The role of microbiota in hepatic encephalopathy

Gut Microbes

Volumn 5, Issue 3, 2014, Pages 397-403

  Bajaj, Jasmohan S ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Cirrhosis; Correlation network; Covert hepatic encephalopathy; Dysbiosis; Endotoxin; Lactulose; Minimal hepatic encephalopathy; Probiotic; Rifaximin; Systemic inflammation

Indexed keywords

LACTULOSE; NEOMYCIN; PROBIOTIC AGENT; RIFAXIMIN; SYNBIOTIC AGENT;

ALCOHOL ABUSE; ARTICLE; COGNITION; DISEASE COURSE; DISEASE SEVERITY; DYSBIOSIS; ENDOTOXEMIA; HEPATIC ENCEPHALOPATHY; HUMAN; INFLAMMATION; INTESTINE FLORA; LACTOBACILLUS; LIVER CIRRHOSIS; MICROBIOME; MICROFLORA; NONHUMAN; SARCOPENIA; STREPTOCOCCUS SALIVARIUS; COMPLICATION; GASTROINTESTINAL TRACT; MICROBIOLOGY; PATHOPHYSIOLOGY;

DYSBIOSIS; GASTROINTESTINAL TRACT; HEPATIC ENCEPHALOPATHY; HUMANS; LIVER CIRRHOSIS;

EID: 84900538213     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.28684     Document Type: Article

References (43)

1. Quigley EM, Stanton C, Murphy EF. The gut microbiota and the liver. Pathophysiological and clinical implications. J Hepatol 2013; 58:1020-7; PMID:23183530; http://dx.doi.org/10.1016/j.jhep.2012.11.023
2. Tandon P, Garcia-Tsao G. Bacterial infections, sepsis, and multiorgan failure in cirrhosis. Semin Liver Dis 2008; 28:26-42; PMID:18293275; http://dx.doi.org/10.1055/s-2008-1040319
3. Bajaj JS, Gillevet PM, Patel NR, Ahluwalia V, Ridlon JM, Kettenmann B, Schubert CM, Sikaroodi M, Heuman DM, Crossey MM, et al. A longitudinal systems biology analysis of lactulose withdrawal in hepatic encephalopathy. Metab Brain Dis 2012; 27:205-15; PMID:22527995; http://dx.doi.org/10.1007/s11011-012-9303-0
4. Bajaj JS, Wade JB, Sanyal AJ. Spectrum of neurocognitive impairment in cirrhosis: Implications for the assessment of hepatic encephalopathy. Hepatology 2009; 50:2014-21; PMID:19787808; http://dx.doi.org/10.1002/hep.23216
5. Ortiz M, Jacas C, Córdoba J. Minimal hepatic encephalopathy: diagnosis, clinical significance and recommendations. J Hepatol 2005; 42(Suppl):S45-53; PMID:15777572; http://dx.doi.org/10.1016/j.jhep.2004.11.028
6. Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT. Hepatic encephalopathy--definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 2002; 35:716-21; PMID:11870389; http://dx.doi.org/10.1053/jhep.2002.31250
7. Shawcross DL, Wright G, Olde Damink SW, Jalan R. Role of ammonia and inflammation in minimal hepatic encephalopathy. Metab Brain Dis 2007; 22:125-38; PMID:17260161; http://dx.doi.org/10.1007/s11011-006-9042-1
8. Bajaj JS. Review article: the modern management of hepatic encephalopathy. Aliment Pharmacol Ther 2010; 31:537-47; PMID:20002027; http://dx.doi.org/10.1111/j.1365-2036.2009.04211.x
9. Romero-Gómez M, Jover M, Del Campo JA, Royo JL, Hoyas E, Galán JJ, Montoliu C, Baccaro E, Guevara M, Córdoba J, et al. Variations in the promoter region of the glutaminase gene and the development of hepatic encephalopathy in patients with cirrhosis: a cohort study. Ann Intern Med 2010; 153:281-8; PMID:20820037; http://dx.doi.org/10.7326/0003-4819-153-5-201009070-00002
10. Riggio O, Varriale M, Testore GP, Di Rosa R, Di Rosa E, Merli M, Romiti A, Candiani C, Capocaccia L. Effect of lactitol and lactulose administration on the fecal flora in cirrhotic patients. J Clin Gastroenterol 1990; 12:433-6; PMID:2398251; http://dx.doi.org/10.1097/00004836-199008000-00016
11. Tarao K, Tamai S, Ito Y, Okawa S, Hayashi M. [Effects of lactitol on fecal bacterial flora in patients with liver cirrhosis and hepatic encephalopathy]. Nihon Shokakibyo Gakkai Zasshi 1995; 92:1037-50; PMID:7643458
12. Liu Q, Duan ZP, Ha DK, Bengmark S, Kurtovic J, Riordan SM. Synbiotic modulation of gut flora: effect on minimal hepatic encephalopathy in patients with cirrhosis. Hepatology 2004; 39:1441-9; PMID:15122774; http://dx.doi.org/10.1002/hep.20194
13. Kamath PS, Kim WR; Advanced Liver Disease Study Group. The model for end-stage liver disease (MELD). Hepatology 2007; 45:797-805; PMID:17326206; http://dx.doi.org/10.1002/hep.21563
14. Chen Y, Yang F, Lu H, Wang B, Chen Y, Lei D, Wang Y, Zhu B, Li L. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 2011; 54:562-72; PMID:21574172; http://dx.doi.org/10.1002/hep.24423
15. Bajaj JS, Ridlon JM, Hylemon PB, Thacker LR, Heuman DM, Smith S, Sikaroodi M, Gillevet PM. Linkage of gut microbiome with cognition in hepatic encephalopathy. Am J Physiol Gastrointest Liver Physiol 2012; 302:G168-75; PMID:21940902; http://dx.doi.org/10.1152/ajpgi.00190.2011
16. Nava GM, Stappenbeck TS. Diversity of the autochthonous colonic microbiota. Gut Microbes 2011; 2:99-104; PMID:21694499; http://dx.doi.org/10.4161/gmic.2.2.15416
17. Bajaj JS, Hylemon PB, Heuman DM, et al. The Cirrhosis Dysbiosis Ratio defines Changes in the Gut Microbiome Associated with Cirrhosis and its Complications. J Hepatol 2014.; http://dx.doi.org/10.1016/j.jhep.2013.12.019
18. Zhang Z, Zhai H, Geng J, Yu R, Ren H, Fan H, Shi P. Large-scale survey of gut microbiota associated with MHE Via 16S rRNA-based pyrosequencing. Am J Gastroenterol 2013; 108:1601-11; PMID:23877352; http://dx.doi.org/10.1038/ajg.2013.221
19. Teltschik Z, Wiest R, Beisner J, Nuding S, Hofmann C, Schoelmerich J, Bevins CL, Stange EF, Wehkamp J. Intestinal bacterial translocation in rats with cirrhosis is related to compromised Paneth cell antimicrobial host defense. Hepatology 2012; 55:1154-63; PMID:22095436; http://dx.doi.org/10.1002/hep.24789
20. Kappus MR, Bajaj JS. Covert hepatic encephalopathy: not as minimal as you might think. Clin Gastroenterol Hepatol 2012; 10:1208-19; PMID:22728384; http://dx.doi.org/10.1016/j.cgh.2012.05.026
21. Ahluwalia V, Wade JB, Heuman DM, Hammeke TA, Sanyal AJ, Sterling RK, Stravitz RT, Luketic V, Siddiqui MS, Puri P, et al. Enhancement of functional connectivity, working memory and inhibitory control on multi-modal brain MR imaging with Rifaximin in Cirrhosis: Implications for the gut-liver-brain axis. Metab Brain Dis 2014; PMID:24590688; http://dx.doi.org/10.1007/s11011-014-9507-6
22. Bajaj JS, Saeian K, Christensen KM, Hafeezullah M, Varma RR, Franco J, Pleuss JA, Krakower G, Hoffmann RG, Binion DG. Probiotic yogurt for the treatment of minimal hepatic encephalopathy. Am J Gastroenterol 2008; 103:1707-15; PMID:18691193; http://dx.doi.org/10.1111/j.1572-0241.2008.01861.x
23. Mittal VV, Sharma BC, Sharma P, Sarin SK. A randomized controlled trial comparing lactulose, probiotics, and L-ornithine L-aspartate in treatment of minimal hepatic encephalopathy. Eur J Gastroenterol Hepatol 2011; 23:725-32; PMID:21646910; http://dx.doi.org/10.1097/MEG.0b013e32834696f5
24. Jain L, Sharma BC, Srivastava S, Puri SK, Sharma P, Sarin S. Serum endotoxin, inflammatory mediators, and magnetic resonance spectroscopy before and after treatment in patients with minimal hepatic encephalopathy. J Gastroenterol Hepatol 2013; 28:1187-93; PMID:23425082; http://dx.doi.org/10.1111/jgh.12160
25. Bajaj JS, Heuman DM, Sanyal AJ, Hylemon PB, Sterling RK, Stravitz RT, Fuchs M, Ridlon JM, Daita K, Monteith P, et al. Modulation of the metabiome by rifaximin in patients with cirrhosis and minimal hepatic encephalopathy. PLoS One 2013; 8:e60042; PMID:23565181; http://dx.doi.org/10.1371/journal.pone.0060042
26. Ahluwalia V, Wade JB, Heuman DM, Hammeke TA, Sanyal AJ, Sterling RK, Stravitz RT, Luketic V, Siddiqui MS, Puri P, et al. Enhancement of functional connectivity, working memory and inhibitory control on multi-modal brain MR imaging with Rifaximin in Cirrhosis: Implications for the gut-liver-brain axis. Metab Brain Dis 2014; PMID:24590688; http://dx.doi.org/10.1007/s11011-014-9507-6
27. Jiang ZD, Ke S, Dupont HL. Rifaximin-induced alteration of virulence of diarrhoea-producing Escherichia coli and Shigella sonnei. Int J Antimicrob Agents 2010; 35:278-81; PMID:20045287; http://dx.doi.org/10.1016/j.ijantimicag.2009.11.013
28. Vanhoutte T, De Preter V, De Brandt E, Verbeke K, Swings J, Huys G. Molecular monitoring of the fecal microbiota of healthy human subjects during administration of lactulose and Saccharomyces boulardii. Appl Environ Microbiol 2006; 72:5990-7; PMID:16957220; http://dx.doi.org/10.1128/AEM.00233-06
29. Bajaj JS, Hylemon PB, Ridlon JM, Heuman DM, Daita K, White MB, Monteith P, Noble NA, Sikaroodi M, Gillevet PM. Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am J Physiol Gastrointest Liver Physiol 2012; 303:G675-85; PMID:22821944; http://dx.doi.org/10.1152/ajpgi.00152.2012
30. Vlahcevic ZR, Buhac I, Bell CC Jr., Swell L. Abnormal metabolism of secondary bile acids in patients with cirrhosis. Gut 1970; 11:420-2; PMID:5428044; http://dx.doi.org/10.1136/gut.11.5.420
31. Kakiyama G, Pandak WM, Gillevet PM, Hylemon PB, Heuman DM, Daita K, Takei H, Muto A, Nittono H, Ridlon JM, et al. Modulation of the fecal bile acid profile by gut microbiota in cirrhosis. J Hepatol 2013; 58:949-55; PMID:23333527; http://dx.doi.org/10.1016/j.jhep.2013.01.003
32. Ridlon JM, Alves JM, Hylemon PB, Bajaj JS. Cirrhosis, bile acids, and gut microbiota: Unraveling a complex relationship. Gut Microbes 2013; 4:4; PMID:23851335; http://dx.doi.org/10.4161/gmic.25723
33. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, 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 U S A 2008; 105:16731-6; PMID:18936492; http://dx.doi.org/10.1073/pnas.0804812105
34. Zoetendal EG, Ben-Amor K, Harmsen HJ, Schut F, Akkermans AD, de Vos WM. Quantification of uncultured Ruminococcus obeum-like bacteria in human fecal samples by fluorescent in situ hybridization and flow cytometry using 16S rRNA-targeted probes. Appl Environ Microbiol 2002; 68:4225-32; PMID:12200269; http://dx.doi.org/10.1128/AEM.68.9.4225-4232.2002
35. Zapater P, Francés R, González-Navajas JM, de la Hoz MA, Moreu R, Pascual S, Monfort D, Montoliu S, Vila C, Escudero A, et al. Serum and ascitic fluid bacterial DNA: a new independent prognostic factor in noninfected patients with cirrhosis. Hepatology 2008; 48:1924-31; PMID:19003911; http://dx.doi.org/10.1002/hep.22564
36. Montano-Loza AJ, Meza-Junco J, Prado CM, Lieffers JR, Baracos VE, Bain VG, Sawyer MB. Muscle wasting is associated with mortality in patients with cirrhosis. Clin Gastroenterol Hepatol 2012; 10:166-73, e1; PMID:21893129; http://dx.doi.org/10.1016/j.cgh.2011.08.028
37. Olde Damink SW, Jalan R, Dejong CH. Interorgan ammonia trafficking in liver disease. Metab Brain Dis 2009; 24:169-81; PMID:19067143; http://dx.doi.org/10.1007/s11011-008-9122-5
38. McPhail MJ, Taylor-Robinson SD. The role of magnetic resonance imaging and spectroscopy in hepatic encephalopathy. Metab Brain Dis 2010; 25:65-72; PMID:20221679; http://dx.doi.org/10.1007/s11011-010-9171-4
39. Mutlu EA, Gillevet PM, Rangwala H, Sikaroodi M, Naqvi A, Engen PA, Kwasny M, Lau CK, Keshavarzian A. Colonic microbiome is altered in alcoholism. Am J Physiol Gastrointest Liver Physiol 2012; 302:G966-78; PMID:22241860; http://dx.doi.org/10.1152/ajpgi.00380.2011
40. Hartmann P, Chen WC, Schnabl B. The intestinal microbiome and the leaky gut as therapeutic targets in alcoholic liver disease. Front Physiol 2012; 3:402; PMID:23087650; http://dx.doi.org/10.3389/fphys.2012.00402
41. Bajaj JS, Forton DM. Cognitive improvement after HCV eradication: Extending the benefits. Hepatology 2013; 58:480-2; PMID:23696270; http://dx.doi.org/10.1002/hep.26481
42. Lu H, Wu Z, Xu W, Yang J, Chen Y, Li L. Intestinal microbiota was assessed in cirrhotic patients with hepatitis B virus infection. Intestinal microbiota of HBV cirrhotic patients. Microb Ecol 2011; 61:693-703; PMID:21286703; http://dx.doi.org/10.1007/s00248-010-9801-8
43. Bajaj JS, Heuman DM, Hylemon PB, Sanyal AJ, Puri P, Sterling RK, Luketic V, Stravitz RT, Siddiqui MS, Fuchs M, et al. Randomised clinical trial: Lactobacillus GG modulates gut microbiome, metabolome and endotoxemia in patients with cirrhosis. Aliment Pharmacol Ther 2014; 39:1113-25; PMID:24628464; http://dx.doi.org/10.1111/apt.12695