Journal Article
. 2012 Oct; 3:402.
doi: 10.3389/fphys.2012.00402.

The intestinal microbiome and the leaky gut as therapeutic targets in alcoholic liver disease

Phillipp Hartmann 1 Wei-Chung Chen  Bernd Schnabl  
Affiliations
  • PMID: 23087650
  •     142 References
  •     46 citations

Abstract

Alcoholic liver disease (ALD) encompasses hepatic steatosis, which may progress to alcoholic hepatitis, fibrosis, and cirrhosis. It remains a leading cause of morbidity and mortality in the US and worldwide. The severity of liver disease correlates with plasma levels of bacterial products in patients, and experimental ALD depends on the level of gut derived bacterial products in rodents. Since intestinal decontamination and deficiency of bacterial product receptors or their downstream signaling molecules protect from alcohol-induced liver disease, bacterial translocation (BT), qualitative, and quantitative changes of the enteric microbiome are considered as being of fundamental importance in the pathogenesis of ALD. Recent enhancements in diagnostic technologies provide a better insight into these shifts. This review highlights vital events in ALD such as BT, the importance of Toll-like receptor (TLR) signaling, intestinal bacterial overgrowth (IBO), and changes in the intestinal microbiome. Furthermore, a treatment trial section of patients reviews possible future options of therapy for ALD modifying the enteric microbiome.

Keywords: alcoholic liver disease; bacterial dysbiosis; bacterial overgrowth; bacterial translocation; microbiome; steatohepatitis.

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Recent Advances in Alcoholic Liver Disease I. Role of intestinal permeability and endotoxemia in alcoholic liver disease.
R K Rao, A Seth, P Sheth.
Am J Physiol Gastrointest Liver Physiol, 2004 May 11; 286(6). PMID: 15132946
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Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease.
Luca Miele, Venanzio Valenza, +12 authors, Antonio Grieco.
Hepatology, 2009 Mar 18; 49(6). PMID: 19291785
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Toll-like receptor-4 mediates obesity-induced non-alcoholic steatohepatitis through activation of X-box binding protein-1 in mice.
Dewei Ye, Francois Y L Li, +7 authors, Aimin Xu.
Gut, 2012 Jan 19; 61(7). PMID: 22253482
Bacterial translocation and peptidoglycan translocation by acute ethanol administration.
Takahisa Tabata, Tohru Tani, Yoshihiro Endo, Kazuyoshi Hanasawa.
J Gastroenterol, 2002 Oct 11; 37(9). PMID: 12375146
Beneficial effects of a probiotic VSL#3 on parameters of liver dysfunction in chronic liver diseases.
Carmela Loguercio, Alessandro Federico, +4 authors, Camillo Del Vecchio Blanco.
J Clin Gastroenterol, 2005 Jun 09; 39(6). PMID: 15942443
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Infections in patients with cirrhosis increase mortality four-fold and should be used in determining prognosis.
Vasiliki Arvaniti, Gennaro D'Amico, +4 authors, Andrew Kenneth Burroughs.
Gastroenterology, 2010 Jun 19; 139(4). PMID: 20558165
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Effect of antibiotics, prebiotics and probiotics in treatment for hepatic encephalopathy.
Ger Bongaerts, René Severijnen, Harro Timmerman.
Med Hypotheses, 2004 Nov 10; 64(1). PMID: 15533613
Effect of endotoxin pretreatment on hepatic stellate cell response to ethanol and acetaldehyde.
S C Quiroz, L Bucio, +6 authors, M C Gutiérrez-Ruiz.
J Gastroenterol Hepatol, 2002 Mar 21; 16(11). PMID: 11903746
Plasma endotoxin concentrations in patients with alcoholic and non-alcoholic liver disease: reevaluation with an improved chromogenic assay.
H Fukui, B Brauner, J C Bode, C Bode.
J Hepatol, 1991 Mar 01; 12(2). PMID: 2050995
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Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2.
A O Aliprantis, R B Yang, +6 authors, A Zychlinsky.
Science, 1999 Jul 31; 285(5428). PMID: 10426996
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Small intestinal motility disturbances and bacterial overgrowth in patients with liver cirrhosis and portal hypertension.
Steingerdur Anna Gunnarsdottir, Riadh Sadik, +6 authors, Einar S Björnsson.
Am J Gastroenterol, 2003 Jun 24; 98(6). PMID: 12818282
Production and excretion of hydrogen gas in man.
M D Levitt.
N Engl J Med, 1969 Jul 17; 281(3). PMID: 5790483
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Reduced early alcohol-induced liver injury in CD14-deficient mice.
M Yin, B U Bradford, +4 authors, R G Thurman.
J Immunol, 2001 Mar 20; 166(7). PMID: 11254735
Experimental acute alcohol pancreatitis-related liver damage and endotoxemia: synbiotics but not metronidazole have a protective effect.
F Marotta, R Barreto, +5 authors, E Fesce.
Chin J Dig Dis, 2005 Oct 26; 6(4). PMID: 16246229
Ciprofloxacin in primary prophylaxis of spontaneous bacterial peritonitis: a randomized, placebo-controlled study.
Rubén Terg, Eduardo Fassio, +10 authors, Raquel Abecasis.
J Hepatol, 2008 Mar 05; 48(5). PMID: 18316137
S-adenosyl-L-methionine attenuates oxidative stress and hepatic stellate cell activation in an ethanol-LPS-induced fibrotic rat model.
Amel Karaa, Kyle J Thompson, +2 authors, Laura W Schrum.
Shock, 2008 Jan 09; 30(2). PMID: 18180699
Effect of alcohol consumption on the gut.
Christiane Bode, J Christian Bode.
Best Pract Res Clin Gastroenterol, 2003 Jun 28; 17(4). PMID: 12828956
Review.
Oral bile acids reduce bacterial overgrowth, bacterial translocation, and endotoxemia in cirrhotic rats.
Vicente Lorenzo-Zúñiga, Ramón Bartolí, +8 authors, Miquel Angel Gassull.
Hepatology, 2003 Feb 26; 37(3). PMID: 12601352
Severity of liver injury in experimental alcoholic liver disease. Correlation with plasma endotoxin, prostaglandin E2, leukotriene B4, and thromboxane B2.
A A Nanji, U Khettry, S M Sadrzadeh, T Yamanaka.
Am J Pathol, 1993 Feb 01; 142(2). PMID: 8382006    Free PMC article.
Breath hydrogen testing in bacterial overgrowth of the small intestine.
P Kerlin, L Wong.
Gastroenterology, 1988 Oct 01; 95(4). PMID: 3410238
Lactobacillus feeding reduces endotoxemia and severity of experimental alcoholic liver (disease).
A A Nanji, U Khettry, S M Sadrzadeh.
Proc Soc Exp Biol Med, 1994 Mar 01; 205(3). PMID: 8171045
Highly Cited.
Diversity of the human intestinal microbial flora.
Paul B Eckburg, Elisabeth M Bik, +6 authors, David A Relman.
Science, 2005 Apr 16; 308(5728). PMID: 15831718    Free PMC article.
Highly Cited.
Role of TLR9 in hepatic stellate cells and experimental liver fibrosis.
Erwin Gäbele, Marcus Mühlbauer, +7 authors, Claus Hellerbrand.
Biochem Biophys Res Commun, 2008 Sep 02; 376(2). PMID: 18760996
Prospective evaluation of alcohol abuse and alcoholic liver injury in men as predictors of development of cirrhosis.
T I Sørensen, M Orholm, +3 authors, P Christoffersen.
Lancet, 1984 Aug 04; 2(8397). PMID: 6146805
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Metagenomic analysis of the human distal gut microbiome.
Steven R Gill, Mihai Pop, +7 authors, Karen E Nelson.
Science, 2006 Jun 03; 312(5778). PMID: 16741115    Free PMC article.
Highly Cited.
LPS signaling enhances hepatic fibrogenesis caused by experimental cholestasis in mice.
Fuyumi Isayama, Ian N Hines, +7 authors, Michael D Wheeler.
Am J Physiol Gastrointest Liver Physiol, 2006 Jan 28; 290(6). PMID: 16439470
Clinical syndromes of alcoholic liver disease.
Masayuki Adachi, David A Brenner.
Dig Dis, 2006 Mar 02; 23(3-4). PMID: 16508290
Review.
EFFECTS OF PROLONGED ETHANOL INTAKE: PRODUCTION OF FATTY LIVER DESPITE ADEQUATE DIETS.
C S LIEBER, D P JONES, L M DECARLI.
J Clin Invest, 1965 Jun 01; 44. PMID: 14322019    Free PMC article.
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Linking intestinal homeostasis and liver disease.
Bernd Schnabl.
Curr Opin Gastroenterol, 2013 Mar 16; 29(3). PMID: 23493073    Free PMC article.
Review.
Splanchnic-aortic inflammatory axis in experimental portal hypertension.
Maria-Angeles Aller, Natalia de las Heras, +3 authors, Vicente Lahera.
World J Gastroenterol, 2013 Dec 07; 19(44). PMID: 24307792    Free PMC article.
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Altered profile of human gut microbiome is associated with cirrhosis and its complications.
Jasmohan S Bajaj, Douglas M Heuman, +9 authors, Patrick M Gillevet.
J Hepatol, 2014 Jan 01; 60(5). PMID: 24374295    Free PMC article.
Highly Cited.
Interactions between the intestinal microbiome and liver diseases.
Bernd Schnabl, David A Brenner.
Gastroenterology, 2014 Jan 21; 146(6). PMID: 24440671    Free PMC article.
Highly Cited. Review.
Changes in gut bacterial populations and their translocation into liver and ascites in alcoholic liver cirrhotics.
Sari Tuomisto, Tanja Pessi, +3 authors, Pekka J Karhunen.
BMC Gastroenterol, 2014 Feb 26; 14. PMID: 24564202    Free PMC article.
From genomes to societies: a holistic view of determinants of human health.
Yuyan Shi, Sheng Zhong.
Curr Opin Biotechnol, 2014 Apr 02; 28. PMID: 24686286    Free PMC article.
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The role of microbiota in hepatic encephalopathy.
Jasmohan S Bajaj.
Gut Microbes, 2014 Apr 03; 5(3). PMID: 24690956    Free PMC article.
Review.
Host-microbiome interactions in alcoholic liver disease.
Peng Chen, Bernd Schnabl.
Gut Liver, 2014 May 16; 8(3). PMID: 24827618    Free PMC article.
Review.
Acute binge drinking increases serum endotoxin and bacterial DNA levels in healthy individuals.
Shashi Bala, Miguel Marcos, +2 authors, Gyongyi Szabo.
PLoS One, 2014 May 16; 9(5). PMID: 24828436    Free PMC article.
Highly Cited.
Role of toll-like receptors in immune activation and tolerance in the liver.
Nobuhiro Nakamoto, Takanori Kanai.
Front Immunol, 2014 Jun 07; 5. PMID: 24904576    Free PMC article.
Review.
Serum metabolomic profiling in acute alcoholic hepatitis identifies multiple dysregulated pathways.
Vikrant Rachakonda, Charles Gabbert, +4 authors, Jaideep Behari.
PLoS One, 2014 Dec 03; 9(12). PMID: 25461442    Free PMC article.
Toll-like receptor-mediated signaling cascade as a regulator of the inflammation network during alcoholic liver disease.
Sara Ceccarelli, Valerio Nobili, Anna Alisi.
World J Gastroenterol, 2014 Dec 04; 20(44). PMID: 25469012    Free PMC article.
Review.
Alcoholic liver disease: the gut microbiome and liver cross talk.
Phillipp Hartmann, Caroline T Seebauer, Bernd Schnabl.
Alcohol Clin Exp Res, 2015 Apr 16; 39(5). PMID: 25872593    Free PMC article.
Highly Cited. Review.
The gut microbiota and liver disease.
Cristina Llorente, Bernd Schnabl.
Cell Mol Gastroenterol Hepatol, 2015 Jun 20; 1(3). PMID: 26090511    Free PMC article.
Highly Cited.
Influence of gut bacteria on development and progression of non-alcoholic fatty liver disease.
Ali Abdul-Hai, Ali Abdallah, Stephen Dh Malnick.
World J Hepatol, 2015 Jul 04; 7(12). PMID: 26140087    Free PMC article.
Review.
The role of the gut-brain axis in alcohol use disorders.
Jonathan Gorky, James Schwaber.
Prog Neuropsychopharmacol Biol Psychiatry, 2015 Jul 19; 65. PMID: 26188287    Free PMC article.
Review.
New drug targets for alcoholic liver disease.
Mingjiang Xu, Binxia Chang, Stephanie Mathews, Bin Gao.
Hepatol Int, 2015 Jul 24; 8 Suppl 2. PMID: 26201327    Free PMC article.
Alcoholic Liver Disease: Role of Cytokines.
Manuela G Neuman, Yaakov Maor, +5 authors, Stephen Malnick.
Biomolecules, 2015 Sep 08; 5(3). PMID: 26343741    Free PMC article.
Review.
Chronic Alcohol Exposure Enhances Lipopolysaccharide-Induced Lung Injury in Mice: Potential Role of Systemic Tumor Necrosis Factor-Alpha.
Veronica L Massey, Lauren G Poole, +6 authors, Gavin E Arteel.
Alcohol Clin Exp Res, 2015 Sep 19; 39(10). PMID: 26380957    Free PMC article.
Potential Role of the Gut/Liver/Lung Axis in Alcohol-Induced Tissue Pathology.
Veronica L Massey, Juliane I Beier, +2 authors, Gavin E Arteel.
Biomolecules, 2015 Oct 06; 5(4). PMID: 26437442    Free PMC article.
Review.
Metabolic derivatives of alcohol and the molecular culprits of fibro-hepatocarcinogenesis: Allies or enemies?
Alex Boye, Yu-Hong Zou, Yan Yang.
World J Gastroenterol, 2016 Jan 13; 22(1). PMID: 26755860    Free PMC article.
Review.
Gut Microbiota of Nonalcoholic Fatty Liver Disease.
Reham M Abdou, Lixin Zhu, Robert D Baker, Susan S Baker.
Dig Dis Sci, 2016 Feb 24; 61(5). PMID: 26898658
Review.
Microbiota-based treatments in alcoholic liver disease.
Hotaik Sung, Seung Woo Kim, Meegun Hong, Ki Tae Suk.
World J Gastroenterol, 2016 Aug 23; 22(29). PMID: 27547010    Free PMC article.
Review.
Precision medicine in alcoholic and nonalcoholic fatty liver disease via modulating the gut microbiota.
Sena Bluemel, Brandon Williams, Rob Knight, Bernd Schnabl.
Am J Physiol Gastrointest Liver Physiol, 2016 Oct 01; 311(6). PMID: 27686615    Free PMC article.
Review.
Gut Microbiota and Complications of Liver Disease.
Chathur Acharya, Jasmohan S Bajaj.
Gastroenterol Clin North Am, 2017 Feb 07; 46(1). PMID: 28164848    Free PMC article.
Review.
Immunoglobulin A and liver diseases.
Tatsuo Inamine, Bernd Schnabl.
J Gastroenterol, 2017 Oct 28; 53(6). PMID: 29075899    Free PMC article.
Review.
Inflammasome in drug abuse.
Enquan Xu, Jianuo Liu, Xiaobei Wang, Huangui Xiong.
Int J Physiol Pathophysiol Pharmacol, 2018 Jan 20; 9(6). PMID: 29348793    Free PMC article.
Risk factors for progression of and treatment options for NAFLD in children.
Phillipp Hartmann, Bernd Schnabl.
Clin Liver Dis (Hoboken), 2018 Apr 10; 11(1). PMID: 29629177    Free PMC article.
Immune checkpoint receptors: homeostatic regulators of immunity.
Antonio Riva, Shilpa Chokshi.
Hepatol Int, 2018 May 10; 12(3). PMID: 29740793    Free PMC article.
Review.
Interactions of Gut Microbiota, Endotoxemia, Immune Function, and Diet in Exertional Heatstroke.
Lawrence E Armstrong, Elaine C Lee, Elizabeth M Armstrong.
J Sports Med (Hindawi Publ Corp), 2018 Jun 01; 2018. PMID: 29850597    Free PMC article.
Review.
The Immunologic Role of Gut Microbiota in Patients with Chronic HBV Infection.
Ruilin Yang, Yao Xu, +2 authors, Huichao Wang.
J Immunol Res, 2018 Aug 28; 2018. PMID: 30148173    Free PMC article.
Review.
Probiotic and glutamine treatments attenuate alcoholic liver disease in a rat model.
Huping Huang, Zhihui Lin, +2 authors, Yali Zhang.
Exp Ther Med, 2019 Nov 30; 18(6). PMID: 31777560    Free PMC article.
Divergent Roles of Kupffer Cell TLR2/3 Signaling in Alcoholic Liver Disease and the Protective Role of EGCG.
Pingping Luo, Fei Wang, +9 authors, Hua Wang.
Cell Mol Gastroenterol Hepatol, 2019 Sep 29; 9(1). PMID: 31562937    Free PMC article.
Chinese tree shrews as a primate experimental animal eligible for the study of alcoholic liver disease: characterization and confirmation by MRI.
Zhihai Shi, Huijie Xing, +3 authors, Xingwang Zhang.
Exp Anim, 2019 Sep 27; 69(1). PMID: 31554748    Free PMC article.
The role of the gut microbiome in chronic liver disease: the clinical evidence revised.
Katherine Jp Schwenger, Nayima Clermont-Dejean, Johane P Allard.
JHEP Rep, 2020 Feb 11; 1(3). PMID: 32039372    Free PMC article.
Review.
Macrophages in the Aging Liver and Age-Related Liver Disease.
Elizabeth C Stahl, Martin J Haschak, Branimir Popovic, Bryan N Brown.
Front Immunol, 2018 Dec 18; 9. PMID: 30555477    Free PMC article.
Review.
A single alcohol binge impacts on neutrophil function without changes in gut barrier function and gut microbiome composition in healthy volunteers.
Vanessa Stadlbauer, Angela Horvath, +11 authors, Bettina Leber.
PLoS One, 2019 Feb 02; 14(2). PMID: 30707717    Free PMC article.
Gut microbiota in liver disease: too much is harmful, nothing at all is not helpful either.
Phillipp Hartmann, Huikuan Chu, Yi Duan, Bernd Schnabl.
Am J Physiol Gastrointest Liver Physiol, 2019 Feb 16; 316(5). PMID: 30767680    Free PMC article.
Review.
Alox12/15 Deficiency Exacerbates, While Lipoxin A4 Ameliorates Hepatic Inflammation in Murine Alcoholic Hepatitis.
Alexander Queck, Annika F Fink, +10 authors, Bernhard Brüne.
Front Immunol, 2020 Aug 08; 11. PMID: 32760397    Free PMC article.
Tumor necrosis factor alpha receptor 1 deficiency in hepatocytes does not protect from non-alcoholic steatohepatitis, but attenuates insulin resistance in mice.
Sena Bluemel, Yanhan Wang, Suhan Lee, Bernd Schnabl.
World J Gastroenterol, 2020 Sep 22; 26(33). PMID: 32952340    Free PMC article.
Alcoholic liver disease: A current molecular and clinical perspective.
Koichiro Ohashi, Michael Pimienta, Ekihiro Seki.
Liver Res, 2019 Jun 20; 2(4). PMID: 31214376    Free PMC article.
Pathogenesis, Early Diagnosis, and Therapeutic Management of Alcoholic Liver Disease.
Ling-Zu Kong, Nisansala Chandimali, +8 authors, Taeho Kwon.
Int J Mol Sci, 2019 Jun 05; 20(11). PMID: 31159489    Free PMC article.
Review.
The role of gut vascular barrier in experimental alcoholic liver disease and A. muciniphila supplementation.
Christoph Grander, Felix Grabherr, +4 authors, Herbert Tilg.
Gut Microbes, 2021 Jan 01; 12(1). PMID: 33382359    Free PMC article.
New Developments in Microbiome in Alcohol-Associated and Nonalcoholic Fatty Liver Disease.
Phillipp Hartmann, Bernd Schnabl.
Semin Liver Dis, 2021 May 07; 41(1). PMID: 33957682    Free PMC article.
Dynamic Changes of the Fungal Microbiome in Alcohol Use Disorder.
Phillipp Hartmann, Sonja Lang, +8 authors, Bernd Schnabl.
Front Physiol, 2021 Aug 06; 12. PMID: 34349667    Free PMC article.
Hypoxia: The "Invisible Pusher" of Gut Microbiota.
Ni Han, Zhiyuan Pan, +2 authors, Bi Yujing.
Front Microbiol, 2021 Aug 10; 12. PMID: 34367091    Free PMC article.
Review.