Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 979515, 9 pages
http://dx.doi.org/10.1155/2015/979515
Review Article

Gut Microbiota: Association with NAFLD and Metabolic Disturbances

Department of Endocrinology, Diabetes and Metabolism, Centro Hospitalar São João, Institute for Research and Innovation in Health Sciences, Faculty of Medicine, University of Porto, Alameda Professor Hernâni Monteiro, 4200-319 Porto, Portugal

Received 3 November 2014; Accepted 7 January 2015

Academic Editor: Maria Carmen Collado

Copyright © 2015 E. Lau et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Sattar, E. Forrest, and D. Preiss, “Non-alcoholic fatty liver disease,” British Medical Journal, vol. 349, Article ID g4596, 2014. View at Publisher · View at Google Scholar
  2. G. Vernon, A. Baranova, and Z. M. Younossi, “Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults,” Alimentary Pharmacology & Therapeutics, vol. 34, no. 3, pp. 274–285, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Vuppalanchi and N. Chalasani, “Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: selected practical issues in their evaluation and management,” Hepatology, vol. 49, no. 1, pp. 306–317, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. J. K. Dowman, J. W. Tomlinson, and P. N. Newsome, “Pathogenesis of non-alcoholic fatty liver disease,” QJM, vol. 103, no. 2, pp. 71–83, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. C. P. Day and O. F. W. James, “Steatohepatitis: a tale of two ‘hits’?” Gastroenterology, vol. 114, no. 4, pp. 842–845, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Qin, R. Li, J. Raes et al., “A human gut microbial gene catalogue established by metagenomic sequencing,” Nature, vol. 464, no. 7285, pp. 59–65, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Prakash, L. Rodes, M. Coussa-Charley, and C. Tomaro-Duchesneau, “Gut microbiota: next frontier in understanding human health and development of biotherapeutics,” Biologics, vol. 5, pp. 71–86, 2011. View at Publisher · View at Google Scholar
  8. R. E. Ley, F. Bäckhed, P. Turnbaugh, C. A. Lozupone, R. D. Knight, and J. I. Gordon, “Obesity alters gut microbial ecology,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 31, pp. 11070–11075, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. R. E. Ley, P. J. Turnbaugh, S. Klein, and J. I. Gordon, “Microbial ecology: human gut microbes associated with obesity,” Nature, vol. 444, no. 7122, pp. 1022–1023, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Vijay-Kumar, J. D. Aitken, F. A. Carvalho et al., “Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5,” Science, vol. 328, no. 5975, pp. 228–231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Bäckhed, H. Ding, T. Wang et al., “The gut microbiota as an environmental factor that regulates fat storage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 44, pp. 15718–15723, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. W. Z. Mehal, “The Gordian Knot of dysbiosis, obesity and NAFLD,” Nature Reviews Gastroenterology and Hepatology, vol. 10, no. 11, pp. 637–644, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Compare, P. Coccoli, A. Rocco et al., “Gut-liver axis: the impact of gut microbiota on non alcoholic fatty liver disease,” Nutrition, Metabolism and Cardiovascular Diseases, vol. 22, no. 6, pp. 471–476, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. V. W.-S. Wong, C.-H. Tse, T. T.-Y. Lam et al., “Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis—a longitudinal study,” PLoS ONE, vol. 8, no. 4, Article ID e62885, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Zhu, S. S. Baker, C. Gill et al., “Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH,” Hepatology, vol. 57, no. 2, pp. 601–609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Raman, I. Ahmed, P. M. Gillevet et al., “Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease,” Clinical Gastroenterology and Hepatology, vol. 11, no. 7, pp. 868–875.e3, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. M. D. Spencer, T. J. Hamp, R. W. Reid, L. M. Fischer, S. H. Zeisel, and A. A. Fodor, “Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency,” Gastroenterology, vol. 140, no. 3, pp. 976–986, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Alisi, G. Bedogni, G. Baviera et al., “Randomised clinical trial: the beneficial effects of VSL#3 in obese children with non-alcoholic steatohepatitis,” Alimentary Pharmacology and Therapeutics, vol. 39, no. 11, pp. 1276–1285, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Malaguarnera, M. Vacante, T. Antic et al., “Bifidobacterium longum with fructo-oligosaccharides in patients with non alcoholic steatohepatitis,” Digestive Diseases and Sciences, vol. 57, no. 2, pp. 545–553, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. S. de Minicis, C. Rychlicki, L. Agostinelli et al., “Dysbiosis contributes to fibrogenesis in the course of chronic liver injury in mice,” Hepatology, vol. 59, no. 5, pp. 1738–1749, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Henao-Mejia, E. Elinav, C. Jin et al., “Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity,” Nature, vol. 482, no. 7384, pp. 179–185, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. T. le Roy, M. Llopis, P. Lepage et al., “Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice,” Gut, vol. 62, no. 12, pp. 1787–1794, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. N. de Wit, M. Derrien, H. Bosch-Vermeulen et al., “Saturated fat stimulates obesity and hepatic steatosis and affects gut microbiota composition by an enhanced overflow of dietary fat to the distal intestine,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 303, no. 5, pp. G589–G599, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. M.-E. Dumas, R. H. Barton, A. Toye et al., “Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 33, pp. 12511–12516, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. A. M. Neyrinck, S. Possemiers, W. Verstraete, F. de Backer, P. D. Cani, and N. M. Delzenne, “Dietary modulation of clostridial cluster XIVa gut bacteria (Roseburia spp.) by chitin-glucan fiber improves host metabolic alterations induced by high-fat diet in mice,” Journal of Nutritional Biochemistry, vol. 23, no. 1, pp. 51–59, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Ritze, G. Bárdos, A. Claus et al., “Lactobacillus rhamnosus GG protects against non-alcoholic fatty liver disease in mice,” PLoS ONE, vol. 9, no. 1, Article ID e80169, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Okubo, H. Sakoda, A. Kushiyama et al., “Lactobacillus casei strain shirota protects against nonalcoholic steatohepatitis development in a rodent model,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 305, no. 12, pp. G911–G918, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. X. Yin, J. Peng, L. Zhao et al., “Structural changes of gut microbiota in a rat non-alcoholic fatty liver disease model treated with a Chinese herbal formula,” Systematic and Applied Microbiology, vol. 36, no. 3, pp. 188–196, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. P. G. Cano, A. Santacruz, Á. Moya, and Y. Sanz, “Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity,” PLoS ONE, vol. 7, no. 7, Article ID e41079, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. B. D. Pachikian, A. Essaghir, J.-B. Demoulin et al., “Prebiotic approach alleviates hepatic steatosis: implication of fatty acid oxidative and cholesterol synthesis pathways,” Molecular Nutrition and Food Research, vol. 57, no. 2, pp. 347–359, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Wagnerberger, A. Spruss, G. Kanuri et al., “Toll-like receptors 1–9 are elevated in livers with fructose-induced hepatic steatosis,” British Journal of Nutrition, vol. 107, no. 12, pp. 1727–1738, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Mencin, J. Kluwe, and R. F. Schwabe, “Toll-like receptors as targets in chronic liver diseases,” Gut, vol. 58, no. 5, pp. 704–720, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Spruss, G. Kanuri, S. Wagnerberger, S. Haub, S. C. Bischoff, and I. Bergheim, “Toll-like receptor 4 is involved in the development of fructose-induced hepatic steatosis in mice,” Hepatology, vol. 50, no. 4, pp. 1094–1104, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. D. A. Brenner, E. Seki, K. Taura et al., “Non-alcoholic steatohepatitis-induced fibrosis: Toll-like receptors, reactive oxygen species and Jun N-terminal kinase,” Hepatology Research, vol. 41, no. 7, pp. 683–686, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. A. J. Wigg, I. C. Roberts-Thomson, R. B. Dymock, P. J. McCarthy, R. H. Grose, and A. G. Cummins, “The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitis,” Gut, vol. 48, no. 2, pp. 206–211, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Miele, V. Valenza, G. la Torre et al., “Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease,” Hepatology, vol. 49, no. 6, pp. 1877–1887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. D. P. Clark, “The fermentation pathways of Escherichia coli,” FEMS Microbiology Reviews, vol. 63, no. 3, pp. 223–234, 1989. View at Google Scholar · View at Scopus
  38. T. Sarkola and C. J. P. Eriksson, “Effect of 4-methylpyrazole on endogenous plasma ethanol and methanol levels in humans,” Alcoholism: Clinical and Experimental Research, vol. 25, no. 4, pp. 513–516, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. P. D. Cani, R. Bibiloni, C. Knauf et al., “Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice,” Diabetes, vol. 57, no. 6, pp. 1470–1481, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Peng, Z.-R. Li, R. S. Green, I. R. Holzman, and J. Lin, “Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers,” Journal of Nutrition, vol. 139, no. 9, pp. 1619–1625, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. W. Scheppach, P. Bartram, A. Richter et al., “Effect of short-chain fatty acids on the human colonic mucosa in vitro,” Journal of Parenteral and Enteral Nutrition, vol. 16, no. 1, pp. 43–48, 1992. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Lee, S.-W. Hong, E.-J. Rhee, and W.-Y. Lee, “GLP-1 receptor agonist and non-alcoholic fatty liver disease,” Diabetes & Metabolism Journal, vol. 36, no. 4, pp. 262–267, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. Z. M. Younossi, M. Stepanova, M. Afendy et al., “Changes in the prevalence of the most common causes of chronic liver diseases in the United States from 1988 to 2008,” Clinical Gastroenterology and Hepatology, vol. 9, no. 6, pp. 524e.1–530.e1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. P. J. Turnbaugh, R. E. Ley, M. A. Mahowald, V. Magrini, E. R. Mardis, and J. I. Gordon, “An obesity-associated gut microbiome with increased capacity for energy harvest,” Nature, vol. 444, no. 7122, pp. 1027–1031, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Paschos and K. Paletas, “Non alcoholic fatty liver disease and metabolic syndrome,” Hippokratia, vol. 13, no. 1, pp. 9–19, 2009. View at Google Scholar · View at Scopus
  46. P. D. Cani, J. Amar, M. A. Iglesias et al., “Metabolic endotoxemia initiates obesity and insulin resistance,” Diabetes, vol. 56, no. 7, pp. 1761–1772, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. J.-M. Sabaté, P. Jouët, F. Harnois et al., “High prevalence of small intestinal bacterial overgrowth in patients with morbid obesity: a contributor to severe hepatic steatosis,” Obesity Surgery, vol. 18, no. 4, pp. 371–377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Kirsch, V. Clarkson, R. C. Verdonk et al., “Rodent nutritional model of steatohepatitis: effects of endotoxin (lipopolysaccharide) and tumor necrosis factor alpha deficiency,” Journal of Gastroenterology and Hepatology, vol. 21, no. 1, part 1, pp. 174–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. S. H. Zeisel, K. A. DaCosta, M. Youssef, and S. Hensey, “Conversion of dietary choline to trimethylamine and dimethylamine in rats: dose-response relationship,” Journal of Nutrition, vol. 119, no. 5, pp. 800–804, 1989. View at Google Scholar · View at Scopus
  50. K. Cope, T. Risby, and A. M. Diehl, “Increased gastrointestinal ethanol production in obese mice: implications for fatty liver disease pathogenesis,” Gastroenterology, vol. 119, no. 5, pp. 1340–1347, 2000. View at Publisher · View at Google Scholar · View at Scopus