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Current Nutrition Reports

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Open Access 01-12-2019 | Obesity | Diabetes and Obesity (CB Chan, Section Editor)

Targeting Carbohydrates and Polyphenols for a Healthy Microbiome and Healthy Weight

Authors: Matthias Van Hul, Patrice D. Cani

Published in: Current Nutrition Reports | Issue 4/2019

Abstract

Purpose of Review

In this review, we focus on microbiota modulation using non-digestible carbohydrate and polyphenols (i.e., prebiotics) that have the potential to modulate body weight.

Recent Findings

Prebiotics derived from plants have gained the interest of public and scientific communities as they may prevent diseases and help maintain health.

Summary

Maintaining a healthy body weight is key to reducing the risk of developing chronic metabolic complications. However, the prevalence of obesity has increased to pandemic proportions and is now ranked globally in the top five risk factors for death. While diet and behavioral modification programs aiming to reduce weight gain and promote weight loss are effective in the short term, they remain insufficient over the long haul as compliance is often low and weight regain is very common. As a result, novel dietary strategies targeting the gut microbiota have been successful in decreasing obesity and metabolic disorders via different molecular mechanisms.

NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet. 2017;390(10113):2627–42. https://doi.org/10.1016/S0140-6736(17)32129-3.CrossRef

Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the global burden of disease study 2013. Lancet. 2014;384(9945):766–81. https://doi.org/10.1016/S0140-6736(14)60460-8.CrossRefPubMedPubMedCentral

Masoodi M, Kuda O, Rossmeisl M, Flachs P, Kopecky J. Lipid signaling in adipose tissue: connecting inflammation & metabolism. Biochim Biophys Acta. 2015;1851(4):503–18. https://doi.org/10.1016/j.bbalip.2014.09.023.CrossRefPubMed

Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121):860–7.CrossRefPubMed

Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol. 2010;314(1):1–16. https://doi.org/10.1016/j.mce.2009.07.031.CrossRefPubMed

Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67(9):1716–25. https://doi.org/10.1136/gutjnl-2018-316723.CrossRefPubMed

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.CrossRefPubMed

Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–3.CrossRefPubMed

Khan MJ, Gerasimidis K, Edwards CA, Shaikh MG. Role of gut microbiota in the aetiology of obesity: proposed mechanisms and review of the literature. J Obes. 2016;2016:7353642. https://doi.org/10.1155/2016/7353642.CrossRefPubMedPubMedCentral

10.

Knox NC, Forbes JD, Van Domselaar G, Bernstein CN. The gut microbiome as a target for IBD treatment: are we there yet? Curr Treat Options Gastroenterol. 2019;17:115–26. https://doi.org/10.1007/s11938-019-00221-w.CrossRefPubMed

11.

Zuo T, Ng SC. The gut microbiota in the pathogenesis and therapeutics of inflammatory bowel disease. Front Microbiol. 2018;9:2247. https://doi.org/10.3389/fmicb.2018.02247.CrossRefPubMedPubMedCentral

12.

Maeda Y, Takeda K. Role of gut microbiota in rheumatoid arthritis. J Clin Med. 2017;6(6). https://doi.org/10.3390/jcm6060060.CrossRefPubMedCentral

13.

Lynch SV, Boushey HA. The microbiome and development of allergic disease. Curr Opin Allergy Clin Immunol. 2016;16(2):165–71. https://doi.org/10.1097/ACI.0000000000000255.CrossRefPubMedPubMedCentral

14.

Wang Y, Kasper LH. The role of microbiome in central nervous system disorders. Brain Behav Immun. 2014;38:1–12. https://doi.org/10.1016/j.bbi.2013.12.015.CrossRefPubMed

15.

Trowell HC. Dietary-fiber hypothesis of the etiology of diabetes mellitus. Diabetes. 1975;24(8):762–5.CrossRefPubMed

16.

Jenkins DJ, Goff DV, Leeds AR, Alberti KG, Wolever TM, Gassull MA, et al. Unabsorbable carbohydrates and diabetes: decreased post-prandial hyperglycaemia. Lancet. 1976;2(7978):172–4.CrossRefPubMed

17.

Jenkins DJ, Wolever TM, Hockaday TD, Leeds AR, Howarth R, Bacon S, et al. Treatment of diabetes with guar gum. Reduction of urinary glucose loss in diabetics. Lancet. 1977;2(8042):779–80.CrossRefPubMed

18.

Jenkins DJ, Wolever TM, Leeds AR, Gassull MA, Haisman P, Dilawari J, et al. Dietary fibres, fibre analogues, and glucose tolerance: importance of viscosity. Br Med J. 1978;1(6124):1392–4.CrossRefPubMedPubMedCentral

19.

Cani PD, Jordan BF. Gut microbiota-mediated inflammation in obesity: a link with gastrointestinal cancer. Nat Rev Gastroenterol Hepatol. 2018;15(11):671–82. https://doi.org/10.1038/s41575-018-0025-6.CrossRefPubMed

20.

Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol. 2017;19(1):29–41. https://doi.org/10.1111/1462-2920.13589.CrossRefPubMed

21.

Chambers ES, Preston T, Frost G, Morrison DJ. Role of gut microbiota-generated short-chain fatty acids in metabolic and cardiovascular health. Curr Nutr Rep. 2018;7(4):198–206. https://doi.org/10.1007/s13668-018-0248-8.CrossRefPubMedPubMedCentral

22.

Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun. 2014;5:3611. https://doi.org/10.1038/ncomms4611.CrossRefPubMed

23.

Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11(10):577–91. https://doi.org/10.1038/nrendo.2015.128.CrossRefPubMed

24.

Daubioul CA, Taper HS, De Wispelaere LD, Delzenne NM. Dietary oligofructose lessens hepatic steatosis, but does not prevent hypertriglyceridemia in obese zucker rats. JNutr. 2000;130(5):1314–9.

25.

Cani PD, Dewever C, Delzenne NM. Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr. 2004;92(3):521–6.CrossRefPubMed

26.

Cani PD, Neyrinck AM, Maton N, Delzenne NM. Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like peptide-1. Obes Res. 2005;13(6):1000–7.CrossRefPubMed

27.

Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, Burcelin R. Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes. 2006;55(5):1484–90.CrossRefPubMed

28.

Delzenne NM, Cani PD, Daubioul C, Neyrinck AM. Impact of inulin and oligofructose on gastrointestinal peptides. BrJNutr. 2005;93(Suppl 1):S157–S61.

29.

Drucker DJ. Mechanisms of action and therapeutic application of glucagon-like peptide-1. Cell Metab. 2018;27(4):740–56. https://doi.org/10.1016/j.cmet.2018.03.001.CrossRefPubMed

30.

Wang X, Gibson GR. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol. 1993;75(4):373–80.CrossRefPubMed

31.

Aziz AA, Kenney LS, Goulet B, Abdel-Aal E. Dietary starch type affects body weight and glycemic control in freely fed but not energy-restricted obese rats. J Nutr. 2009;139(10):1881–9.CrossRefPubMed

32.

Keenan MJ, Zhou J, McCutcheon KL, Raggio AM, Bateman HG, Todd E, et al. Effects of resistant starch, a non-digestible fermentable fiber, on reducing body fat. Obesity(SilverSpring). 2006;14(9):1523–34.

33.

Zhou J, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Shen L, et al. Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab. 2008;295(5):E1160–E6.CrossRefPubMedPubMedCentral

34.

Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A. 2008;105(43):16767–72.CrossRefPubMedPubMedCentral

35.

Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 2012;61(2):364–71.CrossRefPubMedPubMedCentral

36.

Nohr MK, Pedersen MH, Gille A, Egerod KL, Engelstoft MS, Husted AS, et al. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology. 2013;154(10):3552–64. https://doi.org/10.1210/en.2013-1142.CrossRefPubMed

37.

Brooks L, Viardot A, Tsakmaki A, Stolarczyk E, Howard JK, Cani PD, et al. Fermentable carbohydrate stimulates FFAR2-dependent colonic PYY cell expansion to increase satiety. Mol Metab. 2017;6(1):48–60. https://doi.org/10.1016/j.molmet.2016.10.011.CrossRefPubMed

38.

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(3):424–9. https://doi.org/10.1038/ijo.2014.153.CrossRef

39.

• Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–45. https://doi.org/10.1016/j.cell.2016.05.041. An excellent review exploring how the gut bacteria are producing SCFAs and how they contribute to host metabolism. CrossRefPubMed

40.

Cani PD, Joly E, Horsmans Y, Delzenne NM. Oligofructose promotes satiety in healthy human: a pilot study. Eur J Clin Nutr. 2006;60(5):567–72.CrossRefPubMed

41.

Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, Naslain D, et al. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr. 2009;90(5):1236–43.CrossRefPubMed

42.

Parnell JA, Reimer RA. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr. 2009;89(6):1751–9.CrossRefPubMed

43.

Peters HP, Boers HM, Haddeman E, Melnikov SM, Qvyjt F. No effect of added beta-glucan or of fructooligosaccharide on appetite or energy intake. Am J Clin Nutr. 2009;89(1):58–63.CrossRefPubMed

44.

Tarini J, Wolever TM. The fermentable fibre inulin increases postprandial serum short-chain fatty acids and reduces free-fatty acids and ghrelin in healthy subjects. Appl Physiol Nutr Metab. 2010;35(1):9–16.CrossRefPubMed

45.

Klosterbuer AS, Thomas W, Slavin JL. Resistant starch and pullulan reduce postprandial glucose, insulin, and GLP-1, but have no effect on satiety in healthy humans. J Agric Food Chem. 2012;60(48):11928–34. https://doi.org/10.1021/jf303083r.CrossRefPubMed

46.

Frost G, Brynes A, Leeds A. Effect of large bowel fermentation on insulin, glucose, free fatty acids, and glucagon-like peptide 1 (7-36) amide in patients with coronary heart disease. Nutrition. 1999;15(3):183–8.CrossRefPubMed

47.

Bird AR, Conlon MA, Christophersen CT, Topping DL. Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Benefic Microbes. 2010;1(4):423–31. https://doi.org/10.3920/BM2010.0041.CrossRef

48.

Robertson MD. Dietary-resistant starch and glucose metabolism. Curr Opin Clin Nutr Metab Care. 2012;15(4):362–7. https://doi.org/10.1097/MCO.0b013e3283536931.CrossRefPubMed

49.

Nilsson A, Johansson E, Ekstrom L, Bjorck I. Effects of a brown beans evening meal on metabolic risk markers and appetite regulating hormones at a subsequent standardized breakfast: a randomized cross-over study. PLoS One. 2013;8(4):e59985. https://doi.org/10.1371/journal.pone.0059985.CrossRefPubMedPubMedCentral

50.

Daud NM, Ismail NA, Thomas EL, Fitzpatrick JA, Bell JD, Swann JR, et al. The impact of oligofructose on stimulation of gut hormones, appetite regulation and adiposity. Obesity (Silver Spring). 2014;22(6):1430–8. https://doi.org/10.1002/oby.20754.CrossRef

51.

Korczak R, Slavin JL. Fructooligosaccharides and appetite. Curr Opin Clin Nutr Metab Care. 2018;21(5):377–80. https://doi.org/10.1097/MCO.0000000000000502.CrossRefPubMed

52.

•• Zhao L, Zhang F, Ding X, Wu G, Lam YY, Wang X, et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science. 2018;359(6380):1151–6. https://doi.org/10.1126/science.aao5774. An outstanding example of investigation in humans showing how the modification of the source of carbohydrates and polyphenols can positively affect the host metabolism and their link with both the gut microbiota composition and the metabolites produced.CrossRefPubMed

53.

Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125(6):1401–12. https://doi.org/10.1093/jn/125.6.1401.CrossRefPubMed

54.

Carlson JL, Erickson JM, Lloyd BB, Slavin JL. Health effects and sources of prebiotic dietary fiber. Curr Dev Nutr. 2018;2(3):nzy005. https://doi.org/10.1093/cdn/nzy005.CrossRefPubMedPubMedCentral

55.

•• Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491–502. https://doi.org/10.1038/nrgastro.2017.75. In this statement, a panel of experts discuss the term and scope of “prebiotics” in order to define a consensus characterisation that is uniformly applicable in research, marketing and regulation. They also review several aspects of prebiotic science including its development, health benefits and legislation. CrossRefPubMed

56.

Tsao R. Chemistry and biochemistry of dietary polyphenols. Nutrients. 2010;2(12):1231–46. https://doi.org/10.3390/nu2121231.CrossRefPubMedPubMedCentral

57.

Neveu V, Perez-Jimenez J, Vos F, Crespy V, du Chaffaut L, Mennen L, et al. Phenol-explorer: an online comprehensive database on polyphenol contents in foods. Database (Oxford). 2010;2010:bap024. https://doi.org/10.1093/database/bap024.CrossRef

58.

Cory H, Passarelli S, Szeto J, Tamez M, Mattei J. The role of polyphenols in human health and food systems: a mini-review. Front Nutr. 2018;5:87. https://doi.org/10.3389/fnut.2018.00087.CrossRefPubMedPubMedCentral

59.

Singh A, Holvoet S, Mercenier A. Dietary polyphenols in the prevention and treatment of allergic diseases. Clin Exp Allergy. 2011;41(10):1346–59. https://doi.org/10.1111/j.1365-2222.2011.03773.x.CrossRefPubMed

60.

Wang S, Moustaid-Moussa N, Chen L, Mo H, Shastri A, Su R, et al. Novel insights of dietary polyphenols and obesity. J Nutr Biochem. 2014;25(1):1–18. https://doi.org/10.1016/j.jnutbio.2013.09.001.CrossRefPubMedPubMedCentral

61.

• Yang CS, Zhang J, Zhang L, Huang J, Wang Y. Mechanisms of body weight reduction and metabolic syndrome alleviation by tea. Mol Nutr Food Res. 2016;60(1):160–74. https://doi.org/10.1002/mnfr.201500428. In this publication, Yang et al introduce their so-called “AMPK hypothesis” in which polyphenols are suggested to activate AMP-activated protein kinase (AMPK) by phosphorylation, thereby modulating some proteins involved in adipogenesis, lipogenesis, and lipolysis. CrossRefPubMed

62.

Hiroki T, Monira P, Shingo G, Mamoru I, Yoriyuki N. Beneficial effects of plant polyphenols on obesity. Obes Control Ther. 2017;4(3):1–16. https://doi.org/10.15226/2374-8354/4/3/00142.CrossRef

63.

Meydani M, Hasan ST. Dietary polyphenols and obesity. Nutrients. 2010;2(7):737–51. https://doi.org/10.3390/nu2070737.CrossRefPubMedPubMedCentral

64.

Springer M, Moco S. Resveratrol and its human metabolites-effects on metabolic health and obesity. Nutrients. 2019;11(1). https://doi.org/10.3390/nu11010143.CrossRefPubMedCentral

65.

• Chiva-Blanch G, Badimon L. Effects of polyphenol intake on metabolic syndrome: current evidences from human trials. Oxidative Med Cell Longev. 2017;2017:5812401. https://doi.org/10.1155/2017/5812401. Overview of the human interventional trials investigating the effects of polyphenols in patients with metabolic syndrome, suggesting that the protective effects of polyphenols may be reached through a long-term regular, daily consumption. CrossRef

66.

Guo X, Tresserra-Rimbau A, Estruch R, Martínez-González MA, Medina-Remón A, Fitó M, Corella D, et al. Polyphenol levels are inversely correlated with body weight and obesity in an elderly population after 5 years of follow up (The Randomised PREDIMED Study). Nutrients. 2017;9(5):E452. https://doi.org/10.3390/nu9050452.CrossRefPubMedCentral

67.

Rothenberg DO, Zhou C, Zhang L. A review on the weight-loss effects of oxidized tea polyphenols. Molecules. 2018;23(5):E1176. https://doi.org/10.3390/molecules23051176.CrossRefPubMedCentral

68.

Vazquez Cisneros LC, Lopez-Uriarte P, Lopez-Espinoza A, Navarro Meza M, Espinoza-Gallardo AC, Guzman Aburto MB. Effects of green tea and its epigallocatechin (EGCG) content on body weight and fat mass in humans: a systematic review. Nutr Hosp. 2017;34(3):731–7. https://doi.org/10.20960/nh.753.CrossRefPubMed

69.

Rains TM, Agarwal S, Maki KC. Antiobesity effects of green tea catechins: a mechanistic review. J Nutr Biochem. 2011;22(1):1–7. https://doi.org/10.1016/j.jnutbio.2010.06.006.CrossRefPubMed

70.

Miyatake N, Sakano N, Numata T. Comparison of coffee, tea and green tea consumption between Japanese with and without metabolic syndrome in a cross-sectional study. Open J Epidemiol. 2012;2:44–9. https://doi.org/10.4236/ojepi.2012.22007.CrossRef

71.

Zhang B, Deng Z, Ramdath DD, Tang Y, Chen PX, Liu R, et al. Phenolic profiles of 20 Canadian lentil cultivars and their contribution to antioxidant activity and inhibitory effects on alpha-glucosidase and pancreatic lipase. Food Chem. 2015;172:862–72. https://doi.org/10.1016/j.foodchem.2014.09.144.CrossRefPubMed

72.

Yamagata K, Tagami M, Yamori Y. Dietary polyphenols regulate endothelial function and prevent cardiovascular disease. Nutrition. 2015;31(1):28–37. https://doi.org/10.1016/j.nut.2014.04.011.CrossRefPubMed

73.

Xiao JB, Hogger P. Dietary polyphenols and type 2 diabetes: current insights and future perspectives. Curr Med Chem. 2015;22(1):23–38.CrossRefPubMed

74.

Wang S, Sun Z, Dong S, Liu Y, Liu Y. Molecular interactions between (−)-epigallocatechin gallate analogs and pancreatic lipase. PLoS One. 2014;9(11):e111143. https://doi.org/10.1371/journal.pone.0111143.CrossRefPubMedPubMedCentral

75.

Jakobek L. Interactions of polyphenols with carbohydrates, lipids and proteins. Food Chem. 2015;175:556–67. https://doi.org/10.1016/j.foodchem.2014.12.013.CrossRefPubMed

76.

Barrett AH, Farhadi NF, Smith TJ. Slowing starch digestion and inhibiting digestive enzyme activity using plant flavanols/tannins— a review of efficacy and mechanisms. LWT. 2018;87:394–9. https://doi.org/10.1016/j.lwt.2017.09.002.CrossRef

77.

Huang J, Wang Y, Xie Z, Zhou Y, Zhang Y, Wan X. The anti-obesity effects of green tea in human intervention and basic molecular studies. Eur J Clin Nutr. 2014;68(10):1075–87. https://doi.org/10.1038/ejcn.2014.143.CrossRefPubMed

78.

Pan MH, Tung YC, Yang G, Li S, Ho CT. Molecular mechanisms of the anti-obesity effect of bioactive compounds in tea and coffee. Food Funct. 2016;7(11):4481–91. https://doi.org/10.1039/c6fo01168c.CrossRefPubMed

79.

Rocha A, Bolin AP, Cardoso CA, Otton R. Green tea extract activates AMPK and ameliorates white adipose tissue metabolic dysfunction induced by obesity. Eur J Nutr. 2016;55(7):2231–44. https://doi.org/10.1007/s00394-015-1033-8.CrossRefPubMed

80.

Garcia D, Shaw RJ. AMPK: mechanisms of cellular energy sensing and restoration of metabolic balance. Mol Cell. 2017;66(6):789–800. https://doi.org/10.1016/j.molcel.2017.05.032.CrossRefPubMedPubMedCentral

81.

Yang CS, Wang H, Sheridan ZP. Studies on prevention of obesity, metabolic syndrome, diabetes, cardiovascular diseases and cancer by tea. J Food Drug Anal. 2018;26(1):1–13. https://doi.org/10.1016/j.jfda.2017.10.010.CrossRefPubMed

82.

Williamson G, Manach C. Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am J Clin Nutr. 2005;81(1 Suppl):243S–55S. https://doi.org/10.1093/ajcn/81.1.243S.CrossRefPubMed

83.

Hervert-Hernandez D, Pintado C, Rotger R, Goni 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.CrossRefPubMed

84.

Masumoto S, Terao A, Yamamoto Y, Mukai T, Miura T, Shoji T. Non-absorbable apple procyanidins prevent obesity associated with gut microbial and metabolomic changes. Sci Rep. 2016;6:31208. https://doi.org/10.1038/srep31208.CrossRefPubMedPubMedCentral

85.

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.CrossRefPubMedPubMedCentral

86.

Cardona F, Andres-Lacueva C, Tulipani S, Tinahones FJ, Queipo-Ortuno MI. Benefits of polyphenols on gut microbiota and implications in human health. J Nutr Biochem. 2013;24(8):1415–22. https://doi.org/10.1016/j.jnutbio.2013.05.001.CrossRefPubMed

87.

Duda-Chodak A, Tarko T, Satora P, Sroka P. Interaction of dietary compounds, especially polyphenols, with the intestinal microbiota: a review. Eur J Nutr. 2015;54(3):325–41. https://doi.org/10.1007/s00394-015-0852-y.CrossRefPubMedPubMedCentral

88.

Etxeberria U, Fernandez-Quintela A, Milagro FI, Aguirre L, Martinez 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.CrossRefPubMed

89.

Marin L, Miguelez EM, Villar CJ, Lombo F. Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed Res Int. 2015;2015:905215. https://doi.org/10.1155/2015/905215.CrossRefPubMedPubMedCentral

90.

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.CrossRefPubMed

91.

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

92.

Bustos I, Garcia-Cayuela T, Hernandez-Ledesma B, Pelaez C, Requena T, Martinez-Cuesta MC. Effect of flavan-3-ols on the adhesion of potential probiotic lactobacilli to intestinal cells. J Agric Food Chem. 2012;60(36):9082–8. https://doi.org/10.1021/jf301133g.CrossRefPubMed

93.

Celebioglu HU, Svensson B. Dietary nutrients, proteomes, and adhesion of probiotic lactobacilli to mucin and host epithelial cells. Microorganisms. 2018;6(3):E90. https://doi.org/10.3390/microorganisms6030090.CrossRefPubMedCentral

94.

Kailasapathy K, Chin J. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol. 2000;78(1):80–8. https://doi.org/10.1046/j.1440-1711.2000.00886.x.CrossRefPubMed

95.

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

96.

Luca SV, Macovei I, Bujor A, Miron A, Skalicka-Wozniak K, Aprotosoaie AC, et al. Bioactivity of dietary polyphenols: the role of metabolites. Crit Rev Food Sci Nutr. 2019:1–34. https://doi.org/10.1080/10408398.2018.1546669.

97.

Del Rio D, Rodriguez-Mateos A, Spencer JP, Tognolini M, Borges G, Crozier A. Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal. 2013;18(14):1818–92. https://doi.org/10.1089/ars.2012.4581.CrossRefPubMedPubMedCentral

98.

Filosa S, Di Meo F, Crispi S. Polyphenols-gut microbiota interplay and brain neuromodulation. Neural Regen Res. 2018;13(12):2055–9. https://doi.org/10.4103/1673-5374.241429.CrossRefPubMedPubMedCentral

99.

• Ozdal T, Sela DA, Xiao J, Boyacioglu D, Chen F, Capanoglu E. The reciprocal interactions between polyphenols and gut microbiota and effects on bioaccessibility. Nutrients. 2016;8(2):78. https://doi.org/10.3390/nu8020078. Review summarizing how polyphenols are metabolized by the gut microbiota and how the gut microbiota is modulated by polyphenols. CrossRefPubMedPubMedCentral

100.

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.CrossRefPubMed

101.

Aprikian O, Duclos V, Guyot S, Besson C, Manach C, Bernalier A, et al. Apple pectin and a polyphenol-rich apple concentrate are more effective together than separately on cecal fermentations and plasma lipids in rats. J Nutr. 2003;133(6):1860–5. https://doi.org/10.1093/jn/133.6.1860.CrossRefPubMed

102.

Zdunczyk Z, Juskiewicz J, Estrella I. Cecal parameters of rats fed diets containing grapefruit polyphenols and inulin as single supplements or in a combination. Nutrition. 2006;22(9):898–904. https://doi.org/10.1016/j.nut.2006.05.010.CrossRefPubMed

103.

Sadeghi Ekbatan S, Sleno L, Sabally K, Khairallah J, Azadi B, Rodes L, et al. Biotransformation of polyphenols in a dynamic multistage gastrointestinal model. Food Chem. 2016;204:453–62. https://doi.org/10.1016/j.foodchem.2016.02.140.CrossRefPubMed

104.

Fotschki B, Juskiewicz J, Jurgonski A, Kolodziejczyk K, Milala J, Kosmala M, et al. Anthocyanins in strawberry polyphenolic extract enhance the beneficial effects of diets with fructooligosaccharides in the rat cecal environment. PLoS One. 2016;11(2):e0149081. https://doi.org/10.1371/journal.pone.0149081.CrossRefPubMedPubMedCentral

105.

Kawabata K, Kato Y, Sakano T, Baba N, Hagiwara K, Tamura A, et al. Effects of phytochemicals on in vitro anti-inflammatory activity of Bifidobacterium adolescentis. Biosci Biotechnol Biochem. 2015;79(5):799–807. https://doi.org/10.1080/09168451.2015.1006566.CrossRefPubMed

106.

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. https://doi.org/10.1021/jf901931b.CrossRefPubMed

107.

Puupponen-Pimia R, Nohynek L, Hartmann-Schmidlin S, Kahkonen M, Heinonen M, Maatta-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.CrossRefPubMed

108.

Taguri T, Tanaka T, Kouno I. Antimicrobial activity of 10 different plant polyphenols against bacteria causing food-borne disease. Biol Pharm Bull. 2004;27(12):1965–9.CrossRefPubMed

109.

Espin JC, Gonzalez-Sarrias A, Tomas-Barberan FA. The gut microbiota: a key factor in the therapeutic effects of (poly)phenols. Biochem Pharmacol. 2017;139:82–93. https://doi.org/10.1016/j.bcp.2017.04.033.CrossRefPubMed

110.

Van Hul M, Geurts L, Plovier H, Druart C, Everard A, Stahlman M, et al. Reduced obesity, diabetes, and steatosis upon cinnamon and grape pomace are associated with changes in gut microbiota and markers of gut barrier. Am J Physiol Endocrinol Metab. 2018;314(4):E334-E52. https://doi.org/10.1152/ajpendo.00107.2017.CrossRef

111.

Anhe FF, Roy D, Pilon G, Dudonne 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.CrossRefPubMed

112.

•• Anhê FF, Nachbar RT, Varin TV, Trot tier J, Dudonné S, Le Barz M, et al. Treatment with camu camu (Myrciaria dubia) prevents obesity by altering the gut microbiota and increasing energy expenditure in diet-induced obese mice. Gut. 2018;68:453–64:gutjnl-2017-315565. https://doi.org/10.1136/gutjnl-2017-315565. Key example of a study in mice that shows how polyphenols (an extract from Camu camu in this case) causally prevent obesity and metabolic disease and exert its positive effects, at least in part, through the modulation of the gut microbiota (here: a blooming ofA. muciniphilaand a significant reduction inLactobacillusbacteria). CrossRefPubMed

113.

Jiao X, Wang Y, Lin Y, Lang Y, Li E, Zhang X, et al. Blueberry polyphenols extract as a potential prebiotic with anti-obesity effects on C57BL/6 J mice by modulating the gut microbiota. J Nutr Biochem. 2019;64:88–100. https://doi.org/10.1016/j.jnutbio.2018.07.008.CrossRefPubMed

114.

Wang P, Li D, Ke W, Liang D, Hu X, Chen F. Resveratrol-induced gut microbiota reduces obesity in high-fat diet-fed mice. Int J Obes (Lond). 2019. https://doi.org/10.1038/s41366-019-0332-1.

115.

Janssens PL, Penders J, Hursel R, Budding AE, Savelkoul PH, Westerterp-Plantenga MS. Long-term green tea supplementation does not change the human gut microbiota. PLoS One. 2016;11(4):e0153134. https://doi.org/10.1371/journal.pone.0153134.CrossRefPubMedPubMedCentral

116.

Cani PD, de Vos WM. Next-generation beneficial microbes: the case of Akkermansia muciniphila. Front Microbiol. 2017;8:1765. https://doi.org/10.3389/fmicb.2017.01765.CrossRefPubMedPubMedCentral

117.

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 United States of America. 2013;110(22):9066–71. https://doi.org/10.1073/pnas.1219451110.CrossRef

118.

Plovier H, Cani PD. Microbial impact on host metabolism: opportunities for novel treatments of nutritional disorders? Microbiol Spectr. 2017;5(3):1–13. https://doi.org/10.1128/microbiolspec.BAD-0002-2016.CrossRef

119.

Pierre JF, Heneghan AF, Feliciano RP, Shanmuganayagam D, Roenneburg DA, Krueger CG, et al. Cranberry proanthocyanidins improve the gut mucous layer morphology and function in mice receiving elemental enteral nutrition. JPEN J Parenter Enteral Nutr. 2013;37(3):401–9. https://doi.org/10.1177/0148607112463076.CrossRefPubMed

120.

Baldwin J, Collins B, Wolf PG, Martinez K, Shen W, Chuang CC, et al. Table grape consumption reduces adiposity and markers of hepatic lipogenesis and alters gut microbiota in butter fat-fed mice. J Nutr Biochem. 2016;27:123–35. https://doi.org/10.1016/j.jnutbio.2015.08.027.CrossRefPubMed

121.

Anhe FF, Pilon G, Roy D, Desjardins Y, Levy E, Marette A. Triggering Akkermansia with dietary polyphenols: a new weapon to combat the metabolic syndrome? Gut Microbes. 2016;7(2):146–53. https://doi.org/10.1080/19490976.2016.1142036.CrossRefPubMedPubMedCentral

122.

Etxeberria U, Arias N, Boque 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(6):651–60. https://doi.org/10.1016/j.jnutbio.2015.01.002.CrossRefPubMed

123.

Li Z, Henning SM, Lee RP, Lu QY, Summanen PH, Thames G, et al. Pomegranate extract induces ellagitannin metabolite formation and changes stool microbiota in healthy volunteers. Food Funct. 2015;6(8):2487–95. https://doi.org/10.1039/c5fo00669d.CrossRefPubMed

124.

Anhe FF, Varin TV, Le Barz M, Pilon G, Dudonne S, Trottier J, et al. Arctic berry extracts target the gut-liver axis to alleviate metabolic endotoxaemia, insulin resistance and hepatic steatosis in diet-induced obese mice. Diabetologia. 2018;61(4):919–31. https://doi.org/10.1007/s00125-017-4520-z.CrossRefPubMed

125.

Renard CMGC, Watrelot AA, Le Bourvellec C. Interactions between polyphenols and polysaccharides: mechanisms and consequences in food processing and digestion. Trends Food Sci Technol. 2017;60:43–51. https://doi.org/10.1016/j.tifs.2016.10.022.CrossRef

126.

Edwards CA, Havlik J, Cong W, Mullen W, Preston T, Morrison DJ, et al. Polyphenols and health: interactions between fibre, plant polyphenols and the gut microbiota. Nutr Bull. 2017;42(4):356–60. https://doi.org/10.1111/nbu.12296.CrossRefPubMedPubMedCentral

127.

Crowe KM, Francis C. Academy of N, Dietetics. Position of the academy of nutrition and dietetics: functional foods. J Acad Nutr Diet. 2013;113(8):1096–103. https://doi.org/10.1016/j.jand.2013.06.002.CrossRefPubMed

128.

Williamson G, Holst B. Dietary reference intake (DRI) value for dietary polyphenols: are we heading in the right direction? Br J Nutr. 2008;99(Suppl 3):S55–8. https://doi.org/10.1017/S0007114508006867.CrossRefPubMed

129.

Murase T, Haramizu S, Shimotoyodome A, Tokimitsu I. Reduction of diet-induced obesity by a combination of tea-catechin intake and regular swimming. Int J Obes. 2006;30(3):561–8. https://doi.org/10.1038/sj.ijo.0803135.CrossRef

130.

Shimotoyodome A, Haramizu S, Inaba M, Murase T, Tokimitsu I. Exercise and green tea extract stimulate fat oxidation and prevent obesity in mice. Med Sci Sports Exerc. 2005;37(11):1884–92.CrossRefPubMed

131.

Lorenz M, Paul F, Moobed M, Baumann G, Zimmermann BF, Stangl K, et al. The activity of catechol-O-methyltransferase (COMT) is not impaired by high doses of epigallocatechin-3-gallate (EGCG) in vivo. Eur J Pharmacol. 2014;740:645–51. https://doi.org/10.1016/j.ejphar.2014.06.014.CrossRefPubMed

Title: Targeting Carbohydrates and Polyphenols for a Healthy Microbiome and Healthy Weight
Authors: Matthias Van Hul
Patrice D. Cani
Publication date: 01-12-2019
Publisher: Springer US
Keywords: Obesity
Obesity
Respiratory Microbiota
Published in: Current Nutrition Reports / Issue 4/2019
Electronic ISSN: 2161-3311
DOI: https://doi.org/10.1007/s13668-019-00281-5

ACC 2024 Congress Coverage

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Targeting Carbohydrates and Polyphenols for a Healthy Microbiome and Healthy Weight

Abstract

Purpose of Review

Recent Findings

Summary

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Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

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Keynote webinar | Spotlight on sleep in brain health

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Abstract

Purpose of Review

Recent Findings

Summary

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