Dietary Factors and Modulation of Bacteria Strains of Akkermansia muciniphila and Faecalibacterium prausnitzii: A Systematic Review

Sanne Verhoog, Petek Eylul Taneri, Zayne M Roa Díaz, Pedro Marques-Vidal, John P Troup, Lia Bally, Oscar H Franco, Marija Glisic, Taulant Muka, Sanne Verhoog, Petek Eylul Taneri, Zayne M Roa Díaz, Pedro Marques-Vidal, John P Troup, Lia Bally, Oscar H Franco, Marija Glisic, Taulant Muka

Abstract

Akkermansia muciniphila and Faecalibacterium prausnitzii are highly abundant human gut microbes in healthy individuals, and reduced levels are associated with inflammation and alterations of metabolic processes involved in the development of type 2 diabetes. Dietary factors can influence the abundance of A. muciniphila and F. prausnitzii, but the evidence is not clear. We systematically searched PubMed and Embase to identify clinical trials investigating any dietary intervention in relation to A. muciniphila and F. prausnitzii. Overall, 29 unique trials were included, of which five examined A. muciniphila, 19 examined F. prausnitzii, and six examined both, in a total of 1444 participants. A caloric restriction diet and supplementation with pomegranate extract, resveratrol, polydextrose, yeast fermentate, sodium butyrate, and inulin increased the abundance of A. muciniphila, while a diet low in fermentable oligosaccharides, disaccharides, monosaccharides, and polyols decreased the abundance of A. muciniphila. For F. prausnitzii, the main studied intervention was prebiotics (e.g. fructo-oligosaccharides, inulin type fructans, raffinose); seven studies reported an increase after prebiotic intervention, while two studies reported a decrease, and four studies reported no difference. Current evidence suggests that some dietary factors may influence the abundance of A. muciniphila and F. prausnitzii. However, more research is needed to support these microflora strains as targets of microbiome shifts with dietary intervention and their use as medical nutrition therapy in prevention and management of chronic disease.

Keywords: Akkermansia muciniphila; Faecalibacterium prausnitzii; dietary interventions; microbiome; randomized controlled trials; systematic review.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Flowchart of studies included in the current review.

References

    1. Cho I., Blaser M.J. The human microbiome: At the interface of health and disease. Nat. Rev. Genet. 2012;13:260. doi: 10.1038/nrg3182.
    1. Cao Y., Shen J., Ran Z.H. Association between Faecalibacterium prausnitzii Reduction and Inflammatory Bowel Disease: A Meta-Analysis and Systematic Review of the Literature. Gastroenterol. Res. Pract. 2014;2014:872725. doi: 10.1155/2014/872725.
    1. Davies N.K., O’Sullivan J.M., Plank L.D., Murphy R. Altered gut microbiome after bariatric surgery and its association with metabolic benefits: A systematic review. Surg. Obes. Relat. Dis. Off. J. Am. Soc. Bariatr. Surg. 2019;15:656–665. doi: 10.1016/j.soard.2019.01.033.
    1. Ferreira-Halder C.V., Faria A.V.S., Andrade S.S. Action and function of Faecalibacterium prausnitzii in health and disease. Best Pract. Res. Clin. Gastroenterol. 2017;31:643–648. doi: 10.1016/j.bpg.2017.09.011.
    1. Geerlings S.Y., Kostopoulos I., de Vos W.M., Belzer C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms. 2018;6:75. doi: 10.3390/microorganisms6030075.
    1. Lopez-Siles M., Martinez-Medina M., Surís-Valls R., Aldeguer X., Sabat-Mir M., Duncan S.H., Flint H.J., Garcia-Gil L.J. Changes in the Abundance of Faecalibacterium prausnitzii Phylogroups I and II in the Intestinal Mucosa of Inflammatory Bowel Disease and Patients with Colorectal Cancer. Inflamm. Bowel Dis. 2016;22:28–41. doi: 10.1097/MIB.0000000000000590.
    1. Gao Z., Yin J., Zhang J., Ward R.E., Martin R.J., Lefevre M., Cefalu W.T., Ye J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58:1509–1517. doi: 10.2337/db08-1637.
    1. de Goffau M.C., Luopajarvi K., Knip M., Ilonen J., Ruohtula T., Härkönen T., Orivuori L., Hakala S., Welling G.W., Harmsen H.J., et al. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes. 2013;62:1238–1244. doi: 10.2337/db12-0526.
    1. Li J., Lin S., Vanhoutte P.P., Woo C.C., Xu A. Akkermansia Muciniphila Protects Against Atherosclerosis by Preventing Metabolic Endotoxemia-Induced Inflammation in Apoe-/- Mice. Circulation. 2016;133:2434–2446. doi: 10.1161/CIRCULATIONAHA.115.019645.
    1. Derrien M., Vaughan E.E., Plugge C.C., de Vos W.M. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Pt 5Int. J. Syst. Evol. Microbiol. 2004;54:1469–1476. doi: 10.1099/ijs.0.02873-0.
    1. Derrien M., Van Baarlen P., Hooiveld G., Norin E., Muller M., de Vos W.M. Modulation of Mucosal Immune Response, Tolerance, and Proliferation in Mice Colonized by the Mucin-Degrader Akkermansia muciniphila. Front. Microbiol. 2011;2:166. doi: 10.3389/fmicb.2011.00166.
    1. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., Fernandes G.R., Tap J., Bruls T., Batto J.M., et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–180. doi: 10.1038/nature09944.
    1. Louis P., Young P., Holtrop G., Flint H.H. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ. Microbiol. 2010;12:304–314. doi: 10.1111/j.1462-2920.2009.02066.x.
    1. Ganesan K., Chung S.S., Vanamala J., Xu B. Causal Relationship between Diet-Induced Gut Microbiota Changes and Diabetes: A Novel Strategy to Transplant Faecalibacterium prausnitzii in Preventing Diabetes. Int. J. Mol. Sci. 2018;19:3720. doi: 10.3390/ijms19123720.
    1. Schneeberger M., Everard A., Gomez-Valades A.G., Matamoros S., Ramírez S., Delzenne N.M., Gomis R., Claret M., Cani P.D. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci. Rep. 2015;5:16643. doi: 10.1038/srep16643.
    1. Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermúdez-Humarán L.G., Gratadoux J.J., Blugeon S., Bridonneau C., Furet J.P., Corthier G., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA. 2008;105:16731–16736. doi: 10.1073/pnas.0804812105.
    1. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., Collini S., Pieraccini G., Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA. 2010;107:14691–14696. doi: 10.1073/pnas.1005963107.
    1. Ejtahed H.H., Soroush A.A., Siadat S.S., Hoseini-Tavassol Z., Larijani B., Hasani-Ranjbar S. Targeting obesity management through gut microbiota modulation by herbal products: A systematic review. Complement. Ther. Med. 2019;42:184–204. doi: 10.1016/j.ctim.2018.11.019.
    1. Anhe F.F., 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;7:146–153. doi: 10.1080/19490976.2016.1142036.
    1. Jang S., Sun J., Chen P., Lakshman S., Molokin A., Harnly J.M., Vinyard B.T., Urban J.F. Jr., Davis C.D., Solano-Aguilar G. Flavanol-Enriched Cocoa Powder Alters the Intestinal Microbiota, Tissue and Fluid Metabolite Profiles, and Intestinal Gene Expression in Pigs. J. Nutr. 2016;146:673–680. doi: 10.3945/jn.115.222968.
    1. Magistrelli D., Zanchi R., Malagutti L., Galassi G., Canzi E., Rosi F. Effects of Cocoa Husk Feeding on the Composition of Swine Intestinal Microbiota. J. Agric. Food Chem. 2016;64:2046–2052. doi: 10.1021/acs.jafc.5b05732.
    1. Anhê F.F., Varin T.V., Le Barz M., Desjardins Y., Levy E., Roy D., Marette A. Gut Microbiota Dysbiosis in Obesity-Linked Metabolic Diseases and Prebiotic Potential of Polyphenol-Rich Extracts. Curr. Obes. Rep. 2015;4:389–400. doi: 10.1007/s13679-015-0172-9.
    1. Walker J.J., Eckardt P., Aleman J.O., da Rosa J.C., Liang Y., Iizumi T., Etheve S., Blaser M.J., L Breslow J., Holt P.R. The effects of trans-resveratrol on insulin resistance, inflammation, and microbiota in men with the metabolic syndrome: A pilot randomized, placebo-controlled clinical trial. J. Clin. Transl. Res. 2019;4:122–135.
    1. Halmos E.E., Christophersen C.C., Bird A.A., Shepherd S.S., Gibson P.P., Muir J.J. Diets that differ in their FODMAP content alter the colonic luminal microEnvironironment. Gut. 2015;64:93–100. doi: 10.1136/gutjnl-2014-307264.
    1. Halmos E.E., Christophersen C.C., Bird A.A., Shepherd S.S., Muir J.J., Gibson P.P. Consistent Prebiotic Effect on Gut Microbiota With Altered FODMAP Intake in Patients with Crohn’s Disease: A Randomised, Controlled Cross-Over Trial of Well-Defined Diets. Clin. Transl. Gastroenterol. 2016;7:e164. doi: 10.1038/ctg.2016.22.
    1. Ramirez-Farias C., Slezak K., Fuller Z., Duncan A., Holtrop G., Louis P. Effect of inulin on the human gut microbiota: Stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br. J. Nutr. 2009;101:541–550. doi: 10.1017/S0007114508019880.
    1. Ramnani P., Gaudier E., Bingham M., van Bruggen P., Tuohy K.K., Gibson G.G. Prebiotic effect of fruit and vegetable shots containing Jerusalem artichoke inulin: A human intervention study. Br. J. Nutr. 2010;104:233–240. doi: 10.1017/S000711451000036X.
    1. Roshanravan N., Mahdavi R., Alizadeh E., Ghavami A., Rahbar Saadat Y., Mesri Alamdari N., Alipour S., Dastouri M.R., Ostadrahimi A. The effects of sodium butyrate and inulin supplementation on angiotensin signaling pathway via promotion of Akkermansia muciniphila abundance in type 2 diabetes; A randomized, double-blind, placebo-controlled trial. J. Cardiovasc. Thorac. Res. 2017;9:183–190. doi: 10.15171/jcvtr.2017.32.
    1. Moher D., Liberati A., Tetzlaff J., Altman D.D., Group P. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009;6:e1000097. doi: 10.1371/journal.pmed.1000097.
    1. Stroup D.F., Berlin J.J., Morton S.C., Olkin I., Williamson G.D., Rennie D., Moher D., Becker B.J., Sipe T.A., Thacker S.B. Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2008;283:2008–2012. doi: 10.1001/jama.283.15.2008.
    1. Higgins J.P., Altman D.G., Gøtzsche P.C., Jüni P., Moher D., Oxman A.D., Savovic J., Schulz K.F., Weeks L., Sterne J.A., et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928. doi: 10.1136/bmj.d5928.
    1. Benjamin J.L., Hedin C.R., Koutsoumpas A., Ng S.C., McCarthy N.E., Hart A.L., Kamm M.A., Sanderson J.D., Knight S.C., Forbes A., et al. Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn’s disease. Gut. 2011;60:923–929. doi: 10.1136/gut.2010.232025.
    1. Blatchford P., Stoklosinski H., Eady S., Wallace A., Butts C., Gearry R., Gibson G., Ansell J. Consumption of kiwifruit capsules increases Faecalibacterium prausnitzii abundance in functionally constipated individuals: A randomised controlled human trial. J. Nutr. Sci. 2017;6:e52. doi: 10.1017/jns.2017.52.
    1. Clavel T., Fallani M., Lepage P., Levenez F., Mathey J., Rochet V., Sérézat M., Sutren M., Henderson G., Bennetau-Pelissero C., et al. Isoflavones and functional foods alter the dominant intestinal microbiota in postmenopausal women. J. Nutr. 2005;135:2786–2792. doi: 10.1093/jn/135.12.2786.
    1. Dao M.M., Everard A., Aron-Wisnewsky J., Sokolovska N., Prifti E., Verger E.O., Kayser B.D., Levenez F., Chilloux J., Hoyles L., et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: Relationship with gut microbiome richness and ecology. Gut. 2016;65:426–436. doi: 10.1136/gutjnl-2014-308778.
    1. Dewulf E.M., Cani P.D., Claus S.P., Fuentes S., Puylaert P.G., Neyrinck A.M., Bindels L.B., de Vos W.M., Gibson G.R., Thissen J.P., et al. Insight into the prebiotic concept: Lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut. 2013;62:1112–1121. doi: 10.1136/gutjnl-2012-303304.
    1. Fava F., Gitau R., Griffin B.B., Gibson G.G., Tuohy K.K., Lovegrove J.J. The type and quantity of dietary fat and carbohydrate alter faecal microbiome and short-chain fatty acid excretion in a metabolic syndrome ’at-risk’ population. Int. J. Obes. (2005) 2013;37:216–223. doi: 10.1038/ijo.2012.33.
    1. Fernando W.W., Hill J.J., Zello G.G., Tyler R.R., Dahl W.W., Van Kessel A.A. Diets supplemented with chickpea or its main oligosaccharide component raffinose modify faecal microbial composition in healthy adults. Benef. Microbes. 2010;1:197–207. doi: 10.3920/BM2009.0027.
    1. Guadamuro L., Delgado S., Redruello B., Flórez A.B., Suárez A., Martínez-Camblor P., Mayo B. Equol status and changes in fecal microbiota in menopausal women receiving long-term treatment for menopause symptoms with a soy-isoflavone concentrate. Front. Microbiol. 2015;6:777. doi: 10.3389/fmicb.2015.00777.
    1. Hooda S., Boler B.M., Serao M.C., Brulc J.M., Staeger M.A., Boileau T.W., Dowd S.E., Fahey G.C., Jr., Swanson K.S. 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. J. Nutr. 2012;142:1259–1265. doi: 10.3945/jn.112.158766.
    1. Hustoft T.N., Hausken T., Ystad S.O., Valeur J., Brokstad K., Hatlebakk J.G., Lied G.A. Effects of varying dietary content of fermentable short-chain carbohydrates on symptoms, fecal microEnvironironment, and cytokine profiles in patients with irritable bowel syndrome. Neurogastroenterol. Motil. Off. J. Eur. Gastrointest. Motil. Soc. 2017;29:e12969. doi: 10.1111/nmo.12969.
    1. Lee T., Clavel T., Smirnov K., Schmidt A., Lagkouvardos I., Walker A., Lucio M., Michalke B., Schmitt-Kopplin P., Fedorak R., et al. Oral versus intravenous iron replacement therapy distinctly alters the gut microbiota and metabolome in patients with IBD. Gut. 2017;66:863–871. doi: 10.1136/gutjnl-2015-309940.
    1. Li Z., Henning S.M., Lee R.P., Lu Q.Y., Summanen P.H., Thames G., Corbett K., Downes J., Tseng C.H., Finegold S.M., et al. Pomegranate extract induces ellagitannin metabolite formation and changes stool microbiota in healthy volunteers. Food Funct. 2015;6:2487–2495. doi: 10.1039/C5FO00669D.
    1. Majid H.H., Cole J., Emery P.P., Whelan K. Additional oligofructose/inulin does not increase faecal bifidobacteria in critically ill patients receiving enteral nutrition: A randomised controlled trial. Clin. Nutr. (Edinb. Scotl.) 2014;33:966–972. doi: 10.1016/j.clnu.2013.11.008.
    1. Medina-Vera I., Sanchez-Tapia M., Noriega-Lopez L., Granados-Portillo O., Guevara-Cruz M., Flores-López A., Avila-Nava A., Fernández M.L., Tovar A.R., Torres N. A dietary intervention with functional foods reduces metabolic endotoxaemia and attenuates biochemical abnormalities by modifying faecal microbiota in people with type 2 diabetes. Diabetes Metab. 2019;45:122–131. doi: 10.1016/j.diabet.2018.09.004.
    1. Moreno-Indias I., Sanchez-Alcoholado L., Perez-Martinez P., Andrés-Lacueva C., Cardona F., Tinahones F., Queipo-Ortuño M.I. Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients. Food Funct. 2016;7:1775–1787. doi: 10.1039/C5FO00886G.
    1. Most J., Penders J., Lucchesi M., Goossens G.G., Blaak E.E. Gut microbiota composition in relation to the metabolic response to 12-week combined polyphenol supplementation in overweight men and women. Eur. J. Clin. Nutr. 2017;71:1040–1045. doi: 10.1038/ejcn.2017.89.
    1. Pinheiro I., Robinson L., Verhelst A., Marzorati M., Winkens B., den Abbeele P.V., Possemiers S. A yeast fermentate improves gastrointestinal discomfort and constipation by modulation of the gut microbiome: Results from a randomized double-blind placebo-controlled pilot trial. BMC Complement. Altern. Med. 2017;17:441. doi: 10.1186/s12906-017-1948-0.
    1. Tagliabue A., Ferraris C., Uggeri F., Trentani C., Bertoli S., de Giorgis V., Veggiotti P., Elli M. Short-term impact of a classical ketogenic diet on gut microbiota in GLUT1 Deficiency Syndrome: A 3-month prospective observational study. Clin. Nutr. ESPEN. 2017;17:33–37. doi: 10.1016/j.clnesp.2016.11.003.
    1. Wijayabahu A.A., Waugh S.S., Ukhanova M., Mai V. Dietary raisin intake has limited effect on gut microbiota composition in adult volunteers. Nutr. J. 2019;18:14. doi: 10.1186/s12937-019-0439-1.
    1. Xu J., Lian F., Zhao L., Zhao Y., Chen X., Zhang X., Guo Y., Zhang C., Zhou Q., Xue Z., et al. Structural modulation of gut microbiota during alleviation of type 2 diabetes with a Chinese herbal formula. ISME J. 2015;9:552–562. doi: 10.1038/ismej.2014.177.
    1. Benus R.F., van der Werf T.S., Welling G.W., Judd P.A., Taylor M.A., Harmsen H.J., Whelan K. Association between Faecalibacterium prausnitzii and dietary fibre in colonic fermentation in healthy human subjects. Br. J. Nutr. 2010;104:693–700. doi: 10.1017/S0007114510001030.
    1. James S.L., Christophersen C.T., Bird A.R., Conlon M.A., Rosella O., Gibson P.R., Muir J.G. Abnormal fibre usage in UC in remission. Gut. 2015;64:562–570. doi: 10.1136/gutjnl-2014-307198.
    1. Vulevic J., Juric A., Tzortzis G., Gibson G.G. A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults1–3. J. Nutr. 2013;143:324–331. doi: 10.3945/jn.112.166132.
    1. West N.P., Christophersen C.T., Pyne D.B., Cripps A.W., Conlon M.A., Topping D.L., Kang S., McSweeney C.S., Fricker P.A., Aguirre D., et al. Butyrylated starch increases colonic butyrate concentration but has limited effects on immunity in healthy physically active individuals. Exerc. Immunol. Rev. 2013;19:102–119.
    1. Bull M.M., Plummer N.N. Part 1: The Human Gut Microbiome in Health and Disease. Integr. Med. 2014;13:17–22.
    1. Vyas U., Ranganathan N. Probiotics, prebiotics, and synbiotics: Gut and beyond. Gastroenterol. Res. Pract. 2012;2012:872716. doi: 10.1155/2012/872716.
    1. Karlsson F.H., Tremaroli V., Nookaew I., Bergström G., Behre C.J., Fagerberg B., Nielsen J., Bäckhed F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498:99–103. doi: 10.1038/nature12198.
    1. Vrieze A., Van Nood E., Holleman F., Salojärvi J., Kootte R.S., Bartelsman J.F., Dallinga-Thie G.M., Ackermans M.T., Serlie M.J., Oozeer R., et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913–916.e7. doi: 10.1053/j.gastro.2012.06.031.
    1. Belzer C., Chia L.W., Aalvink S., Chamlagain B., Piironen V., Knol J., de Vos W.M. Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B12 Production by Intestinal Symbionts. MBio. 2017;8 doi: 10.1128/mBio.00770-17.
    1. Chang P.P., Hao L., Offermanns S., Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl. Acad. Sci. USA. 2014;111:2247–2252. doi: 10.1073/pnas.1322269111.
    1. Furusawa Y., Obata Y., Fukuda S., Endo T.A., Nakato G., Takahashi D., Nakanishi Y., Uetake C., Kato K., Kato T., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446–450. doi: 10.1038/nature12721.
    1. Kelly C.J., Zheng L., Campbell E.L., Saeedi B., Scholz C.C., Bayless A.J., Wilson K.E., Glover L.E., Kominsky D.J., Magnuson A., et al. Crosstalk between Microbiota-Derived Short-Chain Fatty Acids and Intestinal Epithelial HIF Augments Tissue Barrier Function. Cell Host Microbe. 2015;17:662–671. doi: 10.1016/j.chom.2015.03.005.
    1. Wang H., Hou L., Kwak D., Fassett J., Xu X., Chen A., Chen W., Blazar B.R., Xu Y., Hall J.L., et al. Increasing Regulatory T Cells With Interleukin-2 and Interleukin-2 Antibody Complexes Attenuates Lung Inflammation and Heart Failure Progression. Hypertension. 2016;68:114–122. doi: 10.1161/HYPERTENSIONAHA.116.07084.
    1. De Vadder F., Kovatcheva-Datchary P., Goncalves D., Vinera J., Zitoun C., Duchampt A., Bäckhed F., Mithieux G. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell. 2014;156:84–96. doi: 10.1016/j.cell.2013.12.016.
    1. Lukovac S., Belzer C., Pellis L., Keijser B.J., de Vos W.M., Montijn R.C., Roeselers G. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. MBio. 2014;5 doi: 10.1128/mBio.01438-14.
    1. Lee H., Ko G. Effect of metformin on metabolic improvement and gut microbiota. Appl. Environ. Microbiol. 2014;80:5935–5943. doi: 10.1128/AEM.01357-14.
    1. Shin N.R., Lee J.C., Lee H.Y., Kim M.S., Whon T.W., Lee M.S., Bae J.W. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 2014;63:727–735. doi: 10.1136/gutjnl-2012-303839.
    1. Everard A., Belzer C., Geurts L., Ouwerkerk J.P., Druart C., Bindels L.B., Guiot Y., Derrien M., Muccioli G.G., Delzenne N.M., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA. 2013;110:9066–9071. doi: 10.1073/pnas.1219451110.
    1. Singh R.K., Chang H.W., Yan D., Lee K.M., Ucmak D., Wong K., Abrouk M., Farahnik B., Nakamura M., Zhu T.H., et al. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 2017;15 doi: 10.1186/s12967-017-1175-y.
    1. Morrison D.D., Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes. 2016;7:189–200. doi: 10.1080/19490976.2015.1134082.
    1. Jardine M. Nutrition Considerations for Microbiota Health in Diabetes. Diabetes Spectr. A Publ. Am. Diabetes Assoc. 2016;29:238–244. doi: 10.2337/ds16-0003.
    1. Liu X., Wu Y., Li F., Zhang D. Dietary fiber intake reduces risk of inflammatory bowel disease: Result from a meta-analysis. Nutr. Res. 2015;35:753–758. doi: 10.1016/j.nutres.2015.05.021.
    1. McRae M.M. Dietary Fiber Intake and Type 2 Diabetes Mellitus: An Umbrella Review of Meta-analyses. J. Chiropr. Med. 2018;17:44–53. doi: 10.1016/j.jcm.2017.11.002.
    1. Ismail T., Sestili P., Akhtar S. Pomegranate peel and fruit extracts: A review of potential anti-inflammatory and anti-infective effects. J. Ethnopharmacol. 2012;143:397–405. doi: 10.1016/j.jep.2012.07.004.
    1. Medjakovic S., Jungbauer A. Pomegranate: A fruit that ameliorates metabolic syndrome. Food Funct. 2013;4:19–39. doi: 10.1039/C2FO30034F.
    1. Franco O.H., Chowdhury R., Troup J., Voortman T., Kunutsor S., Kavousi M., Oliver-Williams C., Muka T. Use of Plant-Based Therapies and Menopausal Symptoms: A Systematic Review and Meta-analysis. JAMA. 2016;315:2554–2563. doi: 10.1001/jama.2016.8012.
    1. Glisic M., Kastrati N., Gonzalez-Jaramillo V., Bramer W.M., Ahmadizar F., Chowdhury R., Danser A.J., Roks A.J., Voortman T., Franco O.H., et al. Associations between Phytoestrogens, Glucose Homeostasis, and Risk of Diabetes in Women: A Systematic Review and Meta-Analysis. Adv. Nutr. 2018;9:726–740. doi: 10.1093/advances/nmy048.
    1. Ozdal T., Sela D.D., Xiao J., Boyacioglu D., Chen F., Capanoglu E. The Reciprocal Interactions between Polyphenols and Gut Microbiota and Effects on Bioaccessibility. Nutrients. 2016;8:78. doi: 10.3390/nu8020078.
    1. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E., Ling A.V., Devlin A.S., Varma Y., Fischbach M.A., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. doi: 10.1038/nature12820.
    1. Gomez A., Luckey D., Taneja V. The gut microbiome in autoimmunity: Sex matters. Clin. Immunol. 2015;159:154–162. doi: 10.1016/j.clim.2015.04.016.
    1. Kaplan H., Hill K., Lancaster J., Hurtado A.A. A theory of human life history evolution: Diet, intelligence, and longevity. Evol. Anthropol. Issues News Rev. 2000;9:156–185. doi: 10.1002/1520-6505(2000)9:4<156::AID-EVAN5>;2-7.
    1. Zeevi D., Korem T., Zmora N., Israeli D., Rothschild D., Weinberger A., Ben-Yacov O., Lador D., Avnit-Sagi T., Lotan-Pompan M., et al. Personalized Nutrition by Prediction of Glycemic Responses. Cell. 2015;163:1079–1094. doi: 10.1016/j.cell.2015.11.001.
    1. Moen B., Berget I., Rud I., Hole A.A., Kjos N.N., Sahlstrom S. Extrusion of barley and oat influence the fecal microbiota and SCFA profile of growing pigs. Food Funct. 2016;7:1024–1032. doi: 10.1039/C5FO01452B.
    1. Grundy M.M.-L., Lapsley K., Ellis P.P. A review of the impact of processing on nutrient bioaccessibility and digestion of almonds. Int. J. Food Sci. Technol. 2016;51:1937–1946. doi: 10.1111/ijfs.13192.
    1. Zinöcker M.M., Lindseth I.I. The Western Diet-Microbiome-Host Interaction and Its Role in Metabolic Disease. Nutrients. 2018;10:365. doi: 10.3390/nu10030365.

Source: PubMed

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