Role of intestinal microecology in the regulation of energy metabolism by dietary polyphenols and their metabolites

  • Shaoling Lin College of Food Science, Fujian Agriculture and Forestry University
  • Zhengyu Wang College of Food Science, Fujian Agriculture and Forestry University
  • Ka-Lung Lam School of Life Sciences, The Chinese University of Hong Kong
  • Shaoxiao Zeng College of Food Science, Fujian Agriculture and Forestry University
  • Bee K. Tan Departments of Cardiovascular Sciences, University of Leicester
  • Jiamiao Hu College of Food Science, Fujian Agriculture and Forestry University
Keywords: polyphenols, gut microecology, energy metabolism


Background: Polyphenols are a class of plant secondary metabolites with a variety of physiological functions. Polyphenols and their intestinal metabolites could greatly affect host energy metabolism via multiple mechanisms.

Objective: The objective of this review was to elaborate the role of intestinal microecology in the regulatory effects of dietary polyphenols and their metabolites on energy metabolism.

Methods: In this review, we illustrated the potential mechanisms of energy metabolism regulated by the crosstalk between polyphenols and intestinal microecology including intestinal microbiota, intestinal epithelial cells, and mucosal immune system.

Results: Polyphenols can selectively regulate the growth of susceptible microorganisms (eg. reducing the ratio of Firmicutes to Bacteroides, promoting the growth of beneficial bacteria and inhibiting pathogenic bacteria) as well as alter bacterial enzyme activity. Moreover, polyphenols can influence the absorption and secretion of intestinal epithelial cells, and alter the intestinal mucosal immune system.

Conclusion: The intestinal microecology play a crucial role for the regulation of energy metabolism by dietary polyphenols.


Download data is not yet available.


  1. Meydani M, Hasan ST. Dietary polyphenols and obesity. Nutrients 2010; 2: 737–51. doi: 10.3390/nu2070737

  2. Lin S, Hu J, Zhou X, Cheung PCK. Inhibition of vascular endothelial growth factor-induced angiogenesis by chlorogenic acid via targeting the vascular endothelial growth factor receptor 2-mediated signaling pathway. J Funct Foods 2017; 32: 285–95. doi: 10.1016/j.jff.2017.03.009

  3. Park JH, Schaller M, Crandall CS. Pathogen-avoidance mechanisms and the stigmatization of obese people. Evol Hum Behav 2007; 28: 410–14. doi: 10.1016/j.evolhumbehav.2007.05.008

  4. Dhurandhar NV. Contribution of pathogens in human obesity. Drug News Perspect 2004; 17: 307–13. doi: 10.1358/dnp.2004.17.5.829034

  5. Ismail NA, Ragab SH, Elbaky AA, Shoeib ARS, Alhosary Y, Fekry D. Frequency of Firmicutes and Bacteroidetes in gut microbiota in obese and normal weight Egyptian children and adults. Arch Med Sci 2011; 7: 501–7. doi: 10.5114/aoms.2011.23418

  6. Koliada A, Synko G, Moseiko V, Budovska L, Puchkov K, Perederiy V, et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol 2017; 17: 120. doi: 10.1186/s12866-017-1027-1

  7. Delzenne NM, Neyrinck AM, Bäckhed F, Cani PD. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrino 2011; 7: 639–46. doi: 10.1038/nrendo.2011.126

  8. Blaut M, Bischoff SC. Probiotics and obesity. Ann Nutr Metab 2010; 57: 20–3. doi: 10.1159/000309079

  9. Valdés L, Cuervo A, Salazar N, Ruas-Madiedo P, Gueimonde M, González S. The relationship between phenolic compounds from diet and microbiota: impact on human health. Food Funct 2015; 6: 2424–39. doi: 10.1039/C5FO00322A

  10. Mccracken VJ, Lorenz RG. The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell Microbiol 2001; 3: 1–11. doi: 10.1046/j.1462-5822.2001.00090

  11. Rehman A, Sina C, Gavrilova O, Häsler R, Ott S, Baines JF, et al. Nod2 is essential for temporal development of intestinal microbial communities. Gut 2011; 60: 1354–62. doi: 10.1136/gut.2010.216259

  12. Huang J, Chen L, Xue B, Liu Q, Ou S, Wang Y, et al. Different flavonoids can shape unique gut microbiota profile in vitro. J Food Sci 2016; 81: H2273. doi: 10.1111/1750-3841.13411

  13. Angelakis E, Armougom F, Million M, Raoult D. The relationship between gut microbiota and weight gain in humans. Future Microbiol 2012; 7: 91–109. doi: 10.2217/fmb.11.142

  14. Sanz Y, Santacruz A, Gauffin P. Gut microbiota in obesity and metabolic disorders. Proc Nutr Soc 2010; 69: 434–41. doi: 10.1017/S0029665110001813

  15. Passos MDCF, Moraes-Filho JP. Intestinal microbiota in digestive diseases. Arquivos de gastroenterologia 2017; 54: 255–62. doi: 10.1590/S0004-2803.201700000-31

  16. Węgielska I, Suliburska J. The role of intestinal microbiota in the pathogenesis of metabolic diseases. Acta Sci Pol Technol Aliment 2016; 15: 201–11. doi: 10.17306/J.AFS.2016.2.20

  17. Ouwehand A, Isolauri E, Salminen S. The role of the intestinal microflora for the development of the immune system in early childhood. Eur J Nutr 2002; 41: i32–7. doi: 10.1007/s00394-002-1105-4

  18. Brayden DJ, Jepson MA, Baird AW. Keynote review: intestinal Peyer’s patch M cells and oral vaccine targeting. Drug Discov Today 2005; 10: 1145–57. doi: 10.1016/S1359-6446(05)03536-1

  19. Miele L, Valenza V, La TG, Montalto M, Cammarota G, Ricci R, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 2009; 49: 1877–87. doi: 10.1002/hep.22848

  20. Chandrasekara N, Shahidi F. Effect of roasting on phenolic content and antioxidant activities of whole cashew nuts, kernels, and testa. J Agr Food Chem 2011; 59: 5006–14. doi: 10.1021/jf2000772

  21. Bondonno CP, Croft KD, Ward N, Considine MJ, Hodgson JM. Dietary flavonoids and nitrate: effects on nitric oxide and vascular function. Nut Rev 2015; 73: 216–35. doi: 10.1093/nutrit/nuu014

  22. Dai J, Mumper RJ. Plant phenolics. Extraction, analysis and their antioxidant and anticancer properties. Molecules 2010; 15: 7313–52. doi: 10.3390/molecules15107313

  23. Lee J, Chan BLS, Mitchell AE. Identification/quantification of free and bound phenolic acids in peel and pulp of apples (Malus domestica) using high resolution mass spectrometry (HRMS). Food Chem 2017; 215: 301–10. doi: 10.1016/j.foodchem

  24. Russell WR, Labat A, Scobbie L, Duncan GJ, Duthie GG. Phenolic acid content of fruits commonly consumed and locally produced in Scotland. Food Chem 2009; 115: 100–4. doi: 10.1016/j.foodchem.2008.11.086

  25. Clifford MN. Diet-derived phenols in plasma and tissues and their implications for health. Planta Med 2004; 70: 1103–14. doi: 10.1055/s-2004-835835

  26. Cardona F, Andrés-Lacueva C, Tulipani S, Tinahones FJ, Queipo-Ortuã;o MI. Benefits of polyphenols on gut microbiota and implications in human health. J Nutr Biochem 2013; 24: 1415–22. doi: 10.1016/j.jnutbio.2013.05.001

  27. Trinh HT, Joh EH, Kwak HY, Baek NI, Kim DH. Anti-pruritic effect of baicalin and its metabolites, baicalein and oroxylin A, in mice. Acta Pharmacolo Sin 2010, 31: 718–24. doi: 10.1038/aps.2010.42

  28. Roowi S, Stalmach A, Mullen W, Lean MEJ, Edwards CA, Crozier A. Green tea flavan-3-ols: colonic degradation and urinary excretion of catabolites by humans. J Agric Food Chem 2010; 58: 1296–304. doi: 10.1021/jf9032975

  29. Griffiths LA, Smith GE. Metabolism of apigenin and related compounds in the rat. Metabolite formation in vivo and by the intestinal microflora in vitro. Biochem J 1972; 128: 901–11. doi: 10.1042/bj1280901

  30. Loke WM, Jenner AM, Proudfoot JM, McKinley AJ, Hodgson JM, Halliwell B, et al. A metabolite profiling approach to identify biomarkers of flavonoid intake in humans. J Nutr 2009; 139: 2309–14. doi: 10.3945/jn.109.113613

  31. Li C, Lee M-J, Sheng S, Meng X, Prabhu S, Winnik B, et al. Structural identification of two metabolites of catechins and their kinetics in human urine and blood after tea ingestion. Chem Res Toxicol 2000; 13: 177–84. doi: 10.1021/tx9901837

  32. Serra A, Macià A, Romero M-P, Reguant J, Ortega N, Motilva M-J. Metabolic pathways of the colonic metabolism of flavonoids (flavonols, flavones and flavanones) and phenolic acids. Food Chem 2012; 130: 383–93. doi: 10.1016/j.foodchem.2011.07.055

  33. Rechner AR, Smith MA, Kuhnle G, Gibson GR, Debnam ES, Srai SKS, et al. Colonic metabolism of dietary polyphenols: influence of structure on microbial fermentation products. Free Radical Bio Med 2004; 36: 212–25. doi: 10.1016/j.freeradbiomed.2003.09.022

  34. Winter J, Moore LH, Dowell VR, Bokkenheuser VD. C-ring cleavage of flavonoids by human intestinal bacteria. Appl Environ Microbiol 1989; 55: 1203–8. doi: 10.0000/PMID2757380

  35. Rafii F, Jackson LD, Ross I, Heinze TM, Lewis SM, Aidoo A, et al. Metabolism of daidzein by fecal bacteria in rats. Comparative Med 2007; 57: 282–6. doi: 10.1080/03079450701344738

  36. Hidalgo M, Oruna-Concha MJ, Kolida S, Walton GE, Kallithraka S, Spencer JPE, et al. Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. J Agr Food Chem 2012, 60: 3882–90. doi: 10.1021/jf3002153

  37. Gonthier MP, Remesy C, Scalbert A, Cheynier V, Souquet JM, Poutanen K, et al. Microbial metabolism of caffeic acid and its esters chlorogenic and caftaric acids by human faecal microbiota in vitro. Biomed Pharmacother 2006; 60: 536–40. doi: 10.1016/j.biopha.2006.07.084

  38. Szwajgier D, Jakubczyk A. Biotransformation of ferulic acid by Lactobacillus acidophilus Ki and selected Bifidobacterium strains. Acta Sci Pol Technol Aliment 2010; 9: 45–59. doi: 10.1016/j.biortech.2010.01.086

  39. Cerdá B, Periago P, Espín JC, Tomásbarberán FA. Identification of Urolithin A as a metabolite produced by human colon microflora from ellagic acid and related compounds. J Agr Food Chem 2005; 53: 5571–6. doi: 10.1021/jf050384i

  40. Fang J. Bioavailability of anthocyanins. Drug Metab Rev 2014; 46: 508–20. doi: 10.3109/03602532.2014.978080

  41. Fernandes I, Faria A, Calhau C, de Freitas V, Mateus N. Bioavailability of anthocyanins and derivatives. J Funct Foods 2014; 7: 54–66. doi: 10.1016/j.jff.2013.05.010

  42. Aura A-M, Martin-Lopez P, O’Leary KA, Williamson G, Oksman-Caldentey K-M, Poutanen K, et al. In vitro metabolism of anthocyanins by human gut microflora. Eur J Nutr 2005; 44: 133–42. doi: 10.1007/s00394-004-0502-2

  43. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A, et al. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. P Natl Acad Sci Usa 2009; 106: 5859–64. doi: 10.1073/pnas.0901529106

  44. Xue B, Xie J, Huang J, Chen L, Gao L, Ou S, et al. Plant polyphenols alter a pathway of energy metabolism by inhibiting fecal Bacteroidetes and Firmicutes in vitro. Food Funct 2016; 7: 1501–7. doi: 10.1039/c5fo01438g

  45. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. P Natl Acad Sci Usa 2005; 102: 11070–5. doi: 10.1073/pnas.0504978102

  46. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008; 3: 213–23. doi: 10.1016/j.chom.2008.02.015

  47. Singh RK, Chang H-W, Yan D, Lee KM, Ucmak D, Wong K, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med 2017; 15: 73. doi: 10.1186/s12967-017-1175-y

  48. Kemperman RA, Gross G, Mondot S, Possemiers S, Marzorati M, Van de Wiele T, et al. Impact of polyphenols from black tea and red wine/grape juice on a gut model microbiome. Food Res Int 2013; 53: 659–69. doi: 10.1016/j.foodres.2013.01.034

  49. Serino M, Luche E, Chabo C, Amar J, Burcelin R. Intestinal microflora and metabolic diseases. Diabetes Metab 2009; 35: 262–72. doi: 10.1016/j.diabet.2009.03.003

  50. Rastmanesh R. High polyphenol, low probiotic diet for weight loss because of intestinal microbiota interaction. Chem-Biol Interact 2011; 189: 1–8. doi: 10.1016/j.cbi.2010.10.002

  51. Queipo-Ortuño MI, Boto-Ordóñez M, Murri M, Gomez-Zumaquero JM, Clemente-Postigo M, Estruch R, et al. Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am J Clin Nutr 2012; 95: 1323–34. doi: 10.3945/ajcn.111.027847

  52. Etxeberria U, Arias N, Boqué N, Macarulla MT, Portillo MP, Martinez JA, et al. Reshaping faecal gut microbiota composition by the intake of trans -resveratrol and quercetin in high-fat sucrose diet-fed rats. J Nutr Biochem 2015; 26: 651–60. doi: 10.1016/j.jnutbio.2015.01.002

  53. Zhao L, Zhang Q, Ma W, Tian F, Shen H, Zhou M. A combination of quercetin and resveratrol reduces obesity in high-fat diet-fed rats by modulation of gut microbiota. Food Funct 2017; 8: 4644–56. doi: 10.1039/c7fo01383c

  54. Million M, Lagier JC, Yahav D, Paul M. Gut bacterial microbiota and obesity. Clin Microbiol Infec 2013; 19: 305–13. doi: 10.1111/1469-0691.12172

  55. Festi D, Schiumerini R, Eusebi LH, Marasco G, Taddia M, Colecchia A. Gut microbiota and metabolic syndrome. World J Gastroentero 2014; 20: 16079–94. doi: 10.3748/wjg.v20.i43.16079

  56. Sanchez M, Panahi S, Tremblay A. Childhood obesity: a role for gut microbiota? Int J Env Res Pub He 2015; 12: 162–75. doi: 10.3390/ijerph120100162

  57. Arora T, Singh S, Sharma RK. Probiotics: interaction with gut microbiome and antiobesity potential. Nutrition 2013; 29: 591–6. doi: 10.1016/j.nut.2012.07.017

  58. Chen J, He X, Huang J. Diet effects in gut microbiome and obesity. J Food Sci 2014; 79: R442–51. doi: 10.1111/1750-3841.12397

  59. Tzounis X, Rodriguez-Mateos A, Vulevic J, Gibson GR, Kwik-Uribe C, Spencer JPE. Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am J Clin Nutr 2011; 93: 62–72. doi: 10.3945/ajcn.110.000075

  60. Castell JV, Gómez-Lechón MJ, David M, Andus T, Geiger T, Trullenque R, et al. Interleukin-6 is the major regulator of acute phase protein synthesis in adult human hepatocytes. Febs Lett 1989; 242: 237–9. doi: 10.1016/0014-5793(89)80476-4

  61. Boutsikou T, Mastorakos G, Kyriakakou M, Margeli A, Hassiakos D, Papassotiriou I, et al. Circulating levels of inflammatory markers in intrauterine growth restriction. Mediat Inflamm 2010; 2010: 790605. doi: 10.1155/2010/790605

  62. Hage FG, Szalai AJ. C-reactive protein gene polymorphisms, C-reactive protein blood levels, and cardiovascular disease risk. J Am Coll Cardiol 2007; 50: 1115–22. doi: 10.1016/j.jacc.2007.06.012

  63. Ridker PM, Cook NR. Biomarkers for prediction of cardiovascular events. N Engl J Med 2007; 302: 1472–3. doi: 10.1001/jama.2009.1637

  64. Fogliano V, Corollaro ML, Vitaglione P, Napolitano A, Ferracane R, Travaglia F, et al. In vitro bioaccessibility and gut biotransformation of polyphenols present in the water-insoluble cocoa fraction. Mol Nutr Food Res 2011; 55: S44–55. doi: 10.1002/mnfr.201000360

  65. Neyrinck AM, Van Hée VF, Bindels LB, De Backer F, Cani PD, Delzenne NM. Polyphenol-rich extract of pomegranate peel alleviates tissue inflammation and hypercholesterolaemia in high-fat diet-induced obese mice: potential implication of the gut microbiota. Br J Nutr 2013; 109: 802–9. doi: 10.1017/S0007114512002206

  66. Fei N, Zhao L. An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J 2013; 7: 880–4. doi: 10.1038/is mej.2012.153

  67. Keskitalo A, Munukka E, Toivonen R, Hollmén M, Kainulainen H, Huovinen P, et al. Enterobacter cloacae administration induces hepatic damage and subcutaneous fat accumulation in high-fat diet fed mice. PLoS One 2018; 13: e0198262. doi: 10.1371/journal.pone.0198262

  68. Yan H, Fei N, Wu G, Zhang C, Zhao L, Zhang M. Regulated inflammation and lipid metabolism in colon mRNA expressions of obese germfree mice responding to enterobacter cloacae B29 combined with the high fat diet. Front Microbiol 2016; 7: 1786. doi: 10.3389/fmicb.2016.01786

  69. Lee HC, Jenner AM, Low CS, Lee YK. Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota. Res Microbiol 2006; 157: 876–84. doi: 10.1016/j.resmic.2006.07.004

  70. Moreno-Indias I, Sánchez-Alcoholado L, Pérez-Martínez P, Andrés-Lacueva C, Cardona F, Tinahones F, et al. Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients. Food Funct 2016; 7: 1775–87. doi: 10.1039/c5fo00886g

  71. Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 2016; 65: 426–36. doi: 10.1136/gutjnl-2014-308778

  72. van Passel MWJ, Kant R, Zoetendal EG, Plugge CM, Derrien M, Malfatti SA, et al. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One 2011; 6: e16876. doi: 10.1371/journal.pone.0016876

  73. Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM. The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microb 2008; 74: 1646–8. doi: 10.1128/AEM.01226-07

  74. Belzer C, de Vos WM. Microbes inside–from diversity to function: the case of Akkermansia. ISME J 2012; 6: 1449–58. doi: 10.1038/ismej.2012.6

  75. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli, GM, Neyrinck AM, et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 2011; 60: 2775–86. doi: 10.2337/db11-0227

  76. Everard A, Belzer C, Geurts L, Ouwerkerk, JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Pnas 2013; 110: 9066–71. doi: 10.1073/pnas.1219451110

  77. Ottman N, Geerlings SY, Aalvink S, de Vos WM, Belzer C. Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Pract Res Cl Ga 2017; 31: 637–42. doi: 10.1016/j.bpg.2017.10.001

  78. Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. Nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004; 54: 1469–76. doi: 10.1099/ijs.0.02873-0

  79. Roopchand DE, Carmody RN, Kuhn P, Moskal K, Rojas-Silva P, Turnbaugh PJ, et al. Dietary polyphenols promote growth of the gut bacteriumAkkermansia muciniphila and attenuate high-fat diet–induced metabolic syndrome. Diabetes 2015; 64: 2847–58. doi: 10.2337/db14-1916

  80. Henning SM, Summanen PH, Lee R-P, Yang J, Finegold SM, Heber D, et al. Pomegranate ellagitannins stimulate the growth of Akkermansia muciniphila in vivo. Anaerobe 2017; 43: 56–60. doi: 10.1016/j.anaerobe.2016.12.003

  81. Anhê FF, Roy D, Pilon G, Dudonné S, Matamoros S, Varin TV, et al. A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut 2015; 64: 872–83. doi: 10.1136/gutjnl-2014-307142

  82. Hu J, Lin S, Zheng B, Cheung PCK. Short-chain fatty acids in control of energy metabolism. Crit Rev Food Sci Nutr.2016; 58: 1243–9. doi: 10.1080/10408398.2016.1245650

  83. Yan Y, Peng Y, Tang J, Mi J, Lu L, Li X, et al. Effects of anthocyanins from the fruit of Lycium ruthenicum Murray on intestinal microbiota. J Funct Foods 2018; 48, 533–41. doi: 10.1016/j.jff.2018.07.053

  84. Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I. Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 2015; 7, 2839–49. doi: 10.3390/nu7042839

  85. Wright RS, Anderson JW, Bridges SR. Propionate inhibits hepatocyte lipid synthesis. Proceedings of the Society for Experimental Biology and Medicine Society 1990; 195: 26–9. doi: 10.3181/00379727-195-43113

  86. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. The microbiology of butyrate formation in the human colon. Fems Microbiol Lett 2002; 217: 133–9. doi: 10.1111/j.1574-6968.2002.tb11467

  87. Bauer E, Williams BA, Smidt H, Mosenthin R, Verstegen MWA. Influence of dietary components on development of the microbiota in single-stomached species. Nutr Res Rev 2006; 19: 63–78. doi: 10.1079/NRR2006123

  88. Bleau C, Karelis AD, St-Pierre DH, Lamontagne L. Crosstalk between intestinal microbiota, adipose tissue and skeletal muscle as an early event in systemic low-grade inflammation and the development of obesity and diabetes. Diabetes-Metab Res 2015; 31: 545–61. doi: 10.1002/dmrr.2617

  89. Blaut M, Schoefer L, Braune A. Transformation of flavonoids by intestinal microorganisms. Int J Vitam Nutr Res 2003; 73: 79–87. doi: 10.1024/0300-9831.73.2.79

  90. Zheng C-J, Liu R, Xue B, Luo J, Gao L, Wang Y, et al. Impact and consequences of polyphenols and fructooligosaccharide interplay on gut microbiota in rats. Food Funct 2017; 8: 1925–32. doi: 10.1039/c6fo01783e

  91. Hara H, Orita N, Hatano S, Ichikawa H, Hara Y, Matsumoto N, et al. Effect of tea polyphenols on fecal flora and fecal metabolic products of pigs. J Vet Med Sci 1995; 57: 45–9. doi: 10.1292/jvms.57.45

  92. Henning SM, Yang J, Hsu M, Lee R-P, Grojean EM, Ly A, et al. Decaffeinated green and black tea polyphenols decrease weight gain and alter microbiome populations and function in diet-induced obese mice. Eur J Nutr 2018; 57: 2759–69. doi: 10.1007/s00394-017-1542-8

  93. Kaminsky LS, Zhang Q-Y. The small intestine as a xenobiotic-metabolizing organ. Drug Metab Dispos 2003; 31: 1520–5. doi: 10.1124/dmd.31.12.15290

  94. Mcdonald M, Mila I, Scalbert A. Precipitation of metal ions by plant polyphenols: optimal conditions and origin of precipitation. J Agr Food Chem 1996; 44: 599–606. doi: 10.1021/jf950459q

  95. Smith AH, Zoetendal E, Mackie RI. Bacterial mechanisms to overcome inhibitory effects of dietary tannins. Microbial Ecol 2005; 50: 197–205. doi: 10.1007/s00248-004-0180-x

  96. Matera G, Barreca GS, Puccio R, Quirino A, Liberto MC, De RM, et al. Stenotrophomonas maltophilia lipopolysaccharide (LPS) and antibiotics: ‘in vitro’ effects on inflammatory mediators. Infez Med 2004; 12: 227–38.

  97. Navarro-Martínez MD, Navarro-Perán E, Cabezas-Herrera J, Ruiz-Gómez J, García-Cánovas F, Rodríguez-López JN. Antifolate Activity of Epigallocatechin Gallate against Stenotrophomonas maltophilia. Antimicro Agents 2005; 49: 2914–20. doi: 10.1128/AAC.49.7.2914-2920.2005

  98. Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Yetukuri L, Islam S, et al. The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 2010; 51: 1101–12. doi: 10.1194/jlr.M002774

  99. Zhang L, Carmody RN, Kalariya HM, Duran RM, Moskal K, Poulev A, et al. Grape proanthocyanidin-induced intestinal bloom of Akkermansia muciniphila is dependent on its baseline abundance and precedes activation of host genes related to metabolic health. J Nutr Biochem 2018; 56: 142–51. doi: 10.1016/j.jnutbio.2018.02.009

  100. Shen W, Gaskins HR, McIntosh MK. Influence of dietary fat on intestinal microbes, inflammation, barrier function and metabolic outcomes. J Nutr Biochem 2014; 25: 270–80. doi: 10.1016/j.jnutbio.2013.09.009

  101. Moreno MF, Anhê FF, Nachbar R, St-Pierre P, Oyama LM, Marette A. Effect of synergism between leucine and quercetIn: a new strategy against metabolic disorders. Isanh 2016; 3. doi: 10.18143/JISANH_v3i4_1342

  102. Pham P, Cotten R, Kolinek T, Parker S, Vattem D, Maitin V. Preliminary characterization of secreted bioactive compounds from Bifidobacterium longum with modulatory activity towards enterocytic Fasting Induced Adipocyte Factor (FIAF). Faseb J 2012; 26(1_supplement): 373.6.

  103. Lukovac S, Belzer C, Pellis L, Keijser BJ, de Vos WM, Montijn RC, et al. Differential Modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. Mbio 2014; 5: e01438–14. doi: 10.1128/mBio.01438-14

  104. Jamar G, Estadella D, Pisani LP. Contribution of anthocyanin-rich foods in obesity control through gut microbiota interactions. BioFactors 2017; 43: 507–16. doi: 10.1002/biof.1365

  105. Qiao Y, Sun J, Xia S, Tang X, Shi Y, Le G. Effects of resveratrol on gut microbiota and fat storage in a mouse model with high-fat-induced obesity. Food Funct 2014; 5: 1241–9. doi: 10.1039/c3fo60630a

  106. Grootaert C, Van de Wiele T, Van Roosbroeck I, Possemiers S, Vercoutter-Edouart A-S, Verstraete W, et al. Bacterial monocultures, propionate, butyrate and H2O2 modulate the expression, secretion and structure of the fasting induced adipose factor in gut epithelial cell lines. Environ Microbiol 2011; 13: 1778–89. doi: 10.1111/j.1462-2920.2011.02482.x

  107. Li Y, Perry T, Kindy MS, Harvey BK, Tweedie D, Holloway HW, et al. GLP-1 receptor stimulation preserves primary cortical and dopaminergic neurons in cellular and rodent models of stroke and Parkinsonism. P Natl Acad Sci Usa 2009; 106: 1285–90. doi: 10.1073/pnas.0806720106

  108. Panickar KS. Effects of dietary polyphenols on neuroregulatory factors and pathways that mediate food intake and energy regulation in obesity. Mol Nutr Food Res 2013; 57: 34–47. doi: 10.1002/mnfr.201200431

  109. Dao TMA, Waget A, Klopp P, Serino M, Vachoux C, Pechere L, et al. Resveratrol increases glucose induced GLP-1 secretion in mice: a mechanism which contributes to the glycemic control. PLoS One 2013; 6: e20700. doi: 10.1371/journal.pone.0020700

  110. Kato M, Tani T, Terahara N, Tsuda T. The anthocyanin delphinidin 3-rutinoside stimulates glucagon-like peptide-1 secretion in murine GLUTag cell line via the Ca21/calmodulin-dependent kinase II pathway. PLoS One 2015; 11: e0126157. doi: 10.1371/journal.pone.0126157

  111. Psichas A, Sleeth ML, Murphy KG, Brooks L, Bewick GA, Hanyaloglu AC, et al. The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int J Obes 2015; 39: 424–9. doi: 10.1038/ijo.2014.153

  112. Yadav H, Lee J-H, Lloyd J, Walter P, Rane SG. Beneficial metabolic effects of a probiotic via Butyrate-induced GLP-1 hormone secretion. J Biol Chem 2013; 288: 25088–97. doi: 10.1074/jbc.M113.452516

  113. Gorboulev V, Schürmann A, Vallon V, Kipp H, Jaschke A, Klessen D, et al. Na+-d-glucose Cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes 2012; 61: 187–96. doi: 10.2337/db11-1029

  114. Wang Z, Clifford MN, Sharp P. Analysis of chlorogenic acids in beverages prepared from Chinese health foods and investigation, in vitro, of effects on glucose absorption in cultured Caco-2 cells. Food Chem 2008; 108: 369–73. doi: 10.1016/j.foodchem.2007.10.083

  115. Manzano S, Williamson G. Polyphenols and phenolic acids from strawberry and apple decrease glucose uptake and transport by human intestinal Caco-2 cells. Mol Nutr Food Res 2010; 54: 1773–80. doi: 10.1002/mnfr.201000019

  116. Kwon O, Eck P, Chen S, Corpe CP, Lee JH, Kruhlak M, et al. Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. Faseb J 2007; 21: 366–77. doi: 10.1096/fj.06-6620com

  117. Kobayashi Y, Suzuki M, Satsu H, Arai S, Hara Y, Suzuki K, et al. Green tea polyphenols inhibit the sodium-dependent glucose transporter of intestinal epithelial cells by a competitive mechanism. J Agr Food Chem 2000; 48: 5618–23. doi: 10.1021/jf0006832

  118. Schulze C, Bangert A, Kottra G, Geillinger KE, Schwanck B, Vollert H, et al. Inhibition of the intestinal sodium-coupled glucose transporter 1 (SGLT1) by extracts and polyphenols from apple reduces postprandial blood glucose levels in mice and humans. Mol Nutr Food Res 2014; 58: 1795–808. doi: 10.1002/mnfr.201400016

  119. Masumoto S, Akimoto Y, Oike H, Kobori M. Dietary phloridzin reduces blood glucose levels and reverses Sglt1 expression in the small intestine in streptozotocin-induced diabetic mice. J Agr Food Chem 2009; 57: 4651–6. doi: 10.1021/jf9008197

  120. Schulze C, Bangert A, Schwanck B, Vollert H, Blaschek W, Daniel H. Extracts and flavonoids from onion inhibit the intestinal sodium-coupled glucose transporter 1 (SGLT1) in vitro but show no anti-hyperglycaemic effects in vivo in normoglycaemic mice and human volunteers. J Funct Foods 2015; 18: 117–28. doi: 10.1016/j.jff.2015.06.037

  121. Johnston K, Sharp P, Clifford M, Morgan L. Dietary polyphenols decrease glucose uptake by human intestinal Caco-2 cells. Febs Lett 2005; 579: 1653–7. doi: 10.1016/j.febslet.2004.12.099.

  122. Toop CR, Gentili S. Fructose beverage consumption induces a metabolic syndrome phenotype in the rat: a systematic review and meta-analysis. Nutrients 2016; 8: 577. doi: 10.3390/nu8090577

  123. Andrade N, Araújo JR, Correia-Branco A, Carletti JV, Martel F. Effect of dietary polyphenols on fructose uptake by human intestinal epithelial (Caco-2) cells. J Funct Foods 2017; 36: 429–39. doi: 10.1016/j.soard.2017.09.494

  124. Lee Y, Lim Y, Kwon O. Selected phytochemicals and culinary plant extracts inhibit fructose uptake in Caco-2 cells. Molecules 2015; 20: 17393–404. doi: 10.3390/molecules200917393

  125. Farrell TL, Ellam SL, Forrelli T, Williamson G. Attenuation of glucose transport across Caco-2 cell monolayers by a polyphenol-rich herbal extract: interactions with SGLT1 and GLUT2 transporters. Biofactors 2013; 39: 448–56. doi: 10.1002/biof.1090

  126. Castro Acosta ML. Beneficial effects of blackcurrant and apple polyphenols on glucose homeostasis. London: King’s College London; 2017.

  127. Cao H, Urban JJF, Anderson RA. Cinnamon polyphenol extract affects immune responses by regulating anti- and proinflammatory and glucose transporter gene expression in mouse macrophages. J Nutr 2008; 138: 833–40. doi: 10.1093/jn/138.5.833

  128. Gil-Cardoso K, Ginés I, Pinent M, Ardévol A, Blay M, Terra X. Effects of flavonoids on intestinal inflammation, barrier integrity and changes in gut microbiota during diet-induced obesity. Nutr Res Rev 2016; 29: 234–48. doi: 10.1017/S0954422416000159

  129. Williams AR, Krych L, Fauzan Ahmad H, Nejsum P, Skovgaard K, Nielsen DS, et al. A polyphenol-enriched diet and Ascaris suum infection modulate mucosal immune responses and gut microbiota composition in pigs. PLoS One 2017; 12: e0186546. doi: 10.1371/journal.pone.0186546

  130. Romier B, Schneider YJ, Larondelle Y, During A. Dietary polyphenols can modulate the intestinal inflammatory response. Nutr Rev 2009; 67: 363–78. doi: 10.1111/j.1753-4887.2009.00210.x

  131. Farzaei M, Rahimi R, Abdollahi M. The role of dietary polyphenols in the management of inflammatory bowel disease. Curr Pharm Biotechno 2015; 16: 196–210. doi: 10.2174/1389201016666150118131704

  132. Zhao L. The gut microbiota and obesity: from correlation to causality. Nat Rev Microbiol 2013; 11: 639–47. doi: 10.1038/nrmicro3089

  133. Fan X, Jiao H, Zhao J, Wang X, Lin H. Lipopolysaccharide impairs mucin secretion and stimulated mucosal immune stress response in respiratory tract of neonatal chicks. Comp Biochem Phys C 2017; 204: 71–8. doi: 10.1016/j.cbpc.2017.11.011

  134. Wong X, Madrid AM, Tralma K, Castilo R, Carrasco-Pozo C, Navarrete P, et al. Polyphenol extracts interfere with bacterial lipopolysaccharide in vitro and decrease postprandial endotoxemia in human volunteers. J Funct Foods 2016; 26: 406–17. doi: 10.1016/j.jff.2016.08.011

  135. Morais CA, Oyama LM, Oliveira JLD, Garcia MC, Rosso VVD, Amigo LSM, et al. Jussara (Euterpe edulis Mart.) supplementation during pregnancy and lactation modulates the gene and protein expression of inflammation biomarkers induced by trans-fatty acids in the colon of offspring. Mediat Inflamm 2014; 2014: 987927. doi: 10.1155/2014/987927

  136. Radnai B, Tucsek Z, Bognar Z, Antus C, Mark L, Berente Z, et al. A water-soluble degradation product of polyphenols, inhibits the lipopolysaccharide-induced inflammatory response in mice. J Nutr 2009; 139: 291–7. doi: 10.3945/jn.108.101345

  137. González-Sarrías A, Larrosa M, Tomás-Barberán FA, Dolara P, Espín JC. NF-κB-dependent anti-inflammatory activity of urolithins, gut microbiota ellagic acid-derived metabolites, in human colonic fibroblasts. Brit J Nutr 2010; 104: 503–12. doi: 10.1017/S0007114510000826

  138. Okoko T, Oruambo IF. Inhibitory activity of quercetin and its metabolite on lipopolysaccharide-induced activation of macrophage U937 cells. Food Chem Toxicol 2009; 47: 809–12. doi: 10.1016/j.fct.2009.01.013

How to Cite
Lin S, Wang Z, Lam K-L, Zeng S, Tan B, Hu J. Role of intestinal microecology in the regulation of energy metabolism by dietary polyphenols and their metabolites. fnr [Internet]. 2019Feb.14 [cited 2019Mar.20];630. Available from:
Review Articles