Fecal microbiota transplantation prevents hepatic encephalopathy in rats with carbon tetrachloride-induced acute hepatic dysfunction

World Journal of Gastroenterology

Volumn 23, Issue 38, 2017, Pages 6983-6994

  Wang, Wei Wei ^a   Zhang, Yu ^a   Huang, Xiao Bing ^a   You, Nan ^a   Zheng, Lu ^a   Li, Jing ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Cognitive function; Fecal microbiota transplantation; Hepatic encephalopathy; Intestinal permeability; Toll like receptor

Indexed keywords

AMMONIA; CARBON TETRACHLORIDE; CLAUDIN 1; CLAUDIN 6; INTERLEUKIN 1BETA; INTERLEUKIN 6; OCCLUDIN; TIGHT JUNCTION PROTEIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR;

AMMONIA BLOOD LEVEL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; FECAL MICROBIOTA TRANSPLANTATION; HEPATIC CLEARANCE; HEPATIC ENCEPHALOPATHY; INFLAMMATION; INTESTINE MUCOSA; INTESTINE MUCOSA PERMEABILITY; INTESTINE TISSUE; LIVER DYSFUNCTION; LIVER FUNCTION; LIVER NECROSIS; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; RAT MODEL; SPATIAL LEARNING; ANIMAL; BLOOD; COMPLICATION; EVALUATION STUDY; INTOXICATION; MEMORY; METABOLISM; SPRAGUE DAWLEY RAT;

AMMONIA; ANIMALS; CARBON TETRACHLORIDE POISONING; FECAL MICROBIOTA TRANSPLANTATION; HEPATIC ENCEPHALOPATHY; INTESTINAL MUCOSA; MALE; MEMORY; RATS, SPRAGUE-DAWLEY;

EID: 85031320898     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v23.i38.6983     Document Type: Article

References (50)

1. Wijdicks EFM. Hepatic Encephalopathy. N Engl J Med 2017; 376: 186 [PMID: 28076712 DOI: 10.1056/NEJMc1614962]
2. Ahluwalia V, Betrapally NS, Hylemon PB, White MB, Gillevet PM, Unser AB, Fagan A, Daita K, Heuman DM, Zhou H, Sikaroodi M, Bajaj JS. Impaired Gut-Liver-Brain Axis in Patients with Cirrhosis. Sci Rep 2016; 6: 26800 [PMID: 27225869 DOI: 10.1038/srep26800]
3. Lauridsen MM, Bajaj JS. Hepatic encephalopathy treatment and its effect on driving abilities: A continental divide. J Hepatol 2015; 63: 287-288 [PMID: 25796480 DOI: 10.1016/j.jhep.2015.03.017]
4. Bustamante J, Rimola A, Ventura PJ, Navasa M, Cirera I, Reggiardo V, Rodés J. Prognostic significance of hepatic encephalopathy in patients with cirrhosis. J Hepatol 1999; 30: 890-895 [PMID: 10365817]
5. Dhiman RK, Kurmi R, Thumburu KK, Venkataramarao SH, Agarwal R, Duseja A, Chawla Y. Diagnosis and prognostic significance of minimal hepatic encephalopathy in patients with cirrhosis of liver. Dig Dis Sci 2010; 55: 2381-2390 [PMID: 20508990 DOI: 10.1007/s10620-010-1249-7]
6. Reuben A, Tillman H, Fontana RJ, Davern T, McGuire B, Stravitz RT, Durkalski V, Larson AM, Liou I, Fix O, Schilsky M, McCashland T, Hay JE, Murray N, Shaikh OS, Ganger D, Zaman A, Han SB, Chung RT, Smith A, Brown R, Crippin J, Harrison ME, Koch D, Munoz S, Reddy KR, Rossaro L, Satyanarayana R, Hassanein T, Hanje AJ, Olson J, Subramanian R, Karvellas C, Hameed B, Sherker AH, Robuck P, Lee WM. Outcomes in Adults With Acute Liver Failure Between 1998 and 2013: An Observational Cohort Study. Ann Intern Med 2016; 164: 724-732 [PMID: 27043883 DOI: 10.7326/M15-2211]
7. Gubbins GP, Moritz TE, Marsano LS, Talwalkar R, McClain CJ, Mendenhall CL. Helicobacter pylori is a risk factor for hepatic encephalopathy in acute alcoholic hepatitis: the ammonia hypothesis revisited. The Veterans Administration Cooperative Study Group No. 275. Am J Gastroenterol 1993; 88: 1906-1910 [PMID: 8237940]
8. Kramer L, Tribl B, Gendo A, Zauner C, Schneider B, Ferenci P, Madl C. Partial pressure of ammonia versus ammonia in hepatic encephalopathy. Hepatology 2000; 31: 30-34 [PMID: 10613724 DOI: 10.1002/hep.510310107]
9. Shawcross DL, Shabbir SS, Taylor NJ, Hughes RD. Ammonia and the neutrophil in the pathogenesis of hepatic encephalopathy in cirrhosis. Hepatology 2010; 51: 1062-1069 [PMID: 19890967 DOI: 10.1002/hep.23367]
10. Wright G, Jalan R. Ammonia and inflammation in the pathogenesis of hepatic encephalopathy: Pandora's box? Hepatology 2007; 46: 291-294 [PMID: 17661413 DOI: 10.1002/hep.21843]
11. Ge PS, Runyon BA. Serum ammonia level for the evaluation of hepatic encephalopathy. JAMA 2014; 312: 643-644 [PMID: 25117134 DOI: 10.1001/jama.2014.2398]
12. Rai R, Saraswat VA, Dhiman RK. Gut microbiota: its role in hepatic encephalopathy. J Clin Exp Hepatol 2015; 5: S29-S36 [PMID: 26041954 DOI: 10.1016/j.jceh.2014.12.003]
13. Bajaj JS, Betrapally NS, Hylemon PB, Heuman DM, Daita K, White MB, Unser A, Thacker LR, Sanyal AJ, Kang DJ, Sikaroodi M, Gillevet PM. Salivary microbiota reflects changes in gut microbiota in cirrhosis with hepatic encephalopathy. Hepatology 2015; 62: 1260-1271 [PMID: 25820757 DOI: 10.1002/hep.27819]
14. Victor DW 3rd, Quigley EM. Hepatic encephalopathy involves interactions among the microbiota, gut, brain. Clin Gastroenterol Hepatol 2014; 12: 1009-1011 [PMID: 24462627 DOI: 10.1016/ j.cgh.2014.01.022]
15. Dhiman RK. Gut microbiota and hepatic encephalopathy. Metab Brain Dis 2013; 28: 321-326 [PMID: 23463489 DOI: 10.1007/ s11011-013-9388-0]
16. Garcovich M, Zocco MA, Roccarina D, Ponziani FR, Gasbarrini A. Prevention and treatment of hepatic encephalopathy: focusing on gut microbiota. World J Gastroenterol 2012; 18: 6693-6700 [PMID: 23239905 DOI: 10.3748/wjg.v18.i46.6693]
17. Dhiman RK. Gut microbiota, inflammation and hepatic encephalopathy: a puzzle with a solution in sight. J Clin Exp Hepatol 2012; 2: 207-210 [PMID: 25755435 DOI: 10.1016/ j.jceh.2012.08.004]
18. Maharshi S, Sharma BC, Srivastava S, Jindal A. Randomised controlled trial of lactulose versus rifaximin for prophylaxis of hepatic encephalopathy in patients with acute variceal bleed. Gut 2015; 64: 1341-1342 [PMID: 25320105 DOI: 10.1136/ gutjnl-2014-308521]
19. Kalaitzakis E, Björnsson E. Lactulose treatment for hepatic encephalopathy, gastrointestinal symptoms, and health-related quality of life. Hepatology 2007; 46: 949-950; author reply 951 [PMID: 17879365 DOI: 10.1002/hep.21760]
20. Als-Nielsen B, Gluud LL, Gluud C. Non-absorbable disaccharides for hepatic encephalopathy: systematic review of randomised trials. BMJ 2004; 328: 1046 [PMID: 15054035 DOI: 10.1136/ bmj.38048.506134.EE]
21. Cesaro C, Tiso A, Del Prete A, Cariello R, Tuccillo C, Cotticelli G, Del Vecchio Blanco C, Loguercio C. Gut microbiota and probiotics in chronic liver diseases. Dig Liver Dis 2011; 43: 431-438 [PMID: 21163715 DOI: 10.1016/j.dld.2010.10.015]
22. Lunia MK, Sharma BC, Sharma P, Sachdeva S, Srivastava S. Probiotics prevent hepatic encephalopathy in patients with cirrhosis: a randomized controlled trial. Clin Gastroenterol Hepatol 2014; 12: 1003-1008.e1 [PMID: 24246768 DOI: 10.1016/ j.cgh.2013.11.006]
23. McGee RG, Bakens A, Wiley K, Riordan SM, Webster AC. Probiotics for patients with hepatic encephalopathy. Cochrane Database Syst Rev 2011; 11: CD008716 [PMID: 22071855 DOI: 10.1002/14651858.CD008716.pub2]
24. Xu J, Ma R, Chen LF, Zhao LJ, Chen K, Zhang RB. Effects of probiotic therapy on hepatic encephalopathy in patients with liver cirrhosis: an updated meta-analysis of six randomized controlled trials. Hepatobiliary Pancreat Dis Int 2014; 13: 354-360 [PMID: 25100119]
25. Zhao LN, Yu T, Lan SY, Hou JT, Zhang ZZ, Wang SS, Liu FB. Probiotics can improve the clinical outcomes of hepatic encephalopathy: An update meta-analysis. Clin Res Hepatol Gastroenterol 2015; 39: 674-682 [PMID: 25956487 DOI: 10.1016/ j.clinre.2015.03.008]
26. Lee CH, Steiner T, Petrof EO, Smieja M, Roscoe D, Nematallah A, Weese JS, Collins S, Moayyedi P, Crowther M, Ropeleski MJ, Jayaratne P, Higgins D, Li Y, Rau NV, Kim PT. Frozen vs Fresh Fecal Microbiota Transplantation and Clinical Resolution of Diarrhea in Patients With Recurrent Clostridium difficile Infection: A Randomized Clinical Trial. JAMA 2016; 315: 142-149 [PMID: 26757463 DOI: 10.1001/jama.2015.18098]
27. Ho N, Prasad V. Clostridium difficile diarrhea and fecal transplantation. J Clin Gastroenterol 2011; 45: 742-743 [PMID: 21555950 DOI: 10.1097/MCG.0b013e31821b1094]
28. Rohlke F, Stollman N. Fecal microbiota transplantation in relapsing Clostridium difficile infection. Therap Adv Gastroenterol 2012; 5: 403-420 [PMID: 23152734 DOI: 10.1177/1756283X1245 3637]
29. Youngster I, Russell GH, Pindar C, Ziv-Baran T, Sauk J, Hohmann EL. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA 2014; 312: 1772-1778 [PMID: 25322359 DOI: 10.1001/jama.2014.13875]
30. Abdollahi-Roodsaz S, Abramson SB, Scher JU. The metabolic role of the gut microbiota in health and rheumatic disease: mechanisms and interventions. Nat Rev Rheumatol 2016; 12: 446-455 [PMID: 27256713 DOI: 10.1038/nrrheum.2016.68]
31. Groen AK, Nieuwdorp M. An evaluation of the therapeutic potential of fecal microbiota transplantation to treat infectious and metabolic diseases. EMBO Mol Med 2017; 9: 1-3 [PMID: 27861129 DOI: 10.15252/emmm.201607035]
32. Smits LP, Bouter KE, de Vos WM, Borody TJ, Nieuwdorp M. Therapeutic potential of fecal microbiota transplantation. Gastroenterology 2013; 145: 946-953 [PMID: 24018052 DOI: 10.1053/j.gastro.2013.08.058]
33. Hamilton MJ, Weingarden AR, Sadowsky MJ, Khoruts A. Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection. Am J Gastroenterol 2012; 107: 761-767 [PMID: 22290405 DOI: 10.1038/ajg.2011.482]
34. Satokari R, Mattila E, Kainulainen V, Arkkila PE. Simple faecal preparation and efficacy of frozen inoculum in faecal microbiota transplantation for recurrent Clostridium difficile infection-an observational cohort study. Aliment Pharmacol Ther 2015; 41: 46-53 [PMID: 25355279 DOI: 10.1111/apt.13009]
35. Farjam M, Dehdab P, Abbassnia F, Mehrabani D, Tanideh N, Pakbaz S, Imanieh MH. Thioacetamide-induced acute hepatic encephalopathy in rat: behavioral, biochemical and histological changes. Iran Red Crescent Med J 2012; 14: 164-170 [PMID: 22737573]
36. Zimmermann C, Ferenci P, Pifl C, Yurdaydin C, Ebner J, Lassmann H, Roth E, Hörtnagl H. Hepatic encephalopathy in thioacetamide-induced acute liver failure in rats: characterization of an improved model and study of amino acid-ergic neurotransmission. Hepatology 1989; 9: 594-601 [PMID: 2564368]
37. Tranah TH, Vijay GK, Ryan JM, Shawcross DL. Systemic inflammation and ammonia in hepatic encephalopathy. Metab Brain Dis 2013; 28: 1-5 [PMID: 23224356 DOI: 10.1007/ s11011-012-9370-2]
38. O'Beime JP, Chouhan M, Hughes RD. The role of infection and inflammation in the pathogenesis of hepatic encephalopathy and cerebral edema in acute liver failure. Nat Clin Pract Gastroenterol Hepatol 2006; 3: 118-119 [PMID: 16511529 DOI: 10.1038/ ncpgasthep0417]
39. Blei AT. Infection, inflammation and hepatic encephalopathy, synergism redefined. J Hepatol 2004; 40: 327-330 [PMID: 14739106]
40. Aguirre Valadez JM, Rivera-Espinosa L, Méndez-Guerrero O, Chávez-Pacheco JL, García Juárez I, Torre A. Intestinal permeability in a patient with liver cirrhosis. Ther Clin Risk Manag 2016; 12: 1729-1748 [PMID: 27920543 DOI: 10.2147/TCRM. S115902]
41. Benjamin J, Singla V, Arora I, Sood S, Joshi YK. Intestinal permeability and complications in liver cirrhosis: A prospective cohort study. Hepatol Res 2013; 43: 200-207 [PMID: 22726344 DOI: 10.1111/j.1872-034X.2012.01054.x]
42. Luo M, Guo JY, Cao WK. Inflammation: A novel target of current therapies for hepatic encephalopathy in liver cirrhosis. World J Gastroenterol 2015; 21: 11815-11824 [PMID: 26557005 DOI: 10.3748/wjg.v21.i41.11815]
43. Pathak R, Enuh HA, Patel A, Wickremesinghe P. Treatment of relapsing Clostridium difficile infection using fecal microbiota transplantation. Clin Exp Gastroenterol 2013; 7: 1-6 [PMID: 24421645 DOI: 10.2147/CEG.S53410]
44. Cariello R, Federico A, Sapone A, Tuccillo C, Scialdone VR, Tiso A, Miranda A, Portincasa P, Carbonara V, Palasciano G, Martorelli L, Esposito P, Cartenì M, Del Vecchio Blanco C, Loguercio C. Intestinal permeability in patients with chronic liver diseases: Its relationship with the aetiology and the entity of liver damage. Dig Liver Dis 2010; 42: 200-204 [PMID: 19502117 DOI: 10.1016/ j.dld.2009.05.001]
45. Lambert JC, Zhou Z, Wang L, Song Z, McClain CJ, Kang YJ. Prevention of alterations in intestinal permeability is involved in zinc inhibition of acute ethanol-induced liver damage in mice. J Pharmacol Exp Ther 2003; 305: 880-886 [PMID: 12626662 DOI: 10.1124/jpet.102.047852]
46. Frazier TH, DiBaise JK, McClain CJ. Gut microbiota, intestinal permeability, obesity-induced inflammation, and liver injury. JPEN J Parenter Enteral Nutr 2011; 35: 14S-20S [PMID: 21807932 DOI: 10.1177/0148607111413772]
47. Luo M, Li L, Yang EN, Dai CY, Liang SR, Cao WK. Correlation between interleukin-6 and ammonia in patients with overt hepatic encephalopathy due to cirrhosis. Clin Res Hepatol Gastroenterol 2013; 37: 384-390 [PMID: 23084463 DOI: 10.1016/ j.clinre.2012.08.007]
48. Li W, Li N, Wang R, Li Q, Wu H. Interferon gamma, interleukin-6, and-17a levels were correlated with minimal hepatic encephalopathy in HBV patients. Hepatol Int 2015; 9: 218-223 [PMID: 25794550 DOI: 10.1007/s12072-015-9610-8]
49. Tsai CF, Chu CJ, Huang YH, Wang YP, Liu PY, Lin HC, Lee FY, Lu CL. Detecting minimal hepatic encephalopathy in an endemic country for hepatitis B: the role of psychometrics and serum IL-6. PLoS One 2015; 10: e0128437 [PMID: 26039496 DOI: 10.1371/ journal.pone.0128437]
50. Lata J, Jurankova J, Kopacova M, Vitek P. Probiotics in hepatology. World J Gastroenterol 2011; 17: 2890-2896 [PMID: 21734800 DOI: 10.3748/wjg.v17.i24.2890]