Skip to main content

Advertisement

Log in

Gut Microbiota, Dietary Phytochemicals, and Benefits to Human Health

  • Microbiome (A Patterson, Section Editor)
  • Published:
Current Pharmacology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

In this review, we discuss the roles of the gut microbiota and dietary phytochemicals in improving human health. Recent studies have reported that the human gut microbiota can be altered by dietary phytochemicals, including phenolics, carotenoids, and dietary fibers. In addition, both pathogenic and nonpathogenic bacteria show regulatory effects with phytochemicals, suggesting potential synergistic effects in the improvement of human gut health and prevention of chronic diseases.

Recent Findings

Numerous studies have been conducted on gut microbial alterations induced by phytochemicals, such as phenolics and carotenoids. Butyrate, a short-chain fatty acid produced via bacterial fermentation in the colon, also shows a significantly beneficial effect in the maintenance of gut microbial homeostasis. However, the molecular mechanisms underlying the effects of diets and the interactions of the gut microorganisms remain poorly understood. The gut microbiome profile changes have been observed in chronic inflammation-induced diseases, including colitis, Crohn’s disease, immune dysfunction, colon cancer, obesity, and diabetes. The anti-inflammatory effects of dietary phytochemicals against these diseases may be partially mediated by the regulation of microbial profiles. The latest advances in biomedical technology, such as next-generation sequencing (NGS), and continuous cost reduction associated with these technologies have enabled researchers to perform an ever-increasing number of large-scale, high-throughput computational analyses to elucidate the potential mechanism of phytochemical–microbiome interactions.

Summary

Information obtained from these studies may provide valuable insights to guide future clinical research for the development of therapeutics, botanicals, and drug efficacy testing, many of which will be discussed in this review.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Allaband C, McDonald D, Vázquez-Baeza Y, Minich JJ, Tripathi A, Brenner DA, et al. Microbiome 101: studying, analyzing, and interpreting gut microbiome data for clinicians. Clin Gastroenterol Hepatol. 2019;17(2):218–30. https://doi.org/10.1016/j.cgh.2018.09.017.

    Article  PubMed  Google Scholar 

  2. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837–48. https://doi.org/10.1016/j.cell.2006.02.017.

    Article  CAS  PubMed  Google Scholar 

  3. Dave M, Higgins PD, Middha S, Rioux KP. The human gut microbiome: current knowledge, challenges, and future directions. Transl Res. 2012;160(4):246–57. https://doi.org/10.1016/j.trsl.2012.05.003.

    Article  CAS  PubMed  Google Scholar 

  4. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533. https://doi.org/10.1371/journal.pbio.1002533.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336(6086):1268–73. https://doi.org/10.1126/science.1223490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jarchum I, Pamer EG. Regulation of innate and adaptive immunity by the commensal microbiota. Curr Opin Immunol. 2011;23(3):353–60. https://doi.org/10.1016/j.coi.2011.03.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol. 2012;8(1):36–45. https://doi.org/10.1038/nchembio.741.

    Article  CAS  Google Scholar 

  8. Ismail AS, Hooper LV. Epithelial cells and their neighbors. IV. Bacterial contributions to intestinal epithelial barrier integrity. Am J Physiol Gastrointest Liver Physiol. 2005;289(5):G779–84. https://doi.org/10.1152/ajpgi.00203.2005.

    Article  CAS  PubMed  Google Scholar 

  9. Ramakrishna BS. Role of the gut microbiota in human nutrition and metabolism. J Gastroenterol Hepatol. 2013;28:9–17. https://doi.org/10.1111/jgh.12294.

    Article  CAS  PubMed  Google Scholar 

  10. El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol. 2013;11(7):497–504. https://doi.org/10.1038/nrmicro3050.

    Article  CAS  PubMed  Google Scholar 

  11. Kamada N, Chen GY, Inohara N, Núñez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14(7):685–90. https://doi.org/10.1038/ni.2608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Bäumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016;535(7610):85–93. https://doi.org/10.1038/nature18849.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. https://doi.org/10.1038/nmeth.f.303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3. https://doi.org/10.1038/Nmeth.3869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bäckhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM, et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012;12(5):611–22. https://doi.org/10.1016/j.chom.2012.10.012.

    Article  CAS  PubMed  Google Scholar 

  16. Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014;146(6):1489–99. https://doi.org/10.1053/j.gastro.2014.02.009.

    Article  CAS  PubMed  Google Scholar 

  17. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13(9):R79. https://doi.org/10.1186/gb-2012-13-9-r79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Greenblum S, Turnbaugh PJ, Borenstein E. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A. 2012;109(2):594–9. https://doi.org/10.1073/pnas.1116053109.

    Article  PubMed  Google Scholar 

  19. Lu B, Li M, Yin R. Phytochemical content, health benefits, and toxicology of common edible flowers: a review (2000–2015). Crit Rev Food Sci Nutr. 2016;56(Suppl 1):S130–48. https://doi.org/10.1080/10408398.2015.1078276.

    Article  CAS  PubMed  Google Scholar 

  20. Yin R, Li T, Tian JX, Xi P, Liu RH. Ursolic acid, a potential anticancer compound for breast cancer therapy. Crit Rev Food Sci Nutr. 2018;58(4):568–74. https://doi.org/10.1080/10408398.2016.1203755.

    Article  CAS  PubMed  Google Scholar 

  21. Liu RH. Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. Am J Clin Nutr. 2003;78(3 Suppl):517S–20S. https://doi.org/10.1093/ajcn/78.3.517S.

    Article  CAS  PubMed  Google Scholar 

  22. Sun J, Chu YF, Wu X, Liu RH. Antioxidant and antiproliferative activities of common fruits. J Agric Food Chem. 2002;50(25):7449–54.

    Article  CAS  PubMed  Google Scholar 

  23. Lyu Y, Wu L, Wang F, Shen X, Lin D. Carotenoid supplementation and retinoic acid in immunoglobulin A regulation of the gut microbiota dysbiosis. Exp Biol Med (Maywood). 2018;243(7):613–20. https://doi.org/10.1177/1535370218763760.

    Article  CAS  Google Scholar 

  24. Gomez A, Petrzelkova K, Yeoman CJ, Vlckova K, Mrázek J, Koppova I, et al. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Mol Ecol. 2015;24(10):2551–65. https://doi.org/10.1111/mec.13181.

    Article  CAS  PubMed  Google Scholar 

  25. Russell W, Duthie G. Plant secondary metabolites and gut health: the case for phenolic acids. Proc Nutr Soc. 2011;70(3):389–96. https://doi.org/10.1017/S0029665111000152.

    Article  CAS  PubMed  Google Scholar 

  26. Wang SY, Chen CT, Sciarappa W, Wang CY, Camp MJ. Fruit quality, antioxidant capacity, and flavonoid content of organically and conventionally grown blueberries. J Agric Food Chem. 2008;56(14):5788–94. https://doi.org/10.1021/jf703775r.

    Article  CAS  PubMed  Google Scholar 

  27. Ferguson PJ, Kurowska EM, Freeman DJ, Chambers AF, Koropatnick J. In vivo inhibition of growth of human tumor lines by flavonoid fractions from cranberry extract. Nutr Cancer. 2006;56(1):86–94. https://doi.org/10.1207/s15327914nc5601_12.

    Article  CAS  PubMed  Google Scholar 

  28. Rice-Evans CA, Miller NJ, Bolwell PG, Bramley PM, Pridham JB. The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Radic Res. 1995;22(4):375–83.

    Article  CAS  PubMed  Google Scholar 

  29. Duda-Chodak A. The inhibitory effect of polyphenols on human gut microbiota. J Physiol Pharmacol. 2012;63(5):497–503.

    CAS  PubMed  Google Scholar 

  30. Etxeberria U, Fernández-Quintela A, Milagro FI, Aguirre L, Martínez JA, Portillo MP. Impact of polyphenols and polyphenol-rich dietary sources on gut microbiota composition. J Agric Food Chem. 2013;61(40):9517–33. https://doi.org/10.1021/jf402506c.

    Article  CAS  PubMed  Google Scholar 

  31. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–8. https://doi.org/10.1126/science.1208344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Braune A, Blaut M. Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes. 2016;7(3):216–34. https://doi.org/10.1080/19490976.2016.1158395.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Hidalgo M, Oruna-Concha MJ, Kolida S, Walton GE, Kallithraka S, Spencer JP, et al. Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. J Agric Food Chem. 2012;60(15):3882–90. https://doi.org/10.1021/jf3002153.

    Article  CAS  PubMed  Google Scholar 

  34. Braune A, Gütschow M, Engst W, Blaut M. Degradation of quercetin and luteolin by Eubacterium ramulus. Appl Environ Microbiol. 2001;67(12):5558–67. https://doi.org/10.1128/AEM.67.12.5558-5567.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Schoefer L, Mohan R, Schwiertz A, Braune A, Blaut M. Anaerobic degradation of flavonoids by Clostridium orbiscindens. Appl Environ Microbiol. 2003;69(10):5849–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Liu RH. Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr. 2004;134(12 Suppl):3479S–85S. https://doi.org/10.1093/jn/134.12.3479S.

    Article  CAS  PubMed  Google Scholar 

  37. de Vries JH, Janssen PL, Hollman PC, van Staveren WA, Katan MB. Consumption of quercetin and kaempferol in free-living subjects eating a variety of diets. Cancer Lett. 1997;114(1–2):141–4.

    Article  PubMed  Google Scholar 

  38. Miean KH, Mohamed S. Flavonoid (myricetin, quercetin, kaempferol, luteolin, and apigenin) content of edible tropical plants. J Agric Food Chem. 2001;49(6):3106–12.

    Article  CAS  PubMed  Google Scholar 

  39. Selma MV, Espin JC, Tomas-Barberan FA. Interaction between phenolics and gut microbiota: role in human health. J Agr Food Chem. 2009;57(15):6485–501. https://doi.org/10.1021/jf902107d.

    Article  CAS  Google Scholar 

  40. Rechner AR, Smith MA, Kuhnle G, Gibson GR, Debnam ES, Srai SK, et al. Colonic metabolism of dietary polyphenols: influence of structure on microbial fermentation products. Free Radic Biol Med. 2004;36(2):212–25.

    Article  CAS  PubMed  Google Scholar 

  41. Wu X, Cao G, Prior RL. Absorption and metabolism of anthocyanins in elderly women after consumption of elderberry or blueberry. J Nutr. 2002;132(7):1865–71. https://doi.org/10.1093/jn/132.7.1865.

    Article  CAS  PubMed  Google Scholar 

  42. Pantelidis GE, Vasilakakis M, Manganaris GA, Diamantidis G. Antioxidant capacity, phenol, anthocyanin and ascorbic acid contents in raspberries, blackberries, red currants, gooseberries and Cornelian cherries. Food Chem. 2007;102(3):777–83. https://doi.org/10.1016/j.foodchem.2006.06.021.

    Article  CAS  Google Scholar 

  43. Volden J, Bengtsson GB, Wicklund T. Glucosinolates, L-ascorbic acid, total phenols, anthocyanins, antioxidant capacities and colour in cauliflower (Brassica oleracea L. ssp. botrytis); effects of long-term freezer storage. Food Chem. 2009;112(4):967–76. https://doi.org/10.1016/j.foodchem.2008.07.018.

    Article  CAS  Google Scholar 

  44. Llorach R, Martínez-Sánchez A, Tomás-Barberán FA, Gil MI, Ferreres F. Characterisation of polyphenols and antioxidant properties of five lettuce varieties and escarole. Food Chem. 2008;108(3):1028–38. https://doi.org/10.1016/j.foodchem.2007.11.032.

    Article  CAS  PubMed  Google Scholar 

  45. González-Barrio R, Edwards CA, Crozier A. Colonic catabolism of ellagitannins, ellagic acid, and raspberry anthocyanins: in vivo and in vitro studies. Drug Metab Dispos. 2011;39(9):1680–8. https://doi.org/10.1124/dmd.111.039651.

    Article  CAS  PubMed  Google Scholar 

  46. Sun H, Zhang P, Zhu Y, Lou Q, He S. Antioxidant and prebiotic activity of five peonidin-based anthocyanins extracted from purple sweet potato (Ipomoea batatas (L.) Lam.). Sci Rep. 2018;8(1):5018. https://doi.org/10.1038/s41598-018-23397-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhu Y, Sun H, He S, Lou Q, Yu M, Tang M, et al. Metabolism and prebiotics activity of anthocyanins from black rice (Oryza sativa L.) in vitro. PLoS One. 2018;13(4):e0195754. https://doi.org/10.1371/journal.pone.0195754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hanske L, Engst W, Loh G, Sczesny S, Blaut M, Braune A. Contribution of gut bacteria to the metabolism of cyanidin 3-glucoside in human microbiota-associated rats. Brit J Nutr. 2013;109(8):1433–41. https://doi.org/10.1017/S0007114512003376.

    Article  CAS  PubMed  Google Scholar 

  49. Chen L, Jiang B, Zhong C, Guo J, Zhang L, Mu T, et al. Chemoprevention of colorectal cancer by black raspberry anthocyanins involved the modulation of gut microbiota and SFRP2 demethylation. Carcinogenesis. 2018;39(3):471–81. https://doi.org/10.1093/carcin/bgy009.

    Article  CAS  PubMed  Google Scholar 

  50. Gu J, Thomas-Ahner JM, Riedl KM, Bailey MT, Vodovotz Y, Schwartz SJ, et al. Dietary black raspberries impact the colonic microbiome and phytochemical metabolites in mice. Mol Nutr Food Res. 2019;63(8):e1800636. https://doi.org/10.1002/mnfr.201800636.

    Article  CAS  PubMed  Google Scholar 

  51. Paturi G, Butts CA, Monro JA, Hedderley D. Effects of blackcurrant and dietary fibers on large intestinal health biomarkers in rats. Plant Foods Hum Nutr. 2018;73(1):54–60.

    Article  CAS  PubMed  Google Scholar 

  52. Fernández J, García L, Monte J, Villar CJ, Lombó F. Functional anthocyanin-rich sausages diminish colorectal cancer in an animal model and reduce pro-inflammatory bacteria in the intestinal microbiota. Genes (Basel). 2018;9(3):133. https://doi.org/10.3390/genes9030133.

    Article  CAS  Google Scholar 

  53. Lee S, Keirsey KI, Kirkland R, Grunewald ZI, Fischer JG, de La Serre CB. Blueberry supplementation influences the gut microbiota, inflammation, and insulin resistance in high-fat-diet-fed rats. J Nutr. 2018;148(2):209–19. https://doi.org/10.1093/jn/nxx027.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Boto-Ordóñez M, Urpi-Sarda M, Queipo-Ortuño MI, Tulipani S, Tinahones FJ, Andres-Lacueva C. High levels of Bifidobacteria are associated with increased levels of anthocyanin microbial metabolites: a randomized clinical trial. Food Funct. 2014;5(8):1932–8. https://doi.org/10.1039/c4fo00029c.

    Article  CAS  PubMed  Google Scholar 

  55. Hester SN, Mastaloudis A, Gray R, Antony JM, Evans M, Wood SM. Efficacy of an anthocyanin and prebiotic blend on intestinal environment in obese male and female subjects. J Nutr Metab. 2018;2018:7497260. https://doi.org/10.1155/2018/7497260.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Khanbabaee K, van Ree T. Tannins: classification and definition. Nat Prod Rep. 2001;18(6):641–9.

    Article  CAS  PubMed  Google Scholar 

  57. Moilanen J, Koskinen P, Salminen JP. Distribution and content of ellagitannins in Finnish plant species. Phytochemistry. 2015;116:188–97. https://doi.org/10.1016/j.phytochem.2015.03.002.

    Article  CAS  PubMed  Google Scholar 

  58. Okuda T, Yoshida T, Hatano T. Ellagitannins as active constituents of medicinal plants. Planta Med. 1989;55(2):117–22. https://doi.org/10.1055/s-2006-961902.

    Article  CAS  PubMed  Google Scholar 

  59. Fecka I. Qualitative and quantitative determination of hydrolysable tannins and other polyphenols in herbal products from meadowsweet and dog rose. Phytochem Anal. 2009;20(3):177–90. https://doi.org/10.1002/pca.1113.

    Article  CAS  PubMed  Google Scholar 

  60. Landete JM. Ellagitannins, ellagic acid and their derived metabolites: a review about source, metabolism, functions and health. Food Res Int. 2011;44(5):1150–60. https://doi.org/10.1016/j.foodres.2011.04.027.

    Article  CAS  Google Scholar 

  61. Bialonska D, Kasimsetty SG, Khan SI, Ferreira D. Urolithins, intestinal microbial metabolites of pomegranate ellagitannins, exhibit potent antioxidant activity in a cell-based assay. J Agric Food Chem. 2009;57(21):10181–6.

    Article  CAS  PubMed  Google Scholar 

  62. Romo-Vaquero M, Cortés-Martín A, Loria-Kohen V, Ramírez-de-Molina A, García-Mantrana I, Collado MC, et al. Deciphering the human gut microbiome of urolithin metabotypes: association with enterotypes and potential cardiometabolic health implications. Mol Nutr Food Res. 2019;63(4):e1800958. https://doi.org/10.1002/mnfr.201800958.

    Article  CAS  PubMed  Google Scholar 

  63. García-Villalba R, Beltrán D, Espín JC, Selma MV, Tomás-Barberán FA. Time course production of urolithins from ellagic acid by human gut microbiota. J Agric Food Chem. 2013;61(37):8797–806. https://doi.org/10.1021/jf402498b.

    Article  CAS  PubMed  Google Scholar 

  64. Bialonska D, Ramnani P, Kasimsetty SG, Muntha KR, Gibson GR, Ferreira D. The influence of pomegranate by-product and punicalagins on selected groups of human intestinal microbiota. Int J Food Microbiol. 2010;140(2–3):175–82. https://doi.org/10.1016/j.ijfoodmicro.2010.03.038.

    Article  CAS  PubMed  Google Scholar 

  65. Bialonska D, Kasimsetty SG, Schrader KK, Ferreira D. The effect of pomegranate (Punica granatum L.) byproducts and ellagitannins on the growth of human gut bacteria. J Agric Food Chem. 2009;57(18):8344–9.

    Article  CAS  PubMed  Google Scholar 

  66. Marín L, Miguélez EM, Villar CJ, Lombó F. Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed Res Int. 2015;2015:905215. https://doi.org/10.1155/2015/905215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kawabata K, Yoshioka Y, Terao J. Role of intestinal microbiota in the bioavailability and physiological functions of dietary polyphenols. Molecules. 2019;24(2):370. https://doi.org/10.3390/molecules24020370.

    Article  CAS  PubMed Central  Google Scholar 

  68. Barnes RC, Krenek KA, Meibohm B, Mertens-Talcott SU, Talcott ST. Urinary metabolites from mango (Mangifera indica L. cv. Keitt) galloyl derivatives and in vitro hydrolysis of gallotannins in physiological conditions. Mol Nutr Food Res. 2016;60(3):542–50. https://doi.org/10.1002/mnfr.201500706.

    Article  CAS  PubMed  Google Scholar 

  69. Burns J, Fraser PD, Bramley PM. Identification and quantification of carotenoids, tocopherols and chlorophylls in commonly consumed fruits and vegetables. Phytochemistry. 2003;62(6):939–47.

    Article  CAS  PubMed  Google Scholar 

  70. Rinninella E, Mele M, Merendino N, Cintoni M, Anselmi G, Caporossi A, et al. The role of diet, micronutrients and the gut microbiota in age-related macular degeneration: new perspectives from the gut–retina axis. Nutrients. 2018;10(11):1677.

    Article  CAS  PubMed Central  Google Scholar 

  71. Rao AV, Rao LG. Carotenoids and human health. Pharmacol Res. 2007;55(3):207–16.

    Article  CAS  PubMed  Google Scholar 

  72. Fiedor J, Burda K. Potential role of carotenoids as antioxidants in human health and disease. Nutrients. 2014;6(2):466–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Magnuson AD, Sun T, Yin R, Liu G, Tolba S, Shinde S, et al. Supplemental microalgal astaxanthin produced coordinated changes in intrinsic antioxidant systems of layer hens exposed to heat stress. Algal Res. 2018;33:84–90. https://doi.org/10.1016/j.algal.2018.04.031.

    Article  Google Scholar 

  74. Ambati R, Phang S-M, Ravi S, Aswathanarayana RG. Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Mar Drugs. 2014;12(1):128–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Sun T, Yin R, Magnuson AD, Tolba SA, Liu GC, Lei XG. Dose-dependent enrichments and improved redox status in tissues of broiler chicks under heat stress by dietary supplemental microalgal astaxanthin. J Agr Food Chem. 2018;66(22):5521–30. https://doi.org/10.1021/acs.jafc.8b00860.

    Article  CAS  Google Scholar 

  76. Liu H, Liu M, Fu X, Zhang Z, Zhu L, Zheng X, et al. Astaxanthin prevents alcoholic fatty liver disease by modulating mouse gut microbiota. Nutrients. 2018;10(9):1298.

    Article  CAS  PubMed Central  Google Scholar 

  77. Bennedsen M, Wang X, Willén R, Wadström T, Andersen LP. Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunol Lett. 1999;70(3):185–9.

    Article  CAS  PubMed  Google Scholar 

  78. Tuohy KM, Conterno L, Gasperotti M, Viola R. Up-regulating the human intestinal microbiome using whole plant foods, polyphenols, and/or fiber. J Agr Food Chem. 2012;60(36):8776–82. https://doi.org/10.1021/jf2053959.

    Article  CAS  Google Scholar 

  79. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107(33):14691–6. https://doi.org/10.1073/pnas.1005963107.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Tasse L, Bercovici J, Pizzut-Serin S, Robe P, Tap J, Klopp C, et al. Functional metagenomics to mine the human gut microbiome for dietary fiber catabolic enzymes. Genome Res. 2010;20(11):1605–12. https://doi.org/10.1101/gr.108332.110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol. 1991;70(6):443–59. https://doi.org/10.1111/j.1365-2672.1991.tb02739.x.

    Article  CAS  PubMed  Google Scholar 

  82. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett. 2002;217(2):133–9. https://doi.org/10.1111/j.1574-6968.2002.tb11467.x.

    Article  CAS  PubMed  Google Scholar 

  83. Sealy L, Chalkley R. The effect of sodium butyrate on histone modification. Cell. 1978;14(1):115–21.

    Article  CAS  PubMed  Google Scholar 

  84. Bourassa MW, Alim I, Bultman SJ, Ratan RR. Butyrate, neuroepigenetics and the gut microbiome: can a high fiber diet improve brain health? Neurosci Lett. 2016;625:56–63. https://doi.org/10.1016/j.neulet.2016.02.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Candido EP, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 1978;14(1):105–13.

    Article  CAS  PubMed  Google Scholar 

  86. Gardian G, Browne SE, Choi DK, Klivenyi P, Gregorio J, Kubilus JK, et al. Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington’s disease. J Biol Chem. 2005;280(1):556–63. https://doi.org/10.1074/jbc.M410210200.

    Article  CAS  PubMed  Google Scholar 

  87. Säemann MD, Böhmig GA, Osterreicher CH, Burtscher H, Parolini O, Diakos C, et al. Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000;14(15):2380–2. https://doi.org/10.1096/fj.00-0359fje.

    Article  PubMed  Google Scholar 

  88. Andoh A, Bamba T, Sasaki M. Physiological and anti-inflammatory roles of dietary fiber and butyrate in intestinal functions. JPEN J Parenter Enteral Nutr. 1999;23(5 Suppl):S70–3. https://doi.org/10.1177/014860719902300518.

    Article  CAS  PubMed  Google Scholar 

  89. Leonel AJ, Alvarez-Leite JI. Butyrate: implications for intestinal function. Curr Opin Clin Nutr Metab Care. 2012;15(5):474–9. https://doi.org/10.1097/MCO.0b013e32835665fa.

    Article  CAS  PubMed  Google Scholar 

  90. Dominianni C, Sinha R, Goedert JJ, Pei Z, Yang L, Hayes RB, et al. Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLoS One. 2015;10(4):e0124599. https://doi.org/10.1371/journal.pone.0124599.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Holscher HD, Caporaso JG, Hooda S, Brulc JM, Fahey GC Jr, Swanson KS. Fiber supplementation influences phylogenetic structure and functional capacity of the human intestinal microbiome: follow-up of a randomized controlled trial. Am J Clin Nutr. 2015;101(1):55–64. https://doi.org/10.3945/ajcn.114.092064.

    Article  CAS  PubMed  Google Scholar 

  92. Vernazza CL, Gibson GR, Rastall RA. Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol. 2006;100(4):846–53. https://doi.org/10.1111/j.1365-2672.2006.02832.x.

    Article  CAS  PubMed  Google Scholar 

  93. Serino M, Luche E, Gres S, Baylac A, Bergé M, Cenac C, et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 2012;61(4):543–53. https://doi.org/10.1136/gutjnl-2011-301012.

    Article  CAS  PubMed  Google Scholar 

  94. Guinane CM, Cotter PD. Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Therap Adv Gastroenterol. 2013;6(4):295–308. https://doi.org/10.1177/1756283x13482996.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Caussy C, Tripathi A, Humphrey G, Bassirian S, Singh S, Faulkner C, et al. A gut microbiome signature for cirrhosis due to nonalcoholic fatty liver disease. Nat Commun. 2019;10(1):1406. https://doi.org/10.1038/s41467-019-09455-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Aron-Wisnewsky J, Clément K. The gut microbiome, diet, and links to cardiometabolic and chronic disorders. Nat Rev Nephrol. 2016;12(3):169–81. https://doi.org/10.1038/nrneph.2015.191.

    Article  CAS  PubMed  Google Scholar 

  97. Manichanh C, Borruel N, Casellas F, Guarner F. The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol. 2012;9(10):599–608. https://doi.org/10.1038/nrgastro.2012.152.

    Article  CAS  PubMed  Google Scholar 

  98. Ni J, Wu GD, Albenberg L, Tomov VT. Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol. 2017;14(10):573–84. https://doi.org/10.1038/nrgastro.2017.88.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Lennard-Jones JE. Classification of inflammatory bowel disease. Scand J Gastroenterol Suppl. 1989;170:2–6; discussion 16–9.

    Article  CAS  PubMed  Google Scholar 

  100. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3. https://doi.org/10.1038/nmeth.3869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104(34):13780–5. https://doi.org/10.1073/pnas.0706625104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Ohkusa T, Sato N, Ogihara T, Morita K, Ogawa M, Okayasu I. Fusobacterium varium localized in the colonic mucosa of patients with ulcerative colitis stimulates species-specific antibody. J Gastroenterol Hepatol. 2002;17(8):849–53.

    Article  PubMed  Google Scholar 

  103. Ohkusa T, Okayasu I, Ogihara T, Morita K, Ogawa M, Sato N. Induction of experimental ulcerative colitis by fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut. 2003;52(1):79–83. https://doi.org/10.1136/gut.52.1.79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Strauss J, Kaplan GG, Beck PL, Rioux K, Panaccione R, Devinney R, et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis. 2011;17(9):1971–8. https://doi.org/10.1002/ibd.21606.

    Article  PubMed  Google Scholar 

  105. Sokol H, Lepage P, Seksik P, Dore J, Marteau P. Temperature gradient gel electrophoresis of fecal 16S rRNA reveals active Escherichia coli in the microbiota of patients with ulcerative colitis. J Clin Microbiol. 2006;44(9):3172–7. https://doi.org/10.1128/JCM.02600-05.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Chassaing B, Darfeuille-Michaud A. The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology. 2011;140(6):1720–8. https://doi.org/10.1053/j.gastro.2011.01.054.

    Article  PubMed  Google Scholar 

  107. Feller M, Huwiler K, Stephan R, Altpeter E, Shang A, Furrer H, et al. Mycobacterium avium subspecies paratuberculosis and Crohn’s disease: a systematic review and meta-analysis. Lancet Infect Dis. 2007;7(9):607–13. https://doi.org/10.1016/S1473-3099(07)70211-6.

    Article  PubMed  Google Scholar 

  108. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010;139(6):1844–54.e1. https://doi.org/10.1053/j.gastro.2010.08.049.

  109. Li WJ, Guo Y, Zhang CY, Wu RY, Yang AY, Gaspar J, et al. Dietary phytochemicals and Cancer chemoprevention: a perspective on oxidative stress, inflammation, and epigenetics. Chem Res Toxicol. 2016;29(12):2071–95. https://doi.org/10.1021/acs.chemrestox.6b00413.

    Article  CAS  PubMed  Google Scholar 

  110. Khor TO, Kong ANT. Curcumin from turmeric spice, anti-inflammatory and antioxidant phytochemical, and cancer prevention. In: Kong ANT, editor. Inflammation, oxidative stress, and cancer: dietary approaches for cancer prevention. Boca Raton, FL: CRC Press; 2014. p. 343–54.

    Google Scholar 

  111. Tsai SJ, Yin MC. Antioxidative and anti-inflammatory protection of oleanolic acid and ursolic acid in PC12 cells. J Food Sci. 2008;73(7):H174–8. https://doi.org/10.1111/j.1750-3841.2008.00864.x.

    Article  CAS  PubMed  Google Scholar 

  112. Ou BX, Bosak KN, Brickner PR, Iezzoni DG, Seymour EM. Processed tart cherry products—comparative phytochemical content, in vitro antioxidant capacity and in vitro anti-inflammatory activity. J Food Sci. 2012;77(5):H105–12. https://doi.org/10.1111/j.1750-3841.2012.02681.x.

    Article  CAS  PubMed  Google Scholar 

  113. Olendzki BC, Silverstein TD, Persuitte GM, Ma YS, Baldwin KR, Cave D. An anti-inflammatory diet as treatment for inflammatory bowel disease: a case series report. Nutr J. 2014;13:5. https://doi.org/10.1186/1475-2891-13-5.

    Article  PubMed  PubMed Central  Google Scholar 

  114. Shivappa N, Steck SE, Hurley TG, Hussey JR, Hébert JR. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17(8):1689–96. https://doi.org/10.1017/S1368980013002115.

    Article  PubMed  Google Scholar 

  115. Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, et al. A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr. 2009;139(12):2365–72. https://doi.org/10.3945/jn.109.114025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. D’Argenio G, Mazzone G, Tuccillo C, Ribecco MT, Graziani G, Gravina AG, et al. Apple polyphenols extract (APE) improves colon damage in a rat model of colitis. Dig Liver Dis. 2012;44(7):555–62. https://doi.org/10.1016/j.dld.2012.01.009.

    Article  CAS  PubMed  Google Scholar 

  117. Sommer F, Rühlemann MC, Bang C, Höppner M, Rehman A, Kaleta C, et al. Microbiomarkers in inflammatory bowel diseases: caveats come with caviar. Gut. 2017;66(10):1734–8. https://doi.org/10.1136/gutjnl-2016-313678.

    Article  CAS  PubMed  Google Scholar 

  118. Axling U, Olsson C, Xu J, Fernandez C, Larsson S, Ström K, et al. Green tea powder and Lactobacillus plantarum affect gut microbiota, lipid metabolism and inflammation in high-fat fed C57BL/6J mice. Nutr Metab (Lond). 2012;9(1):105. https://doi.org/10.1186/1743-7075-9-105.

    Article  CAS  Google Scholar 

  119. Scaldaferri F, Lopetuso LR, Petito V, Cufino V, Bilotta M, Arena V, et al. Gelatin tannate ameliorates acute colitis in mice by reinforcing mucus layer and modulating gut microbiota composition: emerging role for ‘gut barrier protectors’ in IBD? United European Gastroenterol J. 2014;2(2):113–22. https://doi.org/10.1177/2050640614520867.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Lepage P, Häsler R, Spehlmann ME, Rehman A, Zvirbliene A, Begun A, et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology. 2011;141(1):227–36. https://doi.org/10.1053/j.gastro.2011.04.011.

    Article  PubMed  Google Scholar 

  121. Knights D, Silverberg MS, Weersma RK, Gevers D, Dijkstra G, Huang HL, et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med. 2014;6:107. https://doi.org/10.1186/s13073-014-0107-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Davis CD. Nutrigenomics and the prevention of colon cancer. Pharmacogenomics. 2007;8(2):121–4. https://doi.org/10.2217/14622416.8.2.121.

    Article  CAS  PubMed  Google Scholar 

  123. Riscuta G, Dumitrescu RG. Nutrigenomics: implications for breast and colon cancer prevention. Methods Mol Biol. 2012;863:343–58. https://doi.org/10.1007/978-1-61779-612-8_22.

    Article  CAS  PubMed  Google Scholar 

  124. Rustgi AK. The genetics of hereditary colon cancer. Genes Dev. 2007;21(20):2525–38. https://doi.org/10.1101/gad.1593107.

    Article  CAS  PubMed  Google Scholar 

  125. Watson AJ, Collins PD. Colon cancer: a civilization disorder. Dig Dis. 2011;29(2):222–8. https://doi.org/10.1159/000323926.

    Article  PubMed  Google Scholar 

  126. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–6. https://doi.org/10.1038/nature12506.

    Article  CAS  PubMed  Google Scholar 

  127. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105(43):16731–6. https://doi.org/10.1073/pnas.0804812105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Devillard E, McIntosh FM, Duncan SH, Wallace RJ. Metabolism of linoleic acid by human gut bacteria: different routes for biosynthesis of conjugated linoleic acid. J Bacteriol. 2007;189(6):2566–70. https://doi.org/10.1128/JB.01359-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe. 2014;15(3):317–28. https://doi.org/10.1016/j.chom.2014.02.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Wang TT, Cai GX, Qiu YP, Fei N, Zhang MH, Pang XY, et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 2012;6(2):320–9. https://doi.org/10.1038/ismej.2011.109.

    Article  CAS  PubMed  Google Scholar 

  131. Kundu P, Blacher E, Elinav E, Pettersson S. Our gut microbiome: the evolving inner self. Cell. 2017;171(7):1481–93. https://doi.org/10.1016/j.cell.2017.11.024.

    Article  CAS  PubMed  Google Scholar 

  132. Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, et al. Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology. 2004;127(1):80–93. https://doi.org/10.1053/j.gastro.2004.03.054.

    Article  CAS  PubMed  Google Scholar 

  133. Lu R, Wu SP, Zhang YG, Xia YL, Zhou ZR, Kato I, et al. Salmonella protein AvrA activates the STAT3 signaling pathway in colon cancer. Neoplasia. 2016;18(5):307–16. https://doi.org/10.1016/j.neo.2016.04.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Ye ZD, Petrof EO, Boone D, Claud EC, Sun J. Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol. 2007;171(3):882–92. https://doi.org/10.2353/ajpath.2007.070220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Shmuely H, Passaro D, Figer A, Niv Y, Pitlik S, Samra Z, et al. Relationship between Helicobacter pylori CagA status and colorectal cancer. Am J Gastroenterol. 2001;96(12):3406–10.

    Article  CAS  PubMed  Google Scholar 

  136. Breuer-Katschinski B, Nemes K, Marr A, Rump B, Leiendecker B, Breuer N, et al. Helicobacter pylori and the risk of colonic adenomas. Digestion. 1999;60(3):210–5. https://doi.org/10.1159/000007661.

    Article  CAS  PubMed  Google Scholar 

  137. Zumkeller N, Brenner H, Zwahlen M, Rothenbacher D. Helicobacter pylori infection and colorectal cancer risk: a meta-analysis. Helicobacter. 2006;11(2):75–80. https://doi.org/10.1111/j.1523-5378.2006.00381.x.

    Article  PubMed  Google Scholar 

  138. Njei BM, Ditah IC, Appiah J, Jinjuvadia R, Birk JW. Helicobacter pylori infection and the risk of colorectal cancer: a meta-analysis of epidemiologic evidence. J Clin Oncol. 2012;30(4_suppl):408. https://doi.org/10.1200/jco.2012.30.4_suppl.408.

    Article  Google Scholar 

  139. Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007;88(6):1354–64.

    Article  PubMed  Google Scholar 

  140. Gao ZG, Guo BM, Gao RY, Zhu QC, Qin HL. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol. 2015;6:20. https://doi.org/10.3389/fmicb.2015.00020.

    Article  PubMed  PubMed Central  Google Scholar 

  141. Wu N, Yang X, Zhang R, Li J, Xiao X, Hu Y, et al. Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol. 2013;66(2):462–70. https://doi.org/10.1007/s00248-013-0245-9.

    Article  CAS  PubMed  Google Scholar 

  142. Gao R, Kong C, Huang L, Li H, Qu X, Liu Z, et al. Mucosa-associated microbiota signature in colorectal cancer. Eur J Clin Microbiol. 2017;36(11):2073–83. https://doi.org/10.1007/s10096-017-3026-4.

    Article  CAS  Google Scholar 

  143. Zhu Q, Jin Z, Wu W, Gao R, Guo B, Gao Z, et al. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS One. 2014;9(3):e90849. https://doi.org/10.1371/journal.pone.0090849.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. McCoy AN, Araujo-Perez F, Azcarate-Peril A, Yeh JJ, Sandler RS, Keku TO. Fusobacterium is associated with colorectal adenomas. PLoS One. 2013;8(1):e53653. https://doi.org/10.1371/journal.pone.0053653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Ramirez CN, Li WJ, Zhang CY, Wu RY, Su S, Wang C, et al. In vitro-in vivo dose response of ursolic acid, sulforaphane, PEITC, and curcumin in cancer prevention. AAPS J. 2018;20(1):19. https://doi.org/10.1208/s12248-017-0177-2.

    Article  CAS  Google Scholar 

  146. Wang L, Li YL, Zhu LD, Yin R, Wang R, Luo XH, et al. Antitumor activities and immunomodulatory of rice bran polysaccharides and its sulfates in vitro. Int J Biol Macromol. 2016;88:424–32. https://doi.org/10.1016/j.ijbiomac.2016.04.016.

    Article  CAS  PubMed  Google Scholar 

  147. Florowska A, Krygier K, Florowski T, Dłużewska E. Prebiotics as functional food ingredients preventing diet-related diseases. Food Funct. 2016;7(5):2147–55. https://doi.org/10.1039/c5fo01459j.

    Article  CAS  PubMed  Google Scholar 

  148. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5(2):220–30. https://doi.org/10.1038/ismej.2010.118.

    Article  CAS  PubMed  Google Scholar 

  149. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63. https://doi.org/10.1038/nature12820.

    Article  CAS  PubMed  Google Scholar 

  150. Hervert-Hernández D, Pintado C, Rotger R, Goñi I. Stimulatory role of grape pomace polyphenols on Lactobacillus acidophilus growth. Int J Food Microbiol. 2009;136(1):119–22. https://doi.org/10.1016/j.ijfoodmicro.2009.09.016.

    Article  CAS  PubMed  Google Scholar 

  151. Puupponen-Pimiä R, Nohynek L, Hartmann-Schmidlin S, Kähkönen M, Heinonen M, Määttä-Riihinen K, et al. Berry phenolics selectively inhibit the growth of intestinal pathogens. J Appl Microbiol. 2005;98(4):991–1000. https://doi.org/10.1111/j.1365-2672.2005.02547.x.

    Article  CAS  PubMed  Google Scholar 

  152. Liu Z, Chen Z, Guo H, He D, Zhao H, Wang Z, et al. The modulatory effect of infusions of green tea, oolong tea, and black tea on gut microbiota in high-fat-induced obese mice. Food Funct. 2016;7(12):4869–79. https://doi.org/10.1039/c6fo01439a.

    Article  CAS  PubMed  Google Scholar 

  153. Tombola F, Campello S, De Luca L, Ruggiero P, Del Giudice G, Papini E, et al. Plant polyphenols inhibit VacA, a toxin secreted by the gastric pathogen Helicobacter pylori. FEBS Lett. 2003;543(1–3):184–9.

    Article  CAS  PubMed  Google Scholar 

  154. Burger O, Ofek I, Tabak M, Weiss EI, Sharon N, Neeman I. A high molecular mass constituent of cranberry juice inhibits Helicobacter pylori adhesion to human gastric mucus. FEMS Immunol Med Microbiol. 2000;29(4):295–301. https://doi.org/10.1111/j.1574-695X.2000.tb01537.x.

    Article  CAS  PubMed  Google Scholar 

  155. Chatterjee A, Yasmin T, Bagchi D, Stohs SJ. Inhibition of Helicobacter pylori in vitro by various berry extracts, with enhanced susceptibility to clarithromycin. Mol Cell Biochem. 2004;265(1–2):19–26.

    Article  CAS  PubMed  Google Scholar 

  156. Romero C, Medina E, Vargas J, Brenes M, De Castro A. In vitro activity of olive oil polyphenols against Helicobacter pylori. J Agric Food Chem. 2007;55(3):680–6. https://doi.org/10.1021/jf0630217.

    Article  CAS  PubMed  Google Scholar 

  157. 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(9):876–84. https://doi.org/10.1016/j.resmic.2006.07.004.

    Article  CAS  PubMed  Google Scholar 

  158. Maru GB, Hudlikar RR, Kumar G, Gandhi K, Mahimkar MB. Understanding the molecular mechanisms of cancer prevention by dietary phytochemicals: from experimental models to clinical trials. World J Biol Chem. 2016;7(1):88–99. https://doi.org/10.4331/wjbc.v7.i1.88.

    Article  PubMed  PubMed Central  Google Scholar 

  159. Poskitt EME. Defining childhood obesity: the relative body mass index (BMI). Acta Paediatr. 1995;84(8):961–3. https://doi.org/10.1111/j.1651-2227.1995.tb13806.x.

    Article  CAS  PubMed  Google Scholar 

  160. Razak F, Anand SS, Shannon H, Vuksan V, Davis B, Jacobs R, et al. Defining obesity cut points in a multiethnic population. Circulation. 2007;115(16):2111–8. https://doi.org/10.1161/Circulationaha.106.635011.

    Article  PubMed  Google Scholar 

  161. AMA adopts new policies on second day of voting at annual meeting. Press release of the American Medical Association. 2013. http://www.npr.org/documents/2013/jun/ama-resolution-obesity.pdf.

  162. Heymsfield SB, Wadden TA. Mechanisms, pathophysiology, and management of obesity. N Engl J Med. 2017;376(3):254–66.

    Article  CAS  PubMed  Google Scholar 

  163. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C. Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation. 2004;109(3):433–8. https://doi.org/10.1161/01.CIR.0000111245.75752.C6.

    Article  PubMed  Google Scholar 

  164. American Heart Association. What Is metabolic syndrome? 2015. https://www.heart.org/-/media/files/health-topics/answers-by-heart/what-is-metabolic-syndrome-300322.pdf?la=en&hash=3B60478685B71C2CD6CEB93782DAE8B7EAD33445.

  165. Xia Q, Grant SFA. The genetics of human obesity. Ann N Y Acad Sci. 2013;1281(1):178–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Conterno L, Fava F, Viola R, Tuohy KM. Obesity and the gut microbiota: does up-regulating colonic fermentation protect against obesity and metabolic disease? Genes Nutr. 2011;6(3):241–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555(7695):210–5. https://doi.org/10.1038/nature25973.

    Article  CAS  PubMed  Google Scholar 

  168. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9(5):313–23. https://doi.org/10.1038/nri2515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Gentile CL, Weir TL. The gut microbiota at the intersection of diet and human health. Science. 2018;362(6416):776–80. https://doi.org/10.1126/science.aau5812.

    Article  CAS  PubMed  Google Scholar 

  170. Chen X, Devaraj S. Gut microbiome in obesity, metabolic syndrome, and diabetes. Curr Diab Rep. 2018;18(12):129.

    Article  CAS  PubMed  Google Scholar 

  171. Kovatcheva-Datchary P, Arora T. Nutrition, the gut microbiome and the metabolic syndrome. Best Pract Res Clin Gastroenterol. 2013;27(1):59–72. https://doi.org/10.1016/j.bpg.2013.03.017.

    Article  CAS  PubMed  Google Scholar 

  172. Parekh PJ, Balart LA, Johnson DA. The influence of the gut microbiome on obesity, metabolic syndrome and gastrointestinal disease. Clin Transl Gastroenterol. 2015;6:e91. https://doi.org/10.1038/ctg.2015.16.

    Article  PubMed  PubMed Central  Google Scholar 

  173. Mazidi M, Rezaie P, Kengne AP, Mobarhan MG, Ferns GA. Gut microbiome and metabolic syndrome. Diabetes Metab Syndr. 2016;10(2 Suppl 1):S150–7. https://doi.org/10.1016/j.dsx.2016.01.024.

    Article  PubMed  Google Scholar 

  174. Ussar S, Fujisaka S, Kahn CR. Interactions between host genetics and gut microbiome in diabetes and metabolic syndrome. Mol Metab. 2016;5(9):795–803. https://doi.org/10.1016/j.molmet.2016.07.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101(44):15718–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102(31):11070–5. https://doi.org/10.1073/pnas.0504978102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31. https://doi.org/10.1038/nature05414.

    Article  PubMed  Google Scholar 

  178. Turnbaugh PJ, Bäckhed 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(4):213–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Erridge C, Bennett-Guerrero E, Poxton IR. Structure and function of lipopolysaccharides. Microbes Infect. 2002;4(8):837–51. https://doi.org/10.1016/S1286-4579(02)01604-0.

    Article  CAS  PubMed  Google Scholar 

  180. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761–72. https://doi.org/10.2337/db06-1491.

    Article  CAS  PubMed  Google Scholar 

  181. Beutler B, Rietschel ET. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol. 2003;3(2):169–76. https://doi.org/10.1038/nri1004.

    Article  CAS  PubMed  Google Scholar 

  182. Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 2010;4(2):232–41. https://doi.org/10.1038/ismej.2009.112.

    Article  CAS  PubMed  Google Scholar 

  183. de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol. 2010;299(2):G440–8. https://doi.org/10.1152/ajpgi.00098.2010.

    Article  CAS  Google Scholar 

  184. Sotos M, Nadal I, Marti A, Martínez A, Martin-Matillas M, Campoy C, et al. Gut microbes and obesity in adolescents. In: Proceedings of the 1st international immunonutrition workshop, Valencia, Spain, 3–5 October 2007. Cambridge: Cambridge University Press; 2008.

  185. Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 2014;159(3):514–29. https://doi.org/10.1016/j.cell.2014.09.048.

    Article  CAS  PubMed  Google Scholar 

  186. Thaiss CA, Levy M, Korem T, Dohnalová L, Shapiro H, Jaitin DA, et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell. 2016;167(6):1495–510.e12.

  187. 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(6):872–83. https://doi.org/10.1136/gutjnl-2014-307142.

    Article  CAS  PubMed  Google Scholar 

  188. Roopchand DE, Carmody RN, Kuhn P, Moskal K, Rojas-Silva P, Turnbaugh PJ, et al. Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet-induced metabolic syndrome. Diabetes. 2015;64(8):2847–58. https://doi.org/10.2337/db14-1916.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Kaakoush NO, Martire SI, Raipuria M, Mitchell HM, Nielsen S, Westbrook RF, et al. Alternating or continuous exposure to cafeteria diet leads to similar shifts in gut microbiota compared to chow diet. Mol Nutr Food Res. 2017;61(1):1500815. https://doi.org/10.1002/mnfr.201500815.

    Article  CAS  Google Scholar 

  190. Nagata N, Xu L, Kohno S, Ushida Y, Aoki Y, Umeda R, et al. Glucoraphanin ameliorates obesity and insulin resistance through adipose tissue browning and reduction of metabolic endotoxemia in mice. Diabetes. 2017;66(5):1222–36. https://doi.org/10.2337/db16-0662.

    Article  CAS  PubMed  Google Scholar 

  191. Chang CJ, Lin CS, Lu CC, Martel J, Ko YF, Ojcius DM, et al. Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat Commun. 2015;6:7489. https://doi.org/10.1038/ncomms8489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all members of Dr. Ah-Ng Kong’s lab for the helpful discussions and preparation of the manuscript.

Funding

This review was supported by R01 CA200129 from the National Cancer Institute (NCI) and R01 AT009152 from the National Center for Complementary and Integrative Health (NCCIH) of the National Institutes of Health (NIH) to Dr. Ah-Ng Tony Kong.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ah-Ng Kong.

Ethics declarations

Conflict of Interest

The authors declare no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Microbiome

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yin, R., Kuo, HC., Hudlikar, R. et al. Gut Microbiota, Dietary Phytochemicals, and Benefits to Human Health. Curr Pharmacol Rep 5, 332–344 (2019). https://doi.org/10.1007/s40495-019-00196-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40495-019-00196-3

Keywords

Navigation