288
Views
16
CrossRef citations to date
0
Altmetric
Reviews

The gut microbiota and the liver: implications for clinical practice

&
Pages 723-732 | Published online: 10 Jan 2014

References

  • Shah VJ, Kamath PS. Portal hypertension and gastrointestinal bleeding. In: Sleisenger and Fordtran’s Gastrointestinal and Liver Disease (9th Edition). Saunders Elsevier, PA, USA, 1489–1516 (2010).
  • Fraher MH, O’Toole PW, Quigley EMM. Techniques used to characterise the intestinal microbiota: a guide for the clinician. Nat. Rev. Gastroenterol. Hepatol. 9(6), 312–322 (2012).
  • Nicholson JK, Holmes E, Kinross J et al. Host-gut microbiota metabolic interactions. Science 336(6086), 1262–1267 (2012).
  • Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13(4), 260–270 (2012).
  • Abu-Shanab A, Quigley EM. The role of the gut microbiota in nonalcoholic fatty liver disease. Nat. Rev. Gastroenterol. Hepatol. 7(12), 691–670 (2010).
  • Miyake Y, Yamammoto K. Role of gut microbiota in liver diseases. Hepatol. Res. 43(2), 139–146 (2013).
  • Chassaing B, Etienne-Mesmin L, Gewirtz AT. Microbiota-liver axis in hepatic disease. Hepatology doi:10.1002/hep.26494 (2013) ( Epub ahead of print).
  • Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13(10), 701–712 (2012).
  • Moschen AR, Wieser V, Tilg H. Dietary factors: major regulators of the gut’s microbiota. Gut. Liver 6(4), 411–416 (2012).
  • Clarke SF, Murphy EF, Nilaweera K et al. The gut microbiota and its relationship to diet and obesity: new insights. Gut Microbes 3(3), 186–202 (2012).
  • Hildebrandt MA, Hoffman C, Sherrill-Mix SA et al. High fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137(5), 1716–1724 (2009).
  • Jernberg C, Lofmark S, Edlund C et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 1(1), 56–66 (2007).
  • Fouhy F, Guinane CM, Hussey S et al. High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob. Agents Chemother. 56(11), 5811–5820 (2012).
  • O’Sullivan O, Coakley M, Lakshminarayanan B et al. Alterations in intestinal microbiota of elderly Irish subjects post-antibiotic therapy. J. Antimicrob. Chemother. 68(1), 214–221 (2013).
  • Claesson MJ, Jeffery IB, Conde S et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410), 178–184 (2012).
  • Cho I, Yamanishi S, Cox L, Methe BA et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488(7413), 621–626 (2012).
  • Membrez M, Blancher F, Jaquet M et al. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. FASEB J. 22(7), 2416–2426 (2008).
  • Mutlu EA, Gillevet PM, Rangwala H et al. Colonic microbiome is altered in alcoholism. Am. J. Physiol. Gastrointest. Liver Physiol. 302(9), G986–G978 (2012).
  • 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. 17(2), 225–235 (2013).
  • Phillips GB, Schwartz R, Gabuzda GJ Jr et al. The syndrome of impending hepatic coma in patients with cirrhosis of the liver given certain nitrogenous substances. N. Engl. J. Med. 247(7), 239–246 (1952).
  • Martini GA, Phear EA, Ruebner B et al. The bacterial content of the small intestine in normal and cirrhotic subjects: relation to methionine toxicity. Clin. Sci (Lond). 16(1), 35–51 (1957).
  • Phear EA, Ruebner B, Sherlock S et al. Methionine toxicity in liver disease and its prevention by chlortetracycline. Clin. Sci (lond). 15(1), 93–117 (1956).
  • Szabo G, Bala S, Petrasek J et al. Gut-liver axis and sensing microbes. Dig. Dis. 28(6), 737–744 (2010).
  • Quigley EMM, Marsh MN, Shaffer JL et al. Hepatobiliary complications of total parenteral nutrition. Gastroenterology 104(1), 286–301 (1993).
  • Terjung B, Spengler U. Atypical p-ANCA in PSC and AIH: a hint toward a “leaky gut”? Clin. Rev. Allergy Immunol. 36(1), 40–51 (2009).
  • Terjung B, Söhne J, Lechtenberg B et al. p-ANCAs in autoimmune liver disorders recognise human beta-tubulin isotype 5 and cross-react with microbial protein FtsZ. Gut 59(6), 808–816 (2010).
  • Quigley EMM. Gastrointestinal dysfunction in liver disease – gut–liver interactions revisited. Dig. Dis. Sci. 41(3), 557–561 (1996).
  • Thalheimer U, Triantos CK, Samonakis DN et al. Infection, coagulation and variceal bleeding in cirrhosis. Gut 54(4), 556–563 (2005).
  • Seki E, Schnabl B. Role of innate immunity and the microbiota in liver fibrosis: crosstalk between the liver and gut. J. Physiol. 590(***), 447–458 (2012).
  • Crispe IN. The liver as a lymphoid organ. Ann. Rev. Immunol. 27, 147–163 (2009).
  • Seo YS, Shah VH. The role of gut liver axis in the pathogenesis of liver cirrhosis and portal hypertension Clin. Mol. Hepatol. 18(4), 337–346 (2012).
  • Catala M, Anton A, Portoles MT. Characterization of the simultaneous binding of history Escherichia coli endotoxin to Kupffer and endothelial liver cells by flow cytometry. Cytometry 36(2), 123–130 (1999).
  • Deng M, Scott MJ, Loughran P et al. Lipopolysaccharide clearance, bacterial clearance, and systemic inflammatory responses are regulated by cell type-specific functions of TLR4 during sepsis. J. Immunol. 190(10), 5152–5160 (2013).
  • Hoque R, Vodovotz Y, Mehal W. Therapeutic strategies in inflammasome mediated diseases of the liver. J. Hepatol. 58(5), 1047–1052 (2013).
  • Hoefert B. Über die Bakterienbefunde im Duodenalsaft von Gesunden und Kranken. Zschr. Klin. Med. 92, 221–235 (1921).
  • Quigley EMM. The liver and gastrointestinal disease. In: Schiff ’s Diseases of the Liver (9th Edition). Schiff ER, Sorrell MF, Maddrey WC ( Eds). Lippincott Raven, Philadelphia, PA (2002).
  • Abu Shanab A, Scully P, Crosbie O et al. Small Intestinal Bacterial Overgrowth in Non-Alcoholic S teato-Hepatitis; association with Toll-Like Receptor 4 expression and plasma levels of Interleukin 8. Dig. Dis. Sci. 56(5), 1524–1534 (2011).
  • Bode C, Kolepke R, Schafer K et al. Breath hydrogen excretion in patients with alcoholic liver disease–evidence of small intestinal bacterial overgrowth. Z. Gastroenterol. 31(1), 3–7 (1993).
  • Teltschik Z, Wiest R, Beisner J et al. Intestinal bacterial translocation in rats with cirrhosis is related to compromised Paneth cell antimicrobial host defense. Hepatology 55(4), 1154–1163 (2012).
  • Purohit V, Bode JC, Bode C et al. Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: summary of a symposium. Alcohol 42(5), 349–361 (2008).
  • Wigg AJ, Roberts-Thomson IC, Dymock RB et al. The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxemia, and tumor necrosis factor alpha in the pathogenesis of nonalcoholic steatohepatitis. Gut 48(2), 206–211 (2001).
  • Bajaj JS, Hylemon PB, Ridlon JM et al. 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. 303(6), G675–G685 (2012).
  • Chen Y, Yang F, Lu H et al. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54(2), 562–572 (2011).
  • Bajaj JS, Ridlon JM, Hylemon PB et al. Linkage of gut microbiome with cognition in hepatic encephalopathy. Am. J. Physiol. Gastrointest. Liver Physiol. 302(1), G168–G175 (2012).
  • Lu H, Wu Z, Xu W et al. Intestinal microbiota was assessed in cirrhotic patients with hepatitis B virus infection. Intestinal microbiota of HBV cirrhotic patients. Microb. Ecol. 61(3), 693–703 (2011).
  • Liu J, Wu D, Ahmed A et al. Comparison of the gut microbe profiles and numbers between patients with liver cirrhosis and healthy individuals. Curr. Microbiol. 65(1), 7–13 (2012).
  • Xu M, Wang B, Fu Y et al. Changes of fecal Bifidobacterial species in adult patients with hepatitis B-Virus-induced chronic liver diseases. Microb. Ecol. 63(2), 304–313 (2012).
  • Machado MV, Cortez-Pinto H. Gut microbiota and nonalcoholic fatty liver disease. Ann. Hepatol. 11(4), 440–449 (2012).
  • Turnbaugh PJ, Ley RE, Mahowald MA et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122), 1027–1031 (2006).
  • Turnbaugh PJ, Gordon JI. The core gut microbiome, energy balance and obesity. J. Physiol. 587(Pt. 17), 4153–4158 (2009).
  • Turnbaugh PJ, Hamady M, Yatsunenko T et al. A core gut microbiome in obese and lean twins. Nature 457(7228), 480–484 (2009).
  • Ley RE, Backhed F, Turnbaugh P et al. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA 102(31), 11070–11075 (2005).
  • Murphy EF, Cotter PD, Healy S et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59(12), 1635–1642 (2010).
  • Parks BW, Nam E, Org E, Kostem E et al. Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. Cell Metab. 17(1), 141–152 (2013).
  • Everard A, Belzer C, Geurts L et al. Cross-talk between Akkermanansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl Acad. Sci. USA 110(22), 9066–9071 (2013).
  • Greenblum S, Turnbaugh PJ, Borenstein E. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc. Natl Acad. Sci. USA 109(2), 594–599 (2012).
  • De Vos WM, Nieuwdorp M. A gut prediction. Nature 498, 48–49 (2013).
  • Karlsson FH, Tremaroli V, Nookaew I et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498(7452), 99–103 (2013).
  • 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 7(8), e43052 (2012).
  • Penas-Steinhardt A, Barcos LS, Belforte FS et al. Functional characterization of TLR4 +3725G/C polymorphism and association with protection against overweight. PLoS ONE 7(12), e50992 (2012).
  • Kim KA, Gu W, Lee IA et al. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signalling pathway. PLoS ONE 7(10), e47713 (2012).
  • Vijay-Kumar M, Aitken JD, Carvalho FA et al. Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science 328(5975), 228–231 (2010).
  • Li JV, Ashrafian H, Bueter M et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 60(9), 1214–1223 (2011).
  • Liou AP, Paziul M, Luevano JM Jr et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med. 5(178), 178ra41 (2013).
  • Wong VW, Tse CH, Lam TT et al. Molecular characterization of the fecal micrbiota in patients with nonalcoholic steatohepatitis – a longitudinal study. PLoS ONE 8(4), e62885 (2013).
  • Raman M, Ahmed I, Gillevet PM et al. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic Fatty liver disease. Clin. Gastroenterol. Hepatol. 11(7), 868–875.e1–3 (2013).
  • 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 57(2), 601–609 (2013).
  • Le Roy T, Llopis M, Lepage P et al. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut doi: 10.1136/gutjnl-2012-303816 (2012) ( epub ahead of print).
  • Spencer MD, Hamp TJ, Reid RW et al. Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology 140(3), 976–986 (2011).
  • Mouzaki M, Comelli EM, Arendt BM et al. Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology 58(1), 120–127 (2013).
  • Henao-Mejia J, Elinav E, Jin C et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482(7384), 179–185 (2012).
  • Cesaro C, Tiso A, Del Prete A et al. Gut microbiota and probiotics in chronic liver diseases. Dig. Liver Dis. 43(6), 431–438 (2011).
  • Pastor Rojo O, Lopez San Roman A, Albeniz A et al. Serum lipopolysaccharide–binding protein in endotoxemic patients with inflammatory bowel disease. Inflamm. Bowel Dis. 13(3), 269–277 (2007).
  • Wang AP, Migita K, Ito M et al. Hepatic expression of toll–like receptor 4 in primary biliary cirrhosis. J. Autoimmun. 25(1), 85–91 (2005).
  • Hopf U, Möller B, Stemerowicz R et al. Relation between Escherichia coli R (rough)-forms in gut, lipid A in liver, and primary biliary cirrhosis. Lancet 2(8677), 1419–1422 (1989).
  • Bogdanos DP, Baum H, Grasso A et al. Microbial mimics are major targets of crossreactivity with human pyruvate dehydrogenase in primary biliary cirrhosis. J. Hepatol. 40(1), 31–39 (2004).
  • Bogdanos DP, Baum H, Okamoto M et al. Primary biliary cirrhosis is characterized by IgG3 antibodies cross-reactive with the major mitochondrial autoepitope and its Lactobacillus mimic. Hepatology. 42(2), 458–465 (2005).
  • Fox JG, Feng Y, Theve EJ et al. Gut microbes define liver cancer risk in mice exposed to chemical and viral transgenic heptocarcinogenesis. Gut 59(1), 88–97 (2010).
  • Yoshimoto S, Loo TM, Atarashi K et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499(7456), 97–101 (2013).
  • Bindels IB, Porporato P, Dewulf EM et al. Gut microbiota-derives propionate reduces cancer cell proliferation in the liver. Br. J. Cancer 107(8), 1337–1344 (2012).
  • Almeida J, Galhenage S, Yu J, Kurtovic J et al. Gut flora and bacterial translocation in chronic liver disease. World J. Gastroenterol. 12(10), 1493–1502 (2006).
  • Rasaratnam B, Connelly N, Chin-Dusting J. Nitric oxide and the hyperdynamic circulation in cirrhosis: is there a role for selective intestinal decontamination? Clin. Sci (Lond). 107(5), 425–434 (2004).
  • Cohen MJ, Sahar T, Benenson S et al. Antibiotic prophylaxis for spontaneous bacterial peritonitis in cirrhotic patients with ascites, without gastro-intestinal bleeding. Cochrane Database Syst. Rev. (2), CD004791 (2009).
  • Chavez-Tapia NC, Barrientos-Gutierrez T, Tellez-Avila FI et al. Antibiotic prophylaxis for cirrhotic patients with upper gastrointestinal bleeding. Cochrane Database Syst. Rev. (9), CD002907 (2010).
  • Bass NM, Mullen KD, Sanyal A et al. Rifaximin treatment in hepatic encephalopathy. N. Engl. J. Med. 362, 1071–1081 (2010).
  • Sidhu SS, Goyal O, Mishra BP et al. Rifaximin improves psychometric performance and health-related quality of life in patients with minimal hepatic encephalopathy (the RIME Trial). Am. J. Gastroenterol. 106(2), 307–316 (2011).
  • Garcovich M, Zocco MA, Roccarina D et al. Prevention and treatment of hepatic encephalopathy: focusing on the gut microbiota. World J. Gastroenterol. 18(46), 6693–6770 (2012).
  • Bajaj JS, Heumann DM, Sanyal AJ et al. Modulation of the metabolome by rifaximin in patients with cirrhosis and minimal hepatic encephalopathy. PloS ONE 8(4), e60042 (2013).
  • Ridlon JM, Alves JM, Hylemon PB et al. Cirrhosis, bile acids, and gut microbiota: unraveling a complex relationship. Gut Microbes 4(5) (2013).
  • Barclay AR, Beattie LM, Weaver LT et al. Systematic review: medical and nutritional interventions for the management of intestinal failure and its resultant complications in children. Aliment. Pharmacol. Ther. 33(2), 175–184 (2011).
  • Li Z, Yang S, Lin H, Huang J et al. Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatology 37(2), 343–350 (2003).
  • Ma X, Hua J, Li Z. Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J. Hepatol. 49(5), 821–830 (2008).
  • Velayudham A, Dolganiuc A, Ellis M et al. VSL#3 probiotic treatment attenuates fibrosis without changes in steatohepatitis in a diet-induced nonalcoholic steatohepatitis model in mice. Hepatology 49(3), 989–997 (2009).
  • Xu RY, Wan YP, Fang QY et al. Supplementation with probiotics modifies gut flora and attenuates liver fat accumulation in rat nonalcoholic fatty liver disease model. J. Clin. Biochem. Nutr. 50(1), 72–77 (2012).
  • Cani PD, Possemiers S, Van den Wiele T et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58(8), 1091–1103 (2009).
  • Forsyth CB, Farhadi A, Jakate SM et al. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43(2), 163–172 (2009).
  • Wang Y, Liu Y, Sidhu A et al. Lactobacillus rhamnosus GG culture supernatant ameliorates acute alcohol-induced intestinal permeability and liver injury. Am. J. Physiol. Gastrointest. Liver Physiol. 303(1), G32–G41 (2012).
  • Wang Y, Kirpich I, Liu Y et al. Lactobacillus rhamnosus GG treatment potentiates intestinal hypoxia-inducible factor, promotes intestinal integrity and ameliorates alcohol-induced liver injury. Am. J. Pathol. 179(6), 2866–2875 (2011).
  • Magna L, Del Piano M, Deidda F et al. Assessment of the in vitro inhibitory activity of specific probiotic bacteria against different Escherichia coli strains. J. Clin. Gastroenterol. 46( Suppl. 46), S29–S32 (2012).
  • Osman N, Adawi D, Ahrné S et al. Endotoxin- and D-galactosamine-induced liver injury improved by the administration of Lactobacillus, Bifidobacterium and blueberry. Dig. Liver Dis. 39(9), 849–856 (207).
  • Forsyth CB, Farhadi A, Jakate SM et al. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43(2), 163–172 (2009).
  • Kirpich IA, Solovieva NV, Leikhter SN et al. Probiotics restore bowel flora and improve liver enzymes in human alcohol-induced liver injury: a pilot study. Alcohol 42(8), 675–682 (2008).
  • Lata J, Jurankova J, Kopacova M et al. Probiotics in hepatology. World J. Gastroenterol. 17(24), 2890–2896 (2011).
  • Nardone G, Compare D, Liguori E et al. Protective effects of Lactobacillus paracasei F19 in a rat model of oxidative and metabolic hepatic injury. Am. J. Physiol. Gastrointest. Liver Physiol. 299(3), G669–G676 (2010).
  • Gratz SW, Mykkanen H, El-Nezami HS. Probiotics and gut health: a special focus on liver diseases. World J. Gastroenterol. 16(4), 403–410 (2010).
  • Lirussi F, Mastropasqua E, Orando S et al. Probiotics for non-alcoholic fatty liver disease and/or steatohepatitis. Cochrane Database Syst. Rev. (1), CD005165 (2007).
  • Jayakumar S, Carbonneau M, Hotte N et al. VSL#3® probiotic therapy does not reduce portal pressures in patients with decompensated cirrhosis. Liver Int. doi:10.1111/liv.12280 (2013) ( Epub ahead of print).
  • McGee RG, Bakens A, Wiley K et al. Probiotics for patients with encephalopthay. Cochrane Database Syst. Rev. (11), CD008716 (2011).
  • Shukla S, Shukla A, Mehboob S et al. Meta-analysis: the effects of gut flora modulation using prebiotics, probiotics and synbiotics on minimal hepatic encephalopathy. Aliment. Pharmacol. Ther. 33(6), 662–671 (2011).
  • Liu Q, Duan ZP, Ha DK, Bengmark S et al. Synbiotic modulation of gut flora: effect on minimal hepatic encephalopathy in patients with cirrhosis. Hepatology 39(5), 1441–1449 (2004).
  • Vrieze A, Van Nood E, Holleman F et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143(4), 913–916 (2012).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.