Systematic review: Microbial dysbiosis and nonalcoholic fatty liver disease

Alimentary Pharmacology and Therapeutics

Volumn 42, Issue 9, 2015, Pages 1051-1063

  Wieland, A ^a   Frank, D N ^b   Harnke, B ^b   Bambha, K ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINE;

ARTICLE; DATA ANALYSIS; DISEASE ACTIVITY; DISEASE ASSOCIATION; DYSBIOSIS; HUMAN; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; METAGENOMICS; MICROBIOME; MOLECULAR PATHOLOGY; NONALCOHOLIC FATTY LIVER; OBESITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMATIC REVIEW; ANIMAL; ANIMAL MODEL; INTESTINE; METAGENOME; MICROBIOLOGY; MICROFLORA; PATHOPHYSIOLOGY;

ANIMALS; DYSBIOSIS; HUMANS; INTESTINES; METAGENOME; MICROBIOTA; MODELS, ANIMAL; NON-ALCOHOLIC FATTY LIVER DISEASE;

EID: 84942991239     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.13376     Document Type: Article

References (81)

1. Sleisenger MH, Feldman M, Friedman LS, Brandt LJ,. Sleisenger and Fordtran's Gastrointestinal and Liver Disease: Pathophysiology, Diagnosis, Management, 9th ed. Philadelphia, PA: Saunders/Elsevier, 2010.
2. Turnbaugh PJ, Gordon JI,. The core gut microbiome, energy balance and obesity. J Physiol 2009; 587: 4153-8.
3. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI,. The human microbiome project. Nature 2007; 449: 804-10.
4. Hooper LV, Falk PG, Gordon JI,. Analyzing the molecular foundations of commensalism in the mouse intestine. Curr Opin Microbiol 2000; 3: 79-85.
5. Hooper LV, Littman DR, Macpherson AJ,. Interactions between the microbiota and the immune system. Science 2012; 336: 1268-73.
6. Hooper LV, Midtvedt T, Gordon JI,. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002; 22: 283-307.
7. Round JL, Mazmanian SK,. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9: 313-23.
8. Kamada N, Seo SU, Chen GY, Nunez G,. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013; 13: 321-35.
9. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI,. Human nutrition, the gut microbiome and the immune system. Nature 2011; 474: 327-36.
10. Frank DN, Pace NR,. Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 2008; 24: 4-10.
11. MacDonald TT, Carter PB,. Requirement for a bacterial flora before mice generate cells capable of mediating the delayed hypersensitivity reaction to sheep red blood cells. J Immunol 1979; 122: 2624-9.
12. Shanahan F,. The host-microbe interface within the gut. Best Pract Res Clin Gastroenterol 2002; 16: 915-31.
13. Okada Y, Setoyama H, Matsumoto S, et al., Effects of fecal microorganisms and their chloroform-resistant variants derived from mice, rats, and humans on immunological and physiological characteristics of the intestines of ex-germfree mice. Infect Immun 1994; 62: 5442-6.
14. O'Hara AM, Shanahan F,. The gut flora as a forgotten organ. EMBO Rep 2006; 7: 688-93.
15. Frank DN, Zhu W, Sartor RB, Li E,. Investigating the biological and clinical significance of human dysbioses. Trends Microbiol 2011; 19: 427-34.
16. Theriot CM, Koenigsknecht MJ, Carlson PE Jr, et al., Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 2014; 5: 3114.
17. Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, Young VB,. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes 2011; 2: 145-58.
18. Ananthakrishnan AN,. Clostridium difficile infection: epidemiology, risk factors and management. Nat Rev Gastroenterol Hepatol 2011; 8: 17-26.
19. Vernon G, Baranova A, Younossi ZM,. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 2011; 34: 274-85.
20. Williams CD, Stengel J, Asike MI, et al., Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 2011; 140: 124-31.
21. Ong JP, Younossi ZM,. Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis 2007; 11: 1-16, vii.
22. Abu-Shanab A, Quigley EM,. The role of the gut microbiota in nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol 2010; 7: 691-701.
23. Compare D, Coccoli P, Rocco A, et al., Gut-liver axis: the impact of gut microbiota on non alcoholic fatty liver disease. Nutr Metab Cardiovasc Dis 2012; 22: 471-6.
24. Schnabl B, Brenner DA,. Interactions between the intestinal microbiome and liver diseases. Gastroenterology 2014; 146: 1513-24.
25. Wilson KH, Blitchington RB,. Human colonic biota studied by ribosomal DNA sequence analysis. Appl Environ Microbiol 1996; 62: 2273-8.
26. Eckburg PB, Bik EM, Bernstein CN, et al., Diversity of the human intestinal microbial flora. Science 2005; 308: 1635-8.
27. Woese CR, Kandler O, Wheelis ML,. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 1990; 87: 4576-9.
28. Pace NR,. A molecular view of microbial diversity and the biosphere. Science 1997; 276: 734-40.
29. Pace NR, Sapp J, Goldenfeld N,. Phylogeny and beyond: scientific, historical, and conceptual significance of the first tree of life. Proc Natl Acad Sci USA 2012; 109: 1011-8.
30. Turnbaugh PJ, Hamady M, Yatsunenko T, et al., A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-4.
31. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR,. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007; 104: 13780-5.
32. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486: 207-14.
33. Scanlan PD, Shanahan F, O'Mahony C, Marchesi JR,. Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn's disease. J Clin Microbiol 2006; 44: 3980-8.
34. Ley RE, Turnbaugh PJ, Klein S, Gordon JI,. Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444: 1022-3.
35. Ley RE,. Obesity and the human microbiome. Curr Opin Gastroenterol 2010; 26: 5-11.
36. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI,. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 2005; 102: 11070-5.
37. Backhed F, Ding H, Wang T, et al., The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101: 15718-23.
38. Zupancic ML, Cantarel BL, Liu Z, et al., Analysis of the gut microbiota in the old order Amish and its relation to the metabolic syndrome. PLoS ONE 2012; 7: e43052.
39. Kelly CJ, Colgan SP, Frank DN,. Of microbes and meals: the health consequences of dietary endotoxemia. Nutr Clin Pract 2012; 27: 215-25.
40. DiBaise JK, Frank DN, Mathur R,. Impact of the gut microbiota on the development of obesity: current concepts. Am J Gastroenterol 2012; 1: 22-7.
41. Delzenne NM, Cani PD,. Interaction between obesity and the gut microbiota: relevance in nutrition. Annu Rev Nutr 2011; 31: 15-31.
42. Crane JK, Byrd IW, Boedeker EC,. Virulence inhibition by zinc in shiga-toxigenic Escherichia coli. Infect Immun 2011; 79: 1696-705.
43. Tremaroli V, Backhed F,. Functional interactions between the gut microbiota and host metabolism. Nature 2012; 489: 242-9.
44. Zvenigorodskaja LA, Cherkashova EA, Samsonova NG, Nilova TV, Seliverstova SJ, Kchomeriki SG,. The role of products of colon microflora in pathogenesis of nonalcoholic fatty liver disease. J Diabetes 2011; 3: 197-8.
45. Schwiertz A, Taras D, Schafer K, et al., Microbiota and SCFA in lean and overweight healthy subjects. Obesity 2010; 18: 190-5.
46. Duncan SH, Lobley GE, Holtrop G, et al., Human colonic microbiota associated with diet, obesity and weight loss. International Journal of Obesity 2008; 32: 1720-4.
47. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE,. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 2007; 73: 1073-8.
48. Finucane MM, Sharpton TJ, Laurent TJ, Pollard KS,. A taxonomic signature of obesity in the microbiome? Getting to the guts of the matter. PLoS ONE 2014; 9: e84689.
49. Marchesini G, Brizi M, Bianchi G, et al., Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes 2001; 50: 1844-50.
50. Cano PG, Santacruz A, Trejo FM, Sanz Y,. Bifidobacterium CECT 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet fed mice. Obesity 2013; 21: 2310-21.
51. Zeng H, Liu J, Jackson MI, Zhao FQ, Yan L, Combs GF Jr,. Fatty liver accompanies an increase in lactobacillus species in the hind gut of C57BL/6 mice fed a high-fat diet. J Nutr 2013; 143: 627-31.
52. Henao-Mejia J, Elinav E, Jin CC, et al., Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482: 179-U167.
53. Le Roy T, Llopis M, Lepage P, et al., Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 2013; 62: 1787-94.
54. Elinav E, Strowig T, Kau AL, et al., NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145: 745-57.
55. Spencer MD, Hamp TJ, Reid RW, Fischer LM, Zeisel SH, Fodor AA,. Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology 2011; 140: 976-86.
56. Zhu L, Baker SS, Gill C, et al., Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 2013; 57: 601-9.
57. Mouzaki M, Comelli E, Arendt B, et al., Intestinal microbiota in patients with non-alcoholic fatty liver disease. Hepatology 2013; 58: 120-7.
58. Raman M, Ahmed I, Gillevet PM, et al., Fecal microbiome and volatile organic compound metabolome in obese human beings with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2013; 11: 868-75.
59. Wong VWS, Tse CH, Lam TTY, et al., Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis-a longitudinal study. PLoS ONE 2013; 8: e62885.
60. Buchman AL, Dubin MD, Moukarzel AA, et al., Choline deficiency: a cause of hepatic steatosis during parenteral nutrition that can be reversed with intravenous choline supplementation. Hepatology (Baltimore, MD) 1995; 22: 1399-403.
61. Yuan J, Baker SS, Liu W, et al., Endotoxemia is not required in the pathogenesis of pediatric non-alcoholic steatohepatitis. J Gastroenterol Hepatol 2013; 29: 1292-8
62. Wong VW, Won GL, Chim AM, et al., Treatment of nonalcoholic steatohepatitis with probiotics. A proof-of-concept study. Ann Hepatol 2013; 12: 256-62.
63. Aron-Wisnewsky J, Gaborit B, Dutour A, Clement K,. Gut microbiota and non-alcoholic fatty liver disease: new insights. Clin Microbiol Infect 2013; 19: 338-48.
64. Vinolo MA, Rodrigues HG, Nachbar RT, Curi R,. Regulation of inflammation by short chain fatty acids. Nutrients 2011; 3: 858-76.
65. Zeisel SH, da Costa KA,. Choline: an essential nutrient for public health. Nutr Rev 2009; 67: 615-23.
66. Dumas ME, Barton RH, Toye A, et al., Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc Natl Acad Sci USA 2006; 103: 12511-6.
67. Russell DW,. The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 2003; 72: 137-74.
68. Ridlon JM, Kang DJ, Hylemon PB,. Bile salt biotransformations by human intestinal bacteria. J Lipid Res 2006; 47: 241-59.
69. Sayin SI, Wahlstrom A, Felin J, et al., Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 2013; 17: 225-35.
70. Swann JR, Want EJ, Geier FM, et al., Systemic gut microbial modulation of bile acid metabolism in host tissue compartments. Proc Natl Acad Sci USA 2011; 108 (Suppl. 1): 4523-30.
71. Islam KB, Fukiya S, Hagio M, et al., Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. Gastroenterology 2011; 141: 1773-81.
72. Schaap FG, Trauner M, Jansen PL,. Bile acid receptors as targets for drug development. Nat Rev Gastroenterol Hepatol 2014; 11: 55-67.
73. Li Y, Jadhav K, Zhang Y,. Bile acid receptors in non-alcoholic fatty liver disease. Biochem Pharmacol 2013; 86: 1517-24.
74. McMahan RH, Wang XX, Cheng LL, et al., Bile acid receptor activation modulates hepatic monocyte activity and improves nonalcoholic fatty liver disease. J Biol Chem 2013; 288: 11761-70.
75. Jiang C, Xie C, Li F, et al., Intestinal farnesoid X receptor signaling promotes nonalcoholic fatty liver disease. J Clin Invest 2015; 125: 386-402.
76. Mudaliar S, Henry RR, Sanyal AJ, et al., Efficacy and safety of the farnesoid X receptor agonist obeticholic acid in patients with type 2 diabetes and nonalcoholic fatty liver disease. Gastroenterology 2013; 145: 574-82 e571.
77. Neuschwander-Tetri BA, Loomba R, Sanyal AJ, et al., Farnesoid X nuclear receptor ligand obeticholic acid for non-cirrhotic, non-alcoholic steatohepatitis (FLINT): a multicentre, randomised, placebo-controlled trial. Lancet 2014; 385: 956-65.
78. Artis D,. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008; 8: 411-20.
79. Miele L, Valenza V, La Torre G, et al., Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 2009; 49: 1877-87.
80. Li S, Wu WC, He CY, Han Z, Jin DY, Wang L,. Change of intestinal mucosa barrier function in the progress of non-alcoholic steatohepatitis in rats. World J Gastroenterol 2008; 14: 3254-8.
81. Gabele E, Dostert K, Hofmann C, et al., DSS induced colitis increases portal LPS levels and enhances hepatic inflammation and fibrogenesis in experimental NASH. J Hepatol 2011; 55: 1391-9.