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Microbiota and metabolic diseases

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Abstract

The microbiota is a complex ecosystem of microorganisms consisting of bacteria, viruses, protozoa, and fungi, living in different districts of the human body, such as the gastro-enteric tube, skin, mouth, respiratory system, and the vagina. Over 70% of the microbiota lives in the gastrointestinal tract in a mutually beneficial relationship with its host. The microbiota plays a major role in many metabolic functions, including modulation of glucose and lipid homeostasis, regulation of satiety, production of energy and vitamins. It exerts a role in the regulation of several biochemical and physiological mechanisms through the production of metabolites and substances. In addition, the microbiota has important anti-carcinogenetic and anti-inflammatory actions. There is growing evidence that any modification in the microbiota composition can lead to several diseases, including metabolic diseases, such as obesity and diabetes, and cardiovascular diseases. This is because alterations in the microbiota composition can cause insulin resistance, inflammation, vascular, and metabolic disorders. The causes of the microbiota alterations and the mechanisms by which microbiota modifications can act on the development of metabolic and cardiovascular diseases have been reported. Current and future preventive and therapeutic strategies to prevent these diseases by an adequate modulation of the microbiota have been also discussed.

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Abbreviations

AMPK:

AMP-Activated protein kinase

CVD:

Cardiovascular diseases

FIAF:

Fasting-induced adipose factor

FMI:

Fecal microbiota transplant

GLP-1:

Glucagon-like peptide 1

GLP-2:

Glucagon-like peptide-2

HDL:

High-density lipoprotein

HFD:

High-fat diet

IR:

Insulin resistance

LPL:

Lipoprotein lipase

LPS:

Lipopolysaccharide

MS:

Metabolic syndrome

PYY:

Peptide YY

RYGB:

Roux-en-Y bypass

SCFAs:

Short-chain fatty acids

T1D:

Type 1 diabetes

T2D:

Type 2 diabetes

TLR4:

Toll-like receptor 4

TMAO:

Trimethylamine-N-oxide

VLDL:

Very low-density lipoprotein

References

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. C. Palmer, E.M. Bik, D.B. DiGiulio, D.A. Relman, P.O. Brown, Development of the human infant intestinal microbiota. PLoS Biol. 5, 1556–1573 (2007). https://doi.org/10.1371/journal.pbio.0050177

    Article  CAS  Google Scholar 

  3. A. Pingitore, E.S. Chambers, T. Hill, I.R. Maldonado, B. Liu, G. Bewick, D.J. Morrison, T. Preston, G.A. Wallis, C. Tedford, R. Castañera González, G.C. Huang, P. Choudhary, G. Frost, S.J. Persaud, The diet-derived short chain fatty acid propionate improves beta-cell function in humans and stimulates insulin secretion from human islets in vitro. Diabetes Obes. Metab. 19, 257–265 (2017). https://doi.org/10.1111/dom.12811

    Article  PubMed  CAS  Google Scholar 

  4. F. Bäckhed, J. Roswall, Y. Peng, Q. Feng, H. Jia, P. Kovatcheva-Datchary, Y. Li, Y. Xia, H. Xie, H. Zhong, M.T. Khan, J. Zhang, J. Li, L. Xiao, J. Al-Aama, D. Zhang, Y.S. Lee, D. Kotowska, C. Colding, V. Tremaroli, Y. Yin, S. Bergman, X. Xu, L. Madsen, K. Kristiansen, J. Dahlgren, J. Wang, W. Jun, Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690–703 (2015). https://doi.org/10.1016/j.chom.2015.04.004

    Article  PubMed  CAS  Google Scholar 

  5. B.S. Ramakrishna, The normal bacterial flora of the human intestine and its regulation. J. Clin. Gastroenterol. 41, S2–S6 (2007)

    Article  Google Scholar 

  6. F. Bäckhed, C.M. Fraser, Y. Ringel, M.E. Sanders, R.B. Sartor, P.M. Sherman, J. Versalovic, V. Young, B.B. Finlay, Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 12, 611–622 (2012). https://doi.org/10.1016/j.chom.2012.10.012

    Article  PubMed  CAS  Google Scholar 

  7. Human Microbiome Project C., A framework for human microbiome research. Nature 486, 215–221 (2012). https://doi.org/10.1038/nature11209

    Article  CAS  Google Scholar 

  8. E.A. Grice, J.A. Segre, The human microbiome: our second genome. Annu. Rev. Genom. Hum. Genet. 13, 151–170 (2012). https://doi.org/10.1146/annurev-genom-090711-163814

    Article  CAS  Google Scholar 

  9. D.A. Hill, D. Artis, Intestinal bacteria and the regulation of immune cell homeostasis. Annu. Rev. Immunol. 28, 623–667 (2010). https://doi.org/10.1146/annurev-immunol-030409-101330

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. C. Mueller, A.J. Macpherson, Layers of mutualism with commensal bacteria protect us from intestinal inflammation. Gut 55, 276–284 (2006)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. F. Guarner, J.-R. Malagelada, Gut flora in health and disease. Lancet 361, 512–519 (2003). https://doi.org/10.1016/S0140-6736(03)12489-0

    Article  PubMed  Google Scholar 

  12. I. Rowland, G. Gibson, A. Heinken, K. Scott, J. Swann, I. Thiele, K. Tuohy, Gut microbiota functions: metabolism of nutrients and other food components. Eur. J. Nutr. 57(1), 1–24 (2017). https://doi.org/10.1007/s00394-017-1445-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. L. Capurso, Il Microbiota intestinale. Recent. Prog. Med. 107, 257–266 (2016)

    Google Scholar 

  14. E.F. Enright, C.G.M. Gahan, S.A. Joyce, B.T. Griffin, The impact of the gut microbiota on drug metabolism and clinical outcome. Yale J. Biol. Med. 89, 375–382 (2016)

    PubMed  PubMed Central  CAS  Google Scholar 

  15. D.R. Donohoe, N. Garge, X. Zhang, W. Sun, T.M. O’Connell, M.K. Bunger, S.J. Bultman, The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 13, 517–526 (2011). https://doi.org/10.1016/j.cmet.2011.02.018

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. N. Kobyliak, O. Virchenko, T. Falalyeyeva, Pathophysiological role of host microbiota in the development of obesity. Nutr. J. 15, 1–12 (2016). https://doi.org/10.1186/s12937-016-0166-9

    Article  CAS  Google Scholar 

  17. Y.E. Borre, G.W. O’Keeffe, G. Clarke, C. Stanton, T.G. Dinan, J.F. Cryan, Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol. Med. 20, 509–518 (2014). https://doi.org/10.1016/j.molmed.2014.05.002

    Article  PubMed  Google Scholar 

  18. D.J. Morrison, T. Preston, Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7, 189–200 (2016). https://doi.org/10.1080/19490976.2015.1134082

    Article  PubMed  PubMed Central  Google Scholar 

  19. G. den Besten, K. van Eunen, A.K. Groen, K. Venema, D.-J. Reijngoud, B.M. Bakker, The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54, 2325–2340 (2013). https://doi.org/10.1194/jlr.R036012

    Article  CAS  Google Scholar 

  20. G.T. Macfarlane, G.R. Gibson, J.H. Cummings, Comparison of fermentation reactions in different regions of the human colon. J. Appl. Bacteriol. 72, 57–64 (1992). https://doi.org/10.1111/j.1365-2672.1992.tb04882.x

    Article  PubMed  CAS  Google Scholar 

  21. J.G. LeBlanc, F. Chain, R. Martín, L.G. Bermúdez-Humarán, S. Courau, P. Langella, Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb. Cell Fact. 16, 1–10 (2017). https://doi.org/10.1186/s12934-017-0691-z

    Article  Google Scholar 

  22. C.K. Chakraborti, New-found link between microbiota and obesity. World J. Gastrointest. Pathophysiol. 6, 110–119 (2015). https://doi.org/10.4291/wjgp.v6.i4.110

    Article  PubMed  PubMed Central  Google Scholar 

  23. X. Li, Y. Shimizu, I. Kimura, Gut microbial metabolite short-chain fatty acids and obesity. Biosci. Micro., Food Heal. 36, 135–140 (2017). https://doi.org/10.12938/bmfh.17-010

    Article  Google Scholar 

  24. P. Schönfeld, L. Wojtczak, Short- and medium-chain fatty acids in energy metabolism: the cellular perspective. J. Lipid Res. 57, 943–954 (2016). https://doi.org/10.1194/jlr.R067629

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. D.N. Cooper, R.J. Martin, N.L. Keim, Does whole grain consumption alter gut microbiota and satiety? Healthc. (Basel, Switz.) 3, 364–392 (2015). https://doi.org/10.3390/healthcare3020364

    Article  Google Scholar 

  26. A. Everard, P.D. Cani, Gut microbiota and GLP-1. Rev. Endocr. Metab. Disord. 15, 189–196 (2014)

    Article  PubMed  CAS  Google Scholar 

  27. G. Frost, M.L. Sleeth, M. Sahuri-Arisoylu, B. Lizarbe, S. Cerdan, L. Brody, J. Anastasovska, S. Ghourab, M. Hankir, S. Zhang, D. Carling, J.R. Swann, G. Gibson, A. Viardot, D. Morrison, E.L. Thomas, J.D. Bell, The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat. Commun. 5, 3611 (2014). https://doi.org/10.1038/ncomms4611

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. L.E.M. Willemsen, M.A. Koetsier, S.J.H. van Deventer, E.A.F. van Tol, Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut 52, 1442–1447 (2003)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. F.J. Cousin, S. Jouan-Lanhouet, N. Theret, C. Brenner, E. Jouan, G. Le Moigne-Muller, M.-T. Dimanche-Boitrel, G. Jan, The probiotic Propionibacterium freudenreichii as a new adjuvant for TRAIL-based therapy in colorectal cancer. Oncotarget 7, 7161–7178 (2016). https://doi.org/10.18632/oncotarget.6881

    Article  PubMed  PubMed Central  Google Scholar 

  30. J. Ni, G.D. Wu, L. Albenberg, V.T. Tomov, Gut microbiota and IBD: Causation or correlation? Nat. Rev. Gastroenterol. Hepatol. 14, 573–584 (2017)

    PubMed  PubMed Central  Google Scholar 

  31. H.J. Flint, E.A. Bayer, Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract. Ann. New Y. Acad. Sci. 1125, 280–288 (2008)

    Article  CAS  Google Scholar 

  32. P. van den Abbeele, P. Gérard, S. Rabot, A. Bruneau, S. El Aidy, M. Derrien, M. Kleerebezem, E.G. Zoetendal, H. Smidt, W. Verstraete, T. van de Wiele, S. Possemiers, Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats. Environ. Microbiol. 13, 2667–2680 (2011). https://doi.org/10.1111/j.1462-2920.2011.02533.x

    Article  PubMed  CAS  Google Scholar 

  33. A.L. McOrist, R.B. Miller, A.R. Bird, J.B. Keogh, M. Noakes, D.L. Topping, M.A. Conlon, Fecal butyrate levels vary widely among individuals but are usually increased by a diet high in resistant starch. J. Nutr. 141, 883–889 (2011). https://doi.org/10.3945/jn.110.128504

    Article  PubMed  CAS  Google Scholar 

  34. C. Grootaert, P. Van Den Abbeele, M. Marzorati, W.F. Broekaert, C.M. Courtin, J.A. Delcour, W. Verstraete, T. Van De Wiele, Comparison of prebiotic effects of arabinoxylan oligosaccharides and inulin in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol. Ecol. 69, 231–242 (2009). https://doi.org/10.1111/j.1574-6941.2009.00712.x

    Article  PubMed  CAS  Google Scholar 

  35. M. Begley, C. Hill, C.G.M. Gahan, Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 72, 1729–1738 (2006). https://doi.org/10.1128/AEM.72.3.1729-1738.2006

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. WHO | Obesity and overweight. (WHO, Geneva, Switzerland, 2018)

  37. K. Ball, G. Mishra, D. Crawford, Which aspects of socioeconomic status are related to obesity among men and women? Int. J. Obes. Relat. Metab. Disord. 26, 559–565 (2002). https://doi.org/10.1038/sj.ijo.0801960

    Article  PubMed  CAS  Google Scholar 

  38. J.F. Rawls, M.A. Mahowald, R.E. Ley, J.I. Gordon, Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127, 423–433 (2018). https://doi.org/10.1016/j.cell.2006.08.043

    Article  CAS  Google Scholar 

  39. R. Ley, P. Turnbaugh, S. Klein, J. Gordon, Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023 (2006). https://doi.org/10.1038/nature4441021a

    Article  PubMed  CAS  Google Scholar 

  40. M.A. Hildebrandt, C. Hoffman, S.A. Sherrill-Mix, S.A. Keilbaugh, M. Hamady, Y.-Y. Chen, R. Knight, R.S. Ahima, F. Bushman, G.D. Wu, High fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137, 1712–1716 (2009). https://doi.org/10.1053/j.gastro.2009.08.042

    Article  CAS  Google Scholar 

  41. P.J. Turnbaugh, F. Bäckhed, L. Fulton, J.I. Gordon, Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213–223 (2008). https://doi.org/10.1016/j.chom.2008.02.015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. M.A. Conlon, A.R. Bird, The impact of diet and lifestyle on gut microbiota and human health. Nutrients 7, 17–44 (2015). https://doi.org/10.3390/nu7010017

    Article  CAS  Google Scholar 

  43. J. Hamzelou, Antibiotic overuse may promote obesity. New Sci. 213, 8–9 (2012). https://doi.org/10.1016/S0262-4079(12)60797-0

    Article  Google Scholar 

  44. L. Trasande, J. Blustein, M. Liu, E. Corwin, L.M. Cox, M.J. Blaser, Infant antibiotic exposures and early-life body mass. Int. J. Obes. (Lond.). 37, 16–23 (2013). https://doi.org/10.1038/ijo.2012.132

    Article  CAS  Google Scholar 

  45. L. Dethlefsen, D.A. Relman, Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl Acad. Sci. U.S.A. 108, Suppl, 4554–4561 (2011). https://doi.org/10.1073/pnas.1000087107

    Article  PubMed  Google Scholar 

  46. P. Vangay, T. Ward, J.S. Gerber, D. Knights, Antibiotics, pediatric dysbiosis, and disease. Cell Host Microbe 17, 553–564 (2015). https://doi.org/10.1016/J.CHOM.2015.04.006

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. F. Bäckhed, H. Ding, T. Wang, L.V. Hooper, G.Y. Koh, A. Nagy, C.F. Semenkovich, J.I. Gordon, The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl Acad. Sci. U.S.A. 101, 15718–15723 (2004). https://doi.org/10.1073/pnas.0407076101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, V. Magrini, E.R. Mardis, J.I. Gordon, An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006). https://doi.org/10.1038/nature05414

    Article  PubMed  Google Scholar 

  49. A.P. Liou, M. Paziuk, J.M. Luevano, S. Machineni, P.J. Turnbaugh, L.M. Kaplan, Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med. 5, 178ra41 (2013). https://doi.org/10.1126/scitranslmed.3005687

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. S. Kersten, S. Mandard, N.S. Tan, P. Escher, D. Metzger, P. Chambon, F.J. Gonzalez, B. Desvergne, W. Wahli, Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J. Biol. Chem. 275, 28488–28493 (2000). https://doi.org/10.1074/jbc.M004029200

    Article  PubMed  CAS  Google Scholar 

  51. E.M. Cushing, X. Chi, K.L. Sylvers, S.K. Shetty, M.J. Potthoff, B.S.J. Davies, Angiopoietin-like 4 directs uptake of dietary fat away from adipose during fasting. Mol. Metab. 6, 809–818 (2017). https://doi.org/10.1016/j.molmet.2017.06.007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. F. Bäckhed, J.K. Manchester, C.F. Semenkovich, J.I. Gordon, Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl Acad. Sci. U.S.A. 104, 979–984 (2007). https://doi.org/10.1073/pnas.0605374104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. N.E. Boutagy, R.P. McMillan, M.I. Frisard, M.W. Hulver, Metabolic endotoxemia with obesity: Is it real and is it relevant? Biochimie 124, 11–20 (2016). https://doi.org/10.1016/j.biochi.2015.06.020

    Article  PubMed  CAS  Google Scholar 

  54. H. Ghanim, S. Abuaysheh, C.L. Sia, K. Korzeniewski, A. Chaudhuri, J.M. Fernandez-Real, P. Dandona, Increase in plasma endotoxin concentrations and the expression of toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal: Implications for insulin resistance. Diabetes Care 32, 2281–2287 (2009). https://doi.org/10.2337/dc09-0979

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. P.D. Cani, J. Amar, M.A. Iglesias, M. Poggi, C. Knauf, D. Bastelica, A.M. Neyrinck, F. Fava, K.M. Tuohy, C. Chabo, A. Waget, E. Delmée, B. Cousin, T. Sulpice, B. Chamontin, J. Ferrières, J.F. Tanti, G.R. Gibson, L. Casteilla, N.M. Delzenne, M.C. Alessi, R. Burcelin, Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761–1772 (2007). https://doi.org/10.2337/db06-1491

    Article  PubMed  CAS  Google Scholar 

  56. M.M. Mihaylova, R.J. Shaw, The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell. Biol. 13, 1016–1023 (2011). https://doi.org/10.1038/ncb2329

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. E. Le Poul, C. Loison, S. Struyf, J.-Y. Springael, V. Lannoy, M.-E. Decobecq, S. Brezillon, V. Dupriez, G. Vassart, J. Van Damme, M. Parmentier, M. Detheux, Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J. Biol. Chem. 278, 25481–25489 (2003). https://doi.org/10.1074/jbc.M301403200

    Article  PubMed  CAS  Google Scholar 

  58. A.J. Brown, S.M. Goldsworthy, A.A. Barnes, M.M. Eilert, L. Tcheang, D. Daniels, A.I. Muir, M.J. Wigglesworth, I. Kinghorn, N.J. Fraser, N.B. Pike, J.C. Strum, K.M. Steplewski, P.R. Murdock, J.C. Holder, F.H. Marshall, P.G. Szekeres, S. Wilson, D.M. Ignar, S.M. Foord, A. Wise, S.J. Dowell, The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 278, 11312–11319 (2003). https://doi.org/10.1074/jbc.M211609200

    Article  PubMed  CAS  Google Scholar 

  59. B.S. Samuel, A. Shaito, T. Motoike, F.E. Rey, F. Backhed, J.K. Manchester, R.E. Hammer, S.C. Williams, J. Crowley, M. Yanagisawa, J.I. Gordon, 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. 105, 16767–16772 (2008)

    Article  PubMed  CAS  Google Scholar 

  60. M. Bjursell, T. Admyre, M. Göransson, A.E. Marley, D.M. Smith, J. Oscarsson, M. Bohlooly-Y, Improved glucose control and reduced body fat mass in free fatty acid receptor 2-deficient mice fed a high-fat diet. Am. J. Physiol. Metab. 300, E211–E220 (2010). https://doi.org/10.1152/ajpendo.00229.2010

    Article  CAS  Google Scholar 

  61. V.K. Ridaura, J.J. Faith, F.E. Rey, J. Cheng, A.E. Duncan, A.L. Kau, N.W. Griffin, V. Lombard, B. Henrissat, J.R. Bain, M.J. Muehlbauer, O. Ilkayeva, C.F. Semenkovich, K. Funai, D.K. Hayashi, B.J. Lyle, M.C. Martini, L.K. Ursell, J.C. Clemente, W. Van Treuren, W.A. Walters, R. Knight, C.B. Newgard, A.C. Heath, J.I. Gordon, Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341, 1241214 (2013). https://doi.org/10.1126/science.1241214

    Article  PubMed  CAS  Google Scholar 

  62. N.-R. Shin, J.-C. Lee, H.-Y. Lee, M.-S. Kim, T.W. Whon, M.-S. Lee, J.-W. Bae, An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63, 727–735 (2014). https://doi.org/10.1136/gutjnl-2012-303839

    Article  PubMed  CAS  Google Scholar 

  63. American Diabetes Association A.D., Diagnosis and classification of diabetes mellitus. Diabetes Care 33(Suppl 1), S62–S69 (2010). https://doi.org/10.2337/dc10-S062

    Article  Google Scholar 

  64. WHO Definition and diagnosis of diabetes mellitus and intermediate hyperglycaemia. (WHO, Geneva, Switzerland, 2013)

  65. F. Navab-Moghadam, M. Sedighi, M.E. Khamseh, F. Alaei-Shahmiri, M. Talebi, S. Razavi, N. Amirmozafari, The association of type II diabetes with gut microbiota composition. Microb. Pathog. 110, 630–636 (2017). https://doi.org/10.1016/j.micpath.2017.07.034

    Article  PubMed  CAS  Google Scholar 

  66. H. Wu, E. Esteve, V. Tremaroli, M.T. Khan, R. Caesar, L. Mannerås-Holm, M. Ståhlman, L.M. Olsson, M. Serino, M. Planas-Fèlix, G. Xifra, J.M. Mercader, D. Torrents, R. Burcelin, W. Ricart, R. Perkins, J.M. Fernàndez-Real, F. Bäckhed, Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat. Med. 23, 850–858 (2017). https://doi.org/10.1038/nm.4345

    Article  PubMed  CAS  Google Scholar 

  67. M.C. De Goffau, S. Fuentes, B. Van Den Bogert, H. Honkanen, W.M. De Vos, G.W. Welling, H. Hyöty, H.J.M. Harmsen, Aberrant gut microbiota composition at the onset of type 1 diabetes in young children. Diabetologia 57, 1569–1577 (2014). https://doi.org/10.1007/s00125-014-3274-0

    Article  PubMed  CAS  Google Scholar 

  68. S. Hasan, V. Aho, P. Pereira, L. Paulin, S.B. Koivusalo, P. Auvinen, J.G. Eriksson, Gut microbiome in gestational diabetes: a cross-sectional study of mothers and offspring 5 years postpartum. Acta Obstet. Gynecol. Scand. 97, 38–46 (2018). https://doi.org/10.1111/aogs.13252

    Article  PubMed  CAS  Google Scholar 

  69. N. Larsen, F.K. Vogensen, F.W.J. Van Den Berg, D.S. Nielsen, A.S. Andreasen, B.K. Pedersen, W.A. Al-Soud, S.J. Sørensen, L.H. Hansen, M. Jakobsen, Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5, e9085 (2010). https://doi.org/10.1371/journal.pone.0009085

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. D. Ríos-Covián, P. Ruas-Madiedo, A. Margolles, M. Gueimonde, C.G. de Los Reyes-Gavilán, N. Salazar, Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol. 7, 185 (2016). https://doi.org/10.3389/fmicb.2016.00185

    Article  PubMed  PubMed Central  Google Scholar 

  71. Z. Gao, J. Yin, J. Zhang, R.E. Ward, R.J. Martin, M. Lefevre, W.T. Cefalu, J. Ye, Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58, 1509–1517 (2009). https://doi.org/10.2337/db08-1637

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. H.V. Lin, A. Frassetto, E.J. Kowalik, A.R. Nawrocki, M.M. Lu, J.R. Kosinski, J.A. Hubert, D. Szeto, X. Yao, G. Forrest, D.J. Marsh, Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS ONE 7, e35240 (2012). https://doi.org/10.1371/journal.pone.0035240

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. R.J. Perry, L. Peng, N.A. Barry, G.W. Cline, D. Zhang, R.L. Cardone, K.F. Petersen, R.G. Kibbey, A.L. Goodman, G.I. Shulman, Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature 534, 213–217 (2016). https://doi.org/10.1038/nature18309

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. S. Devaraj, P. Hemarajata, J. Versalovic, The human gut microbiome and body metabolism: Implications for obesity and diabetes. Clin. Chem. 59, 617–628 (2013)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. M.A.R. Vinolo, H.G. Rodrigues, R.T. Nachbar, R. Curi, Regulation of inflammation by short chain fatty acids. Nutrients 3, 858–876 (2011)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. A. Vrieze, E. Van Nood, F. Holleman, J. Salojärvi, R.S. Kootte, J.F.W.M. Bartelsman, G.M. Dallinga-Thie, M.T. Ackermans, M.J. Serlie, R. Oozeer, M. Derrien, A. Druesne, J.E.T. Van Hylckama Vlieg, V.W. Bloks, A.K. Groen, H.G.H.J. Heilig, E.G. Zoetendal, E.S. Stroes, W.M. De Vos, J.B.L. Hoekstra, M. Nieuwdorp, Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913–6.e7 (2012). https://doi.org/10.1053/j.gastro.2012.06.031

    Article  PubMed  CAS  Google Scholar 

  77. P.D. Cani, N.M. Delzenne, The role of the gut microbiota in energy metabolism and metabolic disease. Curr. Pharm. Des. 15, 1546–1558 (2009). https://doi.org/10.2174/138161209788168164

    Article  PubMed  CAS  Google Scholar 

  78. P.D. Cani, S. Possemiers, T. Van De Wiele, Y. Guiot, A. Everard, O. Rottier, L. Geurts, D. Naslain, A. Neyrinck, D.M. Lambert, G.G. Muccioli, N.M. Delzenne, Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58, 1091–1103 (2009). https://doi.org/10.1136/gut.2008.165886

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. S. Hædersdal, A. Lund, F.K. Knop, T. Vilsbøll, The role of glucagon in the pathophysiology and treatment of type 2 diabetes. Mayo Clin. Proc. 93, 217–239 (2018). https://doi.org/10.1016/j.mayocp.2017.12.003

    Article  PubMed  CAS  Google Scholar 

  80. C.S. Marathe, C.K. Rayner, K.L. Jones, M. Horowitz, Relationships between gastric emptying, postprandial glycemia, and incretin hormones. Diabetes Care. 36, 1396–1405 (2013). https://doi.org/10.2337/dc12-1609

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. G.S. Papaetis, Incretin-based therapies in prediabetes: Current evidence and future perspectives. World J. Diabetes 5, 817–834 (2014). https://doi.org/10.4239/wjd.v5.i6.817

    Article  PubMed  PubMed Central  Google Scholar 

  82. J. Bland, Intestinal microbiome, akkermansia muciniphila, and medical nutrition therapy. Integr. Med. (Encinitas). 15, 14–16 (2016). https://doi.org/10.1136/gutjnl-2015-310904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. K. Forslund, F. Hildebrand, T. Nielsen, G. Falony, E. Le Chatelier, S. Sunagawa, E. Prifti, S. Vieira-Silva, V. Gudmundsdottir, H. Krogh Pedersen, M. Arumugam, K. Kristiansen, A. Yvonne Voigt, H. Vestergaard, R. Hercog, P. Igor Costea, J. Roat Kultima, J. Li, T. Jørgensen, F. Levenez, J. Dore, H. Bjørn Nielsen, S. Brunak, J. Raes, T. Hansen, J. Wang, S. Dusko Ehrlich, P. Bork, O. Pedersen, Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528, 262–266 (2015). https://doi.org/10.1038/nature15766

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. N.M. Maruthur, E. Tseng, S. Hutfless, L.M. Wilson, C. Suarez-Cuervo, Z. Berger, Y. Chu, E. Iyoha, J.B. Segal, S. Bolen, Diabetes medications as monotherapy or metformin-based combination therapy for type 2 diabetes: A systematic review and meta-analysis. Ann. Intern. Med. 164, 740–751 (2016)

    Article  PubMed  Google Scholar 

  85. D. Kopelman, I. Caterson, J. Michael, W. HD, Clinical obesity in adults and children. (2009)

  86. K.M. Levri, E. Slaymaker, A. Last, J. Yeh, J. Ference, F. D’Amico, S.A. Wilson, Metformin as treatment for overweight and obese adults: A systematic review. Ann. Fam. Med. 3, 457–461 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  87. M.P. van der Aa, M.A.J. Elst, E.M.W. van de Garde, E.G.A.H. van Mil, C.A.J. Knibbe, M.M.J. van der Vorst, Long-term treatment with metformin in obese, insulin-resistant adolescents: results of a randomized double-blinded placebo-controlled trial. Nutr. Diabetes 6, e228 (2016). https://doi.org/10.1038/nutd.2016.37

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. U. Uusitalo, X. Liu, J. Yang, C.A. Aronsson, S. Hummel, M. Butterworth, Å. Lernmark, M. Rewers, W. Hagopian, J.-X. She, O. Simell, J. Toppari, A.G. Ziegler, B. Akolkar, J. Krischer, J.M. Norris, S.M. Virtanen; TEDDY Study Group, Association of early exposure of probiotics and islet autoimmunity in the TEDDY study. JAMA Pediatr. 33612, 1–9 (2015). https://doi.org/10.1001/jamapediatrics.2015.2757

    Article  Google Scholar 

  89. W.-H. Lee, P.-C. Hsu, C.-Y. Chu, H.-M. Su, C.-S. Lee, H.-W. Yen, T.-H. Lin, W.-C. Voon, W.-T. Lai, S.-H. Sheu, Cardiovascular events in patients with atherothrombotic disease: a population-based longitudinal study in Taiwan. PLoS. One. 9, e92577 (2014). https://doi.org/10.1371/journal.pone.0092577

    Article  PubMed  PubMed Central  Google Scholar 

  90. C. Gazzaruso, S.B. Solerte, E. De Amici, M. Mancini, A. Pujia, P. Fratino, A. Giustina, A. Garzaniti, Association of the metabolic syndrome and insulin resistance with silent myocardial ischemia in patients with type 2 diabetes mellitus. Am. J. Cardiol. 97, 236–239 (2006). https://doi.org/10.1016/j.amjcard.2005.07.133

    Article  PubMed  CAS  Google Scholar 

  91. C. Gazzaruso, A. Coppola, A. Giustina, Erectile dysfunction and coronary artery disease in patients with diabetes. Curr. Diabetes Rev. 7, 143–147 (2011). https://doi.org/10.2174/157339911794940693

    Article  PubMed  Google Scholar 

  92. G.S. Crowther, M.H. Wilcox, Antibiotic therapy and Clostridium difficile infection -primum non nocere - first do no harm. Infect. Drug Resist. 8, 333–337 (2015). https://doi.org/10.2147/IDR.S87224

    Article  PubMed  PubMed Central  Google Scholar 

  93. W.H.W. Tang, Z. Wang, D.J. Kennedy, Y. Wu, J.A. Buffa, B. Agatisa-Boyle, X.S. Li, B.S. Levison, S.L. Hazen, Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ. Res. 116, 448–455 (2015). https://doi.org/10.1161/CIRCRESAHA.116.305360

    Article  PubMed  CAS  Google Scholar 

  94. R.A. Koeth, Z. Wang, B.S. Levison, J.A. Buffa, E. Org, B.T. Sheehy, E.B. Britt, X. Fu, Y. Wu, L. Li, J.D. Smith, J.A. Didonato, J. Chen, H. Li, G.D. Wu, J.D. Lewis, M. Warrier, J.M. Brown, R.M. Krauss, W.H.W. Tang, F.D. Bushman, A.J. Lusis, S.L. Hazen, Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 19, 576–585 (2013). https://doi.org/10.1038/nm.3145

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. R.A. Koeth, B.S. Levison, M.K. Culley, J.A. Buffa, Z. Wang, J.C. Gregory, E. Org, Y. Wu, L. Li, J.D. Smith, W.H.W. Tang, J.A. Didonato, A.J. Lusis, S.L. Hazen, γ-butyrobetaine is a proatherogenic intermediate in gut microbial metabolism of L-carnitine to TMAO. Cell. Metab. 20, 799–812 (2014). https://doi.org/10.1016/j.cmet.2014.10.006

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. W.H.W. Tang, Z. Wang, Y. Fan, B. Levison, J.E. Hazen, L.M. Donahue, Y. Wu, S.L. Hazen, Prognostic value of elevated levels of intestinal microbe-generated metabolite trimethylamine-N-oxide in patients with heart failure: Refining the gut hypothesis. J. Am. Coll. Cardiol. 64, 1908–1914 (2014)

    Article  PubMed  CAS  Google Scholar 

  97. W.P. Fay, Homocysteine and thrombosis: Guilt by association? Blood 119, 2977–2978 (2012)

    Article  PubMed  CAS  Google Scholar 

  98. R. Ostan, M.C. Béné, L. Spazzafumo, A. Pinto, L.M. Donini, F. Pryen, Z. Charrouf, L. Valentini, H. Lochs, I. Bourdel-Marchasson, C. Blanc-Bisson, F. Buccolini, P. Brigidi, C. Franceschi, P.A. d’Alessio, Impact of diet and nutraceutical supplementation on inflammation in elderly people. Results from the RISTOMED study, an open-label randomized control trial. Clin. Nutr. 35, 812–818 (2016). https://doi.org/10.1016/j.clnu.2015.06.010

    Article  PubMed  CAS  Google Scholar 

  99. J.L. Griffin, X. Wang, E. Stanley, Does Our gut microbiome predict cardiovascular risk? A review of the evidence from metabolomics. Circ. Cardiovasc Genet. 8, 187–191 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. J. Joseph, J. Loscalzo, Nutri(meta)genetics and cardiovascular disease: novel concepts in the interaction of diet and genomic variation. Curr. Atherosler Rep. 17, 505 (2015)

    Google Scholar 

  101. W.H.W. Tang, S.L. Hazen, The contributory role of gut microbiota in cardiovascular disease. J. Clin. Invest. 124, 4204–4211 (2014). https://doi.org/10.1172/JCI72331

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. T. Yang, M.M. Santisteban, V. Rodriguez, E. Li, N. Ahmari, J.M. Carvajal, M. Zadeh, M. Gong, Y. Qi, J. Zubcevic, B. Sahay, C.J. Pepine, M.K. Raizada, M. Mohamadzadeh, Gut dysbiosis is linked to hypertension. Hypertension 65, 1331–1340 (2015). https://doi.org/10.1161/HYPERTENSIONAHA.115.05315

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. X.T. Gan, G. Ettinger, C.X. Huang, J.P. Burton, J.V. Haist, V. Rajapurohitam, J.E. Sidaway, G. Martin, G.B. Gloor, J.R. Swann, G. Reid, M. Karmazyn, Probiotic administration attenuates myocardial hypertrophy and heart failure after myocardial infarction in the rat. Circ. Hear. Fail. 7, 491–499 (2014). https://doi.org/10.1161/CIRCHEARTFAILURE.113.000978

    Article  Google Scholar 

  104. C.S. Hampe, C.L. Roth, Probiotic strains and mechanistic insights for the treatment of type 2 diabetes. Endocrine 58, 207–227 (2017). https://doi.org/10.1007/s12020-017-1433-z

    Article  PubMed  CAS  Google Scholar 

  105. M.H. Floch, Probiotics and prebiotics. Gastroenterol. Hepatol. (N. Y) 10, 680–681 (2014)

    Google Scholar 

  106. M.C. Dao, A. Everard, J. Aron-Wisnewsky, N. Sokolovska, E. Prifti, E.O. Verger, B.D. Kayser, F. Levenez, J. Chilloux, L. Hoyles, M.-E. Dumas, S.W. Rizkalla, J. Doré, P.D. Cani, K. Clément, Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 65, 426–436 (2016)

    Article  PubMed  CAS  Google Scholar 

  107. C. Chevalier, O. Stojanović, D.J. Colin, N. Suarez-Zamorano, V. Tarallo, C. Veyrat-Durebex, D. Rigo, S. Fabbiano, A. Stevanović, S. Hagemann, X. Montet, Y. Seimbille, N. Zamboni, S. Hapfelmeier, M. Trajkovski, Gut microbiota orchestrates energy homeostasis during cold. Cell 163, 1360–1374 (2015). https://doi.org/10.1016/j.cell.2015.11.004

    Article  PubMed  CAS  Google Scholar 

  108. L.J. Cohen, D. Esterhazy, S.-H. Kim, C. Lemetre, R.R. Aguilar, E.A. Gordon, A.J. Pickard, J.R. Cross, A.B. Emiliano, S.M. Han, J. Chu, X. Vila-Farres, J. Kaplitt, A. Rogoz, P.Y. Calle, C. Hunter, J.K. Bitok, S.F. Brady, Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature 549, 48–53 (2017). https://doi.org/10.1038/nature23874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. M. Mimee, R.J. Citorik, T.K. Lu, Microbiome therapeutics—Advances and challenges. Adv. Drug. Deliv. Rev. 105, 44–54 (2016)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Z.Z.R. Hamady, N. Scott, M.D. Farrar, M. Wadhwa, P. Dilger, T.R. Whitehead, R. Thorpe, K.T. Holland, J.P.A. Lodge, S.R. Carding, Treatment of colitis with a commensal gut bacterium engineered to secrete human tgf-β1 under the control of dietary xylan 1. Inflamm. Bowel. Dis. 17, 1925–1935 (2011). https://doi.org/10.1002/ibd.21565

    Article  PubMed  Google Scholar 

  111. K. Vandenbroucke, H. De Haard, E. Beirnaert, T. Dreier, M. Lauwereys, L. Huyck, J. Van Huysse, P. Demetter, L. Steidler, E. Remaut, C. Cuvelier, P. Rottiers, Orally administered L. lactis secreting an anti-TNF Nanobody demonstrate efficacy in chronic colitis. Mucosal Immunol. 3, 49–56 (2010). https://doi.org/10.1038/mi.2009.116

    Article  PubMed  CAS  Google Scholar 

  112. Z.Z.R. Hamady, N. Scott, M.D. Farrar, J.P.A. Lodge, K.T. Holland, T. Whitehead, S.R. Carding, Xylan-regulated delivery of human keratinocyte growth factor-2 to the inflamed colon by the human anaerobic commensal bacterium Bacteroides ovatus. Gut 59, 461–469 (2010)

    Article  PubMed  CAS  Google Scholar 

  113. J.P. Motta, L.G. Bermúdez-Humarán, C. Deraison, L. Martin, C. Rolland, P. Rousset, J. Boue, G. Dietrich, K. Chapman, P. Kharrat, J.P. Vinel, L. Alric, E. Mas, J.M. Sallenave, P. Langella, N. Vergnolle, Food-grade bacteria expressing elafin protect against inflammation and restore colon homeostasis. Sci. Transl. Med. 4, 158ra144 (2012). https://doi.org/10.1126/scitranslmed.3004212

    Article  PubMed  CAS  Google Scholar 

  114. G.R. Gibson, H.M. Probert, J.Van Loo, R.A. Rastall, M.B. Roberfroid, Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr. Res. Rev. 17, 259 (2004). https://doi.org/10.1079/NRR200479

    Article  PubMed  CAS  Google Scholar 

  115. J. Slavin, Fiber and prebiotics: mechanisms and health benefits. Nutrients 5, 1417–1435 (2013). https://doi.org/10.3390/nu5041417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. M. De Vrese, J. Schrezenmeir, Probiotics, prebiotics, and synbiotics. Adv. Biochem. Eng. Biotechnol. 111, 1–66 (2008)

    PubMed  Google Scholar 

  117. B.C. Tungland, D. Meyer, Nondigestible oligo- and polysaccharides (dietary fiber): Their physiology and role in human health and food. Compr. Rev. Food Sci. Food Saf. 1, 90–109 (2002). https://doi.org/10.1111/j.1541-4337.2002.tb00009.x

    Article  Google Scholar 

  118. Z. Wang, E. Klipfell, B.J. Bennett, R. Koeth, B.S. Levison, B. Dugar, A.E. Feldstein, E.B. Britt, X. Fu, Y.M. Chung, Y. Wu, P. Schauer, J.D. Smith, H. Allayee, W.H.W. Tang, J.A. Didonato, A.J. Lusis, S.L. Hazen, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57–65 (2011). https://doi.org/10.1038/nature09922

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. A. Coppola, L. Sasso, A. Bagnasco, A. Giustina, C. Gazzaruso, The role of patient education in the prevention and management of type 2 diabetes: an overview. Endocrine 53, 18–27 (2016)

    Article  PubMed  CAS  Google Scholar 

  120. V. Tosti, B. Bertozzi, L. Fontana, Health Benefits of the Mediterranean Diet: Metabolic and Molecular Mechanisms. J Gerontol A Biol Sci Med Sci. 73, 318–326 (2018)

    Article  PubMed  Google Scholar 

  121. T.T.B. Nguyen, Y.Y. Jin, H.J. Chung, S.T. Hong, Pharmabiotics as an emerging medication for metabolic syndrome and its related diseases. Molecules 22(10), E1795 (2017)

    Article  PubMed  Google Scholar 

  122. R.E. Ley, D.A. Peterson, J.I. Gordon, Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837–848 (2006). https://doi.org/10.1016/J.CELL.2006.02.017

    Article  PubMed  CAS  Google Scholar 

  123. R.E. Ley, F. Bäckhed, P. Turnbaugh, C.A. Lozupone, R.D. Knight, J.I. Gordon, Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. U. S. A. 102, 11070–11075 (2005). https://doi.org/10.1073/pnas.0504978102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. A.L. Komaroff, The microbiome and risk for obesity and diabetes. JAMA 317, 355 (2017). https://doi.org/10.1001/jama.2016.20099

    Article  PubMed  Google Scholar 

  125. S.K. Mazmanian, J.L. Round, D.L. Kasper, A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620–625 (2008). https://doi.org/10.1038/nature07008

    Article  PubMed  CAS  Google Scholar 

  126. L. Wen, R.E. Ley, P.Y. Volchkov, P.B. Stranges, L. Avanesyan, A.C. Stonebraker, C. Hu, F.S. Wong, G.L. Szot, J.A. Bluestone, J.I. Gordon, A.V. Chervonsky, Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455, 1109–1113 (2008). https://doi.org/10.1038/nature07336

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Y.S. Kim, J.A. Milner, Dietary modulation of colon cancer risk. J. Nutr. 137, 2576S–2579S (2007)

    Article  PubMed  Google Scholar 

  128. S.K.P. Lau, P.C.Y. Woo, G.K.S. Woo, A.M.Y. Fung, M.K.M. Wong, K.-M. Chan, D.M.W. Tam, K.-Y. Yuen, Eggerthella hongkongensis sp. nov. and eggerthella sinensis sp. nov., two novel Eggerthella species, account for half of the cases of Eggerthella bacteremia. Diagn. Microbiol. Infect. Dis. 49, 255–263 (2004). https://doi.org/10.1016/j.diagmicrobio.2004.04.012

    Article  PubMed  Google Scholar 

  129. M. Kraatz, R.J. Wallace, L. Svensson, Olsenella umbonata sp. nov., a microaerotolerant anaerobic lactic acid bacterium from the sheep rumen and pig jejunum, and emended descriptions of Olsenella, Olsenella uli and Olsenella profusa. Int. J. Syst. Evol. Microbiol. 61, 795–803 (2011). https://doi.org/10.1099/ijs.0.022954-0

    Article  PubMed  CAS  Google Scholar 

  130. S.K. Lau, P.C. Woo, A.M. Fung, K. Chan, G.K. Woo, K. Yuen, Anaerobic, non-sporulating, Gram-positive bacilli bacteraemia characterized by 16S rRNA gene sequencing. J. Med. Microbiol. 53, 1247–1253 (2004). https://doi.org/10.1099/jmm.0.45803-0

    Article  PubMed  CAS  Google Scholar 

  131. A. Finamore, M. Palmery, S. Bensehaila, I. Peluso, Antioxidant, immunomodulating, and microbial-modulating activities of the sustainable and ecofriendly Spirulina. Oxid. Med. Cell Longev. 2017, 3247528 (2017). https://doi.org/10.1155/2017/3247528. 1–14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. D.J. Hampson, T. La, N.D. Phillips, Emergence of Brachyspira species and strains: reinforcing the need for surveillance. Porc. Heal. Manag. 1, 8 (2015). https://doi.org/10.1186/s40813-015-0002-1

    Article  Google Scholar 

  133. M.Y. Galperin, New feel for new phyla. Environ. Microbiol. 10, 1927–1933 (2008). https://doi.org/10.1111/j.1462-2920.2008.01699.x

    Article  PubMed  PubMed Central  Google Scholar 

  134. M. Yamauchi, P. Lochhead, T. Morikawa, C. Huttenhower, A.T. Chan, E. Giovannucci, C. Fuchs, S. Ogino, Colorectal cancer: a tale of two sides or a continuum? Gut 61, 794–797 (2012). https://doi.org/10.1136/gutjnl-2012-302014

    Article  PubMed  PubMed Central  Google Scholar 

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  1. These authors contributed equally: Alessia Pascale, Nicoletta Marchesi.

Authors and Affiliations

  1. Department of Drug Sciences, Pharmacology section, University of Pavia, 27100, Pavia, Italy

    Alessia Pascale, Nicoletta Marchesi, Cristina Marelli & Stefano Govoni

  2. Diabetes and endocrine and metabolic diseases Unit and the Centre for Applied Clinical Research (Ce.R.C.A.) Clinical Institute “Beato Matteo” (Hospital Group San Donato), 27029, Vigevano, Italy

    Adriana Coppola & Carmine Gazzaruso

  3. Department of Biomedical Sciences for Health, University of Milan, 20100, Milan, Italy

    Livio Luzi

  4. Metabolism Research Center, IRCCS Policlinico San Donato, 20097, San Donato Milanese, Italy

    Livio Luzi

  5. Chair of Endocrinology San Raffaele Vita-Salute University, Milan, Italy

    Andrea Giustina

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Pascale, A., Marchesi, N., Marelli, C. et al. Microbiota and metabolic diseases. Endocrine 61, 357–371 (2018). https://doi.org/10.1007/s12020-018-1605-5

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