, F. A., Beltrán, D., Garcı́a-Villalba, R., & Espı́n, J. C. (2014) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.055095-0 · Cited by 156 · see citing works
Self-citationLi, Z., Henning, S. M., Lee, R., Lu, Q., Summanen, P. H., Thames, G., Corbett, K. M., Downes, J., Tseng, C., Finegold, S. M., et al. (2015) · Food & Function · doi:10.1039/c5fo00669d · Cited by 153 · see citing works
Garcı́a-Villalba, R., Espı́n, J. C., Aaby, K., Alasalvar, C., Heinonen, M., Jacobs, G., Voorspoels, S., Koivumäki, T., Kroon, P. A., Pelvan, E., et al. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b02062 · Cited by 153 · see citing works
Self-citationSharma, M., Li, L., Celver, J. P., Killian, C., Kovoor, A., & Seeram, N. P. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf902857v · Cited by 150 · see citing works
Pomegranate: a fruit that ameliorates metabolic syndrome
Medjakovic, S., & Jungbauer, A. (2012) · Food & Function · doi:10.1039/c2fo30034f · Cited by 148 · see citing works
Qiu, Z., Zhou, B., Jin, L. G., Yu, H., Liu, L., Liu, Y., Qin, C., Xie, S., & Zhu, F. (2013) · Food and Chemical Toxicology · doi:10.1016/j.fct.2013.06.025 · Cited by 137 · see citing works
Garcia-Muñoz, C., & Vaillant, F. (2014) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2011.644643 · Cited by 133 · see citing works
Garcı́a-Villalba, R., Espı́n, J. C., & Tomás-Barberán, F. A. (2015) · Journal of Chromatography A · doi:10.1016/j.chroma.2015.08.044 · Cited by 132 · see citing works
Self-citationPhase-II metabolism limits the antiproliferative activity of urolithins in human colon cancer cells
González‐Sarrías, A., Giménez‐Bastida, J. A., Núñez‐Sánchez, M. Á., Larrosa, M., García‐Conesa, M., Tomás-Barberán, F. A., & Espı́n, J. C. (2013) · European Journal of Nutrition · doi:10.1007/s00394-013-0589-4 · Cited by 132 · see citing works
Self-citationIn vivo anti-inflammatory and antioxidant properties of ellagitannin metabolite urolithin A
Ishimoto, H., Shibata, M., Myojin, Y., Ito, H., Sugimoto, Y., Tai, A., & Hatano, T. (2011) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2011.07.086 · Cited by 131 · see citing works
van der Hooft, J. J. J., de Vos, R. C. H., Mihaleva, V. V., Bino, R. J., Ridder, L., de Roo, N., Jacobs, D. M., van Duynhoven, J., & Vervoort, J. J. M. (2012) · Analytical Chemistry · doi:10.1021/ac3017339 · Cited by 131 · see citing works
Cerdá, B., Soto, C., Albaladejo, M. D., Martínez, P., Sánchez-Gascón, F., Tomás-Barberán, F. A., & Espı́n, J. C. (2005) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602309 · Cited by 130 · see citing works
Self-citationHazim, S., Curtis, P. J., Schär, M. Y., Ostertag, L. M., Kay, C. D., Minihane, A. M., & Cassidy, A. (2016) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.125690 · Cited by 130 · see citing works
Selma, M. V., Romo‐Vaquero, M., Garcı́a-Villalba, R., González‐Sarrías, A., Tomás-Barberán, F. A., & Espı́n, J. C. (2015) · Food & Function · doi:10.1039/c5fo01100k · Cited by 128 · see citing works
Self-citationShema‐Didi, L., Sela, S., Ore, L., Shapiro, G., Geron, R., Goldfeld, M., & Kristal, B. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.05.013 · Cited by 125 · see citing works
Piwowarski, J. P., Kiss, A. K., Granica, S., & Moeslinger, T. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500264 · Cited by 124 · see citing works
Antiplasmodial activity of Punica granatum L. fruit rind
Dell’Agli, M., Galli, G. V., Corbett, Y., et al. (2009) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2009.06.025 · Cited by 121 · see citing works
González‐Sarrías, A., Tomé‐Carneiro, J., Bellesia, A., Tomás-Barberán, F. A., & Espı́n, J. C. (2015) · Food & Function · doi:10.1039/c5fo00120j · Cited by 119 · see citing works
Self-citationMetabolites of the Ellagitannin Geraniin and Their Antioxidant Activities
Ito, H. (2011) · Planta Medica · doi:10.1055/s-0030-1270749 · Cited by 114 · see citing works
Kang, I., Kim, Y., Tomás-Barberán, F. A., Espı́n, J. C., & Chung, S. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500796 · Cited by 114 · see citing works
Self-citationFrankenfeld, C. L., Atkinson, C., Wähälä, K., & Lampe, J. W. (2014) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2014.23 · Cited by 110 · see citing works
Romo‐Vaquero, M., Garcı́a-Villalba, R., González‐Sarrías, A., Beltrán, D., Tomás-Barberán, F. A., Espı́n, J. C., & Selma, M. V. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.06.040 · Cited by 109 · see citing works
Self-citationPuupponen‐Pimiä, R., Seppänen‐Laakso, T., Kankainen, M., Maukonen, J., Törrönen, R., Kolehmainen, M., Leppänen, T., Moilanen, E., Nohynek, L. J., Aura, A., et al. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300280 · Cited by 109 · see citing works
Self-citationLiu, W., Ma, H., Frost, L., Yuan, T., Dain, J. A., & Seeram, N. P. (2014) · Food & Function · doi:10.1039/c4fo00538d · Cited by 108 · see citing works
Piwowarski, J. P., Granica, S., Zwierzyńska, M., Stefańska, J., Schopohl, P., Melzig, M. F., & Kiss, A. K. (2014) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2014.06.032 · Cited by 107 · see citing works
Matthaiou, C., Goutzourelas, N., Stagos, D., Σαράφογλου, Ε., Jamurtas, A. Z., Koulocheri, S. D., Haroutounian, S. A., Tsatsakis, A. M., & Kouretas, D. (2014) · Food and Chemical Toxicology · doi:10.1016/j.fct.2014.07.027 · Cited by 107 · see citing works
The metabolism of ellagic acid in the rat
Doyle, B., & Griffiths, L. A. (1980) · Xenobiotica · doi:10.3109/00498258009033752 · Cited by 106 · see citing works
Slackia equolifaciens sp. nov., a human intestinal bacterium capable of producing equol
Jin, J., Kitahara, M., Sakamoto, M., Hattori, M., & Benno, Y. (2009) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.016774-0 · Cited by 104 · see citing works
Dell’Agli, M., Galli, G. V., Bulgari, M., Basilico, N., Romeo, S., Bhattacharya, D., Taramelli, D., & Bosisio, E. (2010) · Malaria Journal · doi:10.1186/1475-2875-9-208 · Cited by 102 · see citing works
González‐Sarrías, A., Miguel, V., Merino, G., Lucas, R., Morales, J. C., Tomás-Barberán, F. A., Álvarez, A. I., & Espı́n, J. C. (2013) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf4007505 · Cited by 101 · see citing works
Self-citationTruchado, P., Larrosa, M., García‐Conesa, M., Cerdá, B., Vidal-Guevara, M. L., Tomás-Barberán, F. A., & Espı́n, J. C. (2011) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf203641r · Cited by 98 · see citing works
Self-citationGiménez‐Bastida, J. A., Larrosa, M., González‐Sarrías, A., Tomás-Barberán, F. A., Espı́n, J. C., & García‐Conesa, M. (2012) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf300290f · Cited by 97 · see citing works
Self-citationVicinanza, R., Zhang, Y., Henning, S. M., & Heber, D. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/247504 · Cited by 97 · see citing works
Wang, Y., Qiu, Z., Zhou, B., Liu, C., Ruan, J., Yan, Q., Liao, J., & Zhu, F. (2015) · Toxicology in Vitro · doi:10.1016/j.tiv.2015.04.008 · Cited by 96 · see citing works
High concordance of daidzein-metabolizing phenotypes in individuals measured 1 to 3 years apart
Frankenfeld, C. L., Atkinson, C., Thomas, W. K., Gonzalez, A., Jokela, T., Wähälä, K., Schwartz, S. M., Li, S. S., & Lampe, J. W. (2005) · British Journal Of Nutrition · doi:10.1079/bjn20051565 · Cited by 96 · see citing works
Identification of Urinary and Intestinal Bacterial Metabolites of Ellagitannin Geraniin in Rats
Ito, H., Iguchi, A., & Hatano, T. (2007) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf0726942 · Cited by 94 · see citing works
Bookheimer, S. Y., Renner, B., Ekstrom, A. D., Li, Z., Henning, S. M., Brown, J. A., Jones, M., Moody, T. D., & Small, G. W. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/946298 · Cited by 93 · see citing works
Subash, S., Essa, M. M., Al-Asmi, A. R., Al‐Adawi, S., Vaishnav, R., Braidy, N., Manivasagam, T., & Guillemin, G. J. (2014) · Journal of Traditional and Complementary Medicine · doi:10.4103/2225-4110.139107 · Cited by 90 · see citing works
Natural Dibenzo-α-Pyrones and Their Bioactivities
Mao, Z., Sun, W., Fu, L., Luo, H., Lai, D., & Zhou, L. (2014) · Molecules · doi:10.3390/molecules19045088 · Cited by 90 · see citing works
González‐Sarrías, A., Núñez‐Sánchez, M. Á., Tomé‐Carneiro, J., Tomás-Barberán, F. A., García‐Conesa, M., & Espı́n, J. C. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500780 · Cited by 84 · see citing works
Self-citationFreedland, S. J., Carducci, M., Kroeger, N., Partin, A. W., Rao, J.-Y., Jin, Y., Kerkoutian, S., Wu, H., Li, Y., Creel, P. A., et al. (2013) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-12-0423 · Cited by 83 · see citing works
Stolarczyk, M., Piwowarski, J. P., Granica, S., et al. (2013) · Phytotherapy Research · doi:10.1002/ptr.4941 · Cited by 83 · see citing works
Cho, H., Jung, H., Lee, H., Yi, H. C., Kwak, H., & Hwang, K. T. (2015) · Food & Function · doi:10.1039/c5fo00274e · Cited by 83 · see citing works
Effect of a walnut meal on postprandial oxidative stress and antioxidants in healthy individuals
Haddad, E. H., Gaban‐Chong, N., Oda, K., & Sabaté, J. (2014) · Nutrition Journal · doi:10.1186/1475-2891-13-4 · Cited by 80 · see citing works
Kasimsetty, S. G., Białońska, D., Reddy, M. K., Thornton, C., Willett, K. L., & Ferreira, D. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf902716r · Cited by 79 · see citing works
González‐Sarrías, A., Azorín‐Ortuño, M., Yáñez-Gascón, M. J., Tomás-Barberán, F. A., García‐Conesa, M., & Espı́n, J. C. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf900725e · Cited by 78 · see citing works
Self-citationMosele, J. I., Gosalbes, M. J., Macià, A., Rubió, L., Vázquez-Castellanos, J. F., Jiménez‐Hernández, N., Moyá, A., Latorre, A., & Motilva, M. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500227 · Cited by 77 · see citing works
Intestinal Bacterium Eubacterium cellulosolvens Deglycosylates Flavonoid C- and O- Glucosides
Braune, A., & Blaut, M. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.02115-12 · Cited by 75 · see citing works
Olennikov, D. N., Kashchenko, N. I., & Chirikova, N. K. (2015) · Nutrients · doi:10.3390/nu7105406 · Cited by 73 · see citing works
Antioxidative Properties of Functional Polyphenols and Their Metabolites Assessed by an ORAC Assay
Ishimoto, H., Tai, A., Yoshimura, M., Amakura, Y., Yoshida, T., Hatano, T., & Ito, H. (2012) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.110717 · Cited by 73 · see citing works
Giménez‐Bastida, J. A., Truchado, P., Larrosa, M., et al. (2011) · Food Chemistry · doi:10.1016/j.foodchem.2011.12.003 · Cited by 72 · see citing works
González‐Sarrías, A., Núñez‐Sánchez, M. Á., Garcı́a-Villalba, R., Tomás-Barberán, F. A., & Espı́n, J. C. (2015) · European Journal of Nutrition · doi:10.1007/s00394-015-1131-7 · Cited by 72 · see citing works
Self-citationChemistry and biochemistry of some mammalian secretions and excretions
LEDERER, E. (1949) · Journal of the Chemical Society (Resumed) · doi:10.1039/jr9490002115 · Cited by 71 · see citing works
Jackman, K. A., Woodman, O. L., Chrissobolis, S., & Sobey, C. G. (2007) · Brain Research · doi:10.1016/j.brainres.2007.01.007 · Cited by 71 · see citing works
Tulipani, S., Urpí-Sardà, M., Garcı́a-Villalba, R., Rabassa, M., López-Uriarte, P. J., Bulló, M., Jáuregui, O., Tomás-Barberán, F. A., Salas‐Salvadó, J., Espı́n, J. C., et al. (2012) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf301509w · Cited by 71 · see citing works
Self-citationNúñez‐Sánchez, M. Á., Dávalos, A., González‐Sarrías, A., Casas‐Agustench, P., Visioli, F., Monedero‐Saiz, T., Espin, N. V. G.-T., Gómez‐Sánchez, M. B., Sánchez‐Álvarez, C., García‐Albert, A. M., et al. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500357 · Cited by 71 · see citing works
Self-citationAntiatherogenic effects of ellagic acid and urolithins in vitro
Mele, L., Mena, P. R., Piemontese, A., Marino, V., López-Gutiérrez, N., Bernini, F., Brighenti, F., Zanotti, I., & Rio, D. D. (2016) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2016.02.017 · Cited by 70 · see citing works
Ito, H., Li, P., Koreishi, M., et al. (2013) · Food Chemistry · doi:10.1016/j.foodchem.2013.11.160 · Cited by 67 · see citing works
Sánchez‐González, C., Ciudad, C. J., Noé, V., & Izquierdo-Pulido, M. (2014) · Food & Function · doi:10.1039/c4fo00542b · Cited by 66 · see citing works
Subash, S., Braidy, N., Essa, M. M., Al‐Buraiki, Z., Vaishnav, R., Al‐Adawi, S., Al-Asmi, A. R., & Guillemin, G. J. (2014) · Nutrition · doi:10.1016/j.nut.2014.06.004 · Cited by 65 · see citing works
The current status of chemical systematics
Waterman, P. G. (2007) · Phytochemistry · doi:10.1016/j.phytochem.2007.06.029 · Cited by 63 · see citing works
Kosmala, M., Zduńczyk, Z., Juśkiewicz, J., Jurgoński, A., Karlińska, E., Macierzyński, J., Jańczak, R., & Rój, E. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b00648 · Cited by 62 · see citing works
Cozza, G., Gianoncelli, A., Bonvini, P., Zorzi, E., Pasquale, R., Rosolen, A., Pinna, L. A., Meggio, F., Zagotto, G., & Moro, S. (2011) · ChemMedChem · doi:10.1002/cmdc.201100338 · Cited by 61 · see citing works
Piwowarski, J. P., Granica, S., & Kiss, A. K. (2014) · Planta Medica · doi:10.1055/s-0034-1368615 · Cited by 60 · see citing works
Gasperotti, M., Masuero, D., Guella, G., Mattivi, F., & Vrhovšek, U. (2014) · Talanta · doi:10.1016/j.talanta.2014.04.058 · Cited by 59 · see citing works
Urolithin A causes p21 up-regulation in prostate cancer cells
Sánchez‐González, C., Ciudad, C. J., Izquierdo-Pulido, M., & Noé, V. (2015) · European Journal of Nutrition · doi:10.1007/s00394-015-0924-z · Cited by 58 · see citing works
Cubillos, L. X. M., Tulipani, S., Garcia‐Aloy, M., Bulló, M., Tinahones, F. J., & Andrés‐Lacueva, C. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500549 · Cited by 53 · see citing works
Sala, R., Mena, P. R., Savi, M., Brighenti, F., Crozier, A., Miragoli, M., Stilli, D., & Rio, D. D. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.03.019 · Cited by 53 · see citing works
Kallio, T., Kallio, J., Jaakkola, M., Mäki, M., Kilpeläinen, P., & Virtanen, V. T. (2013) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf403208d · Cited by 52 · see citing works
Metabolism of Oak Leaf Ellagitannins and Urolithin Production in Beef Cattle
González‐Barrio, R., Truchado, P., Garcı́a-Villalba, R., Hervás, G., Frutos, P., Espı́n, J. C., & Tomás-Barberán, F. A. (2012) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf300718k · Cited by 49 · see citing works
Self-citationKiss, A. K., Granica, S., Stolarczyk, M., & Melzig, M. F. (2011) · Food Chemistry · doi:10.1016/j.foodchem.2011.09.109 · Cited by 49 · see citing works
Nealmongkol, P., Tangdenpaisal, K., Sitthimonchai, S., et al. (2013) · Tetrahedron · doi:10.1016/j.tet.2013.08.045 · Cited by 48 · see citing works
Gülcan, H. O., Ünlü, S., Esiringü, İ., Erçeti̇n, T., Şahin, Y., Öz, D., & Sahin, M. F. (2014) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2014.08.016 · Cited by 47 · see citing works
Natural Dibenzo[b,d]Pyran-6-Ones: Structural Diversity and Biological Activity
Garazd, Y. L., & Garazd, M. M. (2016) · Chemistry of Natural Compounds · doi:10.1007/s10600-016-1536-4 · Cited by 47 · see citing works
Pilot Walnut Intervention Study of Urolithin Bioavailability in Human Volunteers
Pfundstein, B., Haubner, R., Würtele, G., Gehres, N., Ulrich, C. M., & Owen, R. W. (2014) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf5040652 · Cited by 47 · see citing works
Anti-atherogenic properties of date vs. pomegranate polyphenols: the benefits of the combination
Rosenblat, M., Volkova, N., Borochov‐Neori, H., Judeinstein, S., & Aviram, M. (2015) · Food & Function · doi:10.1039/c4fo00998c · Cited by 43 · see citing works
Dellafiora, L., Mena, P. R., Cozzini, P., Brighenti, F., & Rio, D. D. (2013) · Food & Function · doi:10.1039/c3fo60117j · Cited by 43 · see citing works
de Molina, A. R., Vargas, T., Molina, S., Sánchez, J., Martínez-Romero, J., González‐Vallinas, M., Martín‐Hernández, R., Sánchez‐Martínez, R., de Cedrón, M. G., Dávalos, A., et al. (2015) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.114.221796 · Cited by 41 · see citing works
Self-citationGiorgio, C., Mena, P. R., Rio, D. D., Brighenti, F., Barocelli, E., Hassan‐Mohamed, I., Callegari, D., Lodola, A., & Tognolini, M. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500470 · Cited by 40 · see citing works
de Felipe, F. L., Rivas, B. D. L., & Muñoz, R. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00684 · Cited by 40 · see citing works
Hyaluronidase Inhibitory Active 6H-Dibenzo[b,d]pyran-6-ones from the Feces ofTrogopterus xanthipes
Jeong, S., Kim, N.-Y., Kim, D., et al. (2009) · Planta Medica · doi:10.1055/s-0029-1243114 · Cited by 38 · see citing works
Natella, F., Leoni, G., Maldini, M., Natarelli, L., Comitato, R., Schönlau, F., Virgili, F., & Canali, R. (2013) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf403493a · Cited by 38 · see citing works
Food Polyphenols Fail to Cause a Biologically Relevant Reduction of COX-2 Activity
Willenberg, I., Meschede, A. K., Gueler, F., Jang, M.-S., Shushakova, N., & Schebb, N. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0139147 · Cited by 36 · see citing works
Muñoz, M. C. G., Hernández, L., Pérez, A. M., & Vaillant, F. E. (2013) · Food Research International · doi:10.1016/j.foodres.2013.10.049 · Cited by 35 · see citing works
Furlanetto, V., Zagotto, G., Pasquale, R., Moro, S., & Gatto, B. (2012) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf302600q · Cited by 33 · see citing works
Fotschki, B., Milala, J., Jurgoński, A., Karlińska, E., Zduńczyk, Z., & Juśkiewicz, J. (2014) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf405612a · Cited by 32 · see citing works
BACTERIAL TANNASES: PRODUCTION, PROPERTIES AND APPLICATIONS
Aguilar‐Zárate, P., Cruz-Hernández, Montañez, J., Belmares, R. E., & Aguilar, C. N. (2014) · Redalyc (Universidad Autónoma del Estado de México) · Cited by 31 · see citing works
Yang, J., Lee, R., Henning, S. M., et al. (2015) · Food Chemistry · doi:10.1016/j.foodchem.2015.08.099 · Cited by 23 · see citing works
Azorín‐Ortuño, M., Urbán, C., Cerón, J. M. C., et al. (2008) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf8000857 · Cited by 20 · see citing works
Isolation of two benzocoumarins from ‘clover stone’ a type of renal calculus found in sheep
Pope, G. S. (1964) · Biochemical Journal · doi:10.1042/bj0930474 · Cited by 19 · see citing works
Atkinson, C., Newton, K. M., Yong, M., Stanczyk, F. Z., Westerlind, K. C., Li, L., & Lampe, J. W. (2012) · Metabolism · doi:10.1016/j.metabol.2012.05.012 · Cited by 14 · see citing works
Inhibitory Effect of Ellagitannin Metabolites on IgE-Mediated Allergic Responses in RBL-2H3 Cells
Nagano, T., Ito, H., & Okamoto, T. (2012) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.120448 · Cited by 5 · see citing works
COMPARATIVE DOCKING STUDY OF ‘DUKUNG ANAK’ PHYTONUTRIENT COMPOUNDS WITH ANTI-CHOLESTEROL PROPERTIES
Rozano, L., Abdullah‐Zawawi, M., Ahmad, M. A., & Jaganath, I. B. (2015) · Jurnal Teknologi · doi:10.11113/jt.v77.6900 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gut microbiota functions: metabolism of nutrients and other food components
Rowland, I., Gibson, G., Heinken, A., Scott, K., Swann, J., Thiele, I., & Tuohy, K. (2018) · European Journal of Nutrition · doi:10.1007/s00394-017-1445-8 · Cited by 2,878 · see citing works
Regulation of Intestinal Barrier Function by Microbial Metabolites
Ghosh, S., Whitley, C. S., Haribabu, B., & Jala, V. R. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.02.007 · Cited by 835 · see citing works
The effects of vegetarian and vegan diets on gut microbiota
Tomova, A., Bukovsky, I., Rembert, E., Yonas, W., Alwarith, J., Barnard, N. D., & Kahleova, H. (2019) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00047 · Cited by 713 · see citing works
Enhancement of the gut barrier integrity by a microbial metabolite through the Nrf2 pathway
Singh, R., Chandrashekharappa, S., Bodduluri, S. R., Baby, B. V., Hegde, B., Kotla, N. G., Hiwale, A. A., Saiyed, T., Patel, P., Vijay-Kumar, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-07859-7 · Cited by 713 · see citing works
The gut microbiota: a key factor in the therapeutic effects of (poly)phenols
Espín, J. C., González-Sarrías, A., & Tomás-Barberán, F. A. (2017) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.04.033 · Cited by 603 · see citing works
Self-citationAndreux, P. A., Blanco-Bose, W., Ryu, D., Burdet, F., Ibberson, M., Aebischer, P., Auwerx, J., Singh, A., & Rinsch, C. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0073-4 · Cited by 590 · see citing works
González-Sarrías, A., Núñez-Sánchez, M. A., Tomás-Barberán, F. A., & Espín, J. C. (2017) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.6b04538 · Cited by 174 · see citing works
Linking dietary patterns with gut microbial composition and function
Sheflin, A. M., Melby, C. L., Carbonero, F., & Weir, T. L. (2017) · Gut Microbes · doi:10.1080/19490976.2016.1270809 · Cited by 162 · see citing works
Urolithin A improves Alzheimer's disease cognition and restores mitophagy and lysosomal functions
Hou, Y., Chu, X., Park, J., Zhu, Q., Hussain, M., Li, Z., Madsen, H. B., Yang, B., Wei, Y., Wang, Y., et al. (2024) · Alzheimer's & Dementia · doi:10.1002/alz.13847 · Cited by 145 · see citing works
Food Design To Feed the Human Gut Microbiota
Ercolini, D., & Fogliano, V. (2018) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.8b00456 · Cited by 146 · see citing works
Gaya, P., Peirotén, Á., Medina, M., Álvarez, I., & Landete, J. M. (2018) · Journal of Functional Foods · doi:10.1016/j.jff.2018.03.040 · Cited by 116 · see citing works
- Authors
- Tomás‐Barberán, F. A., González‐Sarrías, A., García‐Villalba, R., Núñez‐Sánchez, M. A., Selma, M. V., García‐Conesa, M. T., & Espín, J. C.
- Affiliations
- Research Group on Quality Safety and Bioactivity of Plant Foods CEBAS‐CSIC Murcia Spain
- Consejo Superior de Investigaciones Científicas (ES)
- Venue
- Molecular Nutrition & Food Research
- Publisher
- Wiley
- Published
- 2016-06-20
- Volume
- 61
- Issue
- 1
- ISSN
- 1613-4125 (ISSN-L)
- 1613-4133
- OpenAlex
- W2346306153
- Cited by
- 465
- References
- 148
- Citations by year
- 2026: 42 · 2025: 39 · 2024: 49 · 2023: 47 · 2022: 60 · 2021: 57 · 2020: 67 · 2019: 35 · 2018: 33 · 2017: 27 · 2016: 7 · 2013: 1
- FWCI
- 4.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Nutrition & Food Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Directorate-General for Research and Innovation (312090)
- Ministerio de Economía y Competitividad (AGL2011‐22447)
- Consejo Superior de Investigaciones Científicas (201370E068)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Pomegranate: compositions and health benefits
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Biochemistry › Phytochemicals and Antioxidant Activities
- Keywords
- urolithins, ellagitannins, ellagic acid, gut microbiota, metabolic phenotypes, dysbiosis, phenolic metabolism, interindividual variability, daidzein, equol, health effects, mechanism of action
- MeSH terms
- Gastrointestinal Microbiome, Animals, Anti-Inflammatory Agents, Non-Steroidal, Antineoplastic Agents, Antioxidants, Chromatography, High Pressure Liquid, Coumarins, Health Status, Humans, Mass Spectrometry, Hydrolyzable Tannins, Lipid Metabolism, Dysbiosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review