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The Role of the Gut Microbiome in Chronic Liver Disease: the Clinical Evidence Revised

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The Role of the Gut Microbiome in Chronic Liver Disease: the Clinical Evidence Revised Review The role of the gut microbiome in chronic liver disease: the clinical evidence revised Katherine JP Schwenger,1,2 Nayima Clermont-Dejean,1 Johane P. Allard1,2,3,* Keywords: microbiome; Summary microbiota; intestinal Recent research has suggested a role for the intestinal microbiota in the pathogenesis and potential microbiota; liver diseases; treatment of a wide range of liver diseases. The intestinal microbiota and bacterial products may prebiotics; probiotics; fecal contribute to the development of liver diseases through multiple mechanisms including increased transplantation; synbiotics; gut-liver axis. intestinal permeability, chronic systemic inflammation,productionofshort-chainfattyacidsand changes in metabolism. This suggests a potential role for pre-, pro- and synbiotic products in the Received 2 January 2019; prevention or treatment of some liver diseases. In addition, there is emerging evidence on the effects received in revised form 8 April 2019; accepted 27 of faecal microbial transplant. Herein, we discuss the relationship between the intestinal microbiota April 2019; available and liver diseases, as well as reviewing intestinal microbiota-based treatment options that are online 31 July 2019 currently being investigated. © 2019 The Author(s). Published by Elsevier B.V. on behalf of European Association for the Study of the Liver (EASL). This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). Introduction and cirrhosis. This review will focus on clinical The human intestinal microbiota (IM) is made up of data and interventions for each of these pathologies. bacteria, archaea and eukaryotic microorganisms and viruses.1,2 Currently, there are 1,000 known Intestinal microbiota and liver disease: species of bacteria3 and approximately 1014 micro- Overall mechanisms 4 organisms. Two dominant phyla, Bacteroidetes Bile acid metabolism and Firmicutes, comprise 90% of bacteria in the Synthesised from cholesterol in the liver, bile acids 5–7 human digestive tract. The IM plays an essential (BAs) are essential in cholesterol metabolism and role in the digestion of food, synthesis of vitamins, lipid digestion.15 BAs are stored in the gallbladder metabolism, immune system function, inflamma- and are secreted during digestion into the small 4,8,9 tion and cell proliferation. Recently, dis- intestine.16 Over 95% of BAs are reabsorbed in turbances in the IM, or dysbiosis, have been the terminal ileum and transported back to the associated with several diseases, including a wide liver via the portal vein. BAs promote the absorp- 4,9–12 range of hepatic disorders. tion of dietary fats, cholesterol and fat-soluble Emerging evidence supports the bidirectional vitamins.16 In addition, BAs also function as signal- relationship between the IM and the liver, which ling molecules that influence physiological pro- results from the liver receiving 75% of its blood sup- cesses,16 which include the regulation of glucose ply from the intestines via the portal vein13 and the and lipid metabolism through farnesoid X receptor liver releasing bile acids into the biliary tract.14 As a (FXR) activation and binding of G-protein-coupled – result, the IM may contribute to liver diseases bile acid receptor 1.17 19 BAs can also influence through several mechanisms that can be influenced the IM as it has been shown to be directly asso- 1Toronto General Hospital, by bacterial composition, IM metabolism of bile ciated with intestinal mucosal integrity and synthe- University Health Network, 20 Toronto, Canada; acids, diet, environmental factors and genetics, sis of antibacterial peptides. When BAs bind to 2Department of Medicine, with bacteria, bacterial products and metabolites FXR, antimicrobial peptides, such as angiogenin 1, University of Toronto, Toronto, translocating through the intestinal barrier into are produced. These peptides can inhibit IM over- Canada; 3 11,12 Department of Nutritional the portal system, and then the liver. growth by increasing the intestinal epithelial cell Sciences, University of Toronto, The aim of this review is to outline how the IM potential to prevent bacterial uptake, improving Toronto, Canada and liver interact with each other. We will focus gut-barrier function.20 In turn, the IM can influence *Corresponding author. on the IM’s role in the pathogenesis and treatment the size and composition of the BA pool through Address: Toronto General Hospi- of liver diseases, specifically non-alcoholic fatty the conversion of primary to secondary BAs.21,22 tal, 585 University Avenue, 9-973, liver disease (NAFLD), alcohol-related liver disease This may subsequently change the composition of Toronto, ON M5G 2C4; Tel.: 416- 340-5159, fax: 416-348-0065. (ALD), primary sclerosing cholangitis, primary the circulating BAs, which act as signalling mole- E-mail address: Dr.Johane.Allar- biliary cholangitis, hepatocellular carcinoma (HCC) cules affecting, for example, lipid and glucose [email protected] (J. Allard). Review metabolism and predisposing individuals to non- Key points alcoholic fatty liver disease (NAFLD). Therefore, The intestinal microbiota and bacterial products can directly and indirectly affect the liver both the dysbiosis of IM and/or imbalance of BAs through various mechanisms, leading to a wide variety of liver diseases. can contribute to the pathogenesis and progression This suggests a potential role for pre-, pro- and synbiotic products in the prevention or treat- 21,22 of liver diseases, which will be discussed. ment of some liver diseases. There is also emerging evidence that faecal microbiota transplant may be an effective treat- Intestinal permeability ment for certain liver diseases. The intestinal epithelium plays an essential role in restricting toxins, antigens and enteric flora from entering the circulation, while selectively permitting systems. The innate immune system defends against the absorption of nutrients across the tight microorganisms and toxins, whereas the adaptive junctions.23 The intestinal barrier is comprised of immune system is antigen specific and requires enterocytes that are bound to each other by trans- self-non-self-recognition.28 Kupffer cells (KCs) are membrane proteins including desmosomes, adhe- critical components of the innate immune system, rens junctions and tight junctions.23 The intestinal residing within the sinusoidal vascular space.29 barrier is also strengthened by immunoglobulins, KCs can be activated by various endogenous and mucins and commensal bacteria.23 The IM can alter exogenous stimuli including endotoxins.29 Activa- the intestinal barrier by altering tight junctions, tion of KCs triggers the production of inflammatory degrading the mucus layer or inhibiting the produc- cytokines, such as TNF-α,aswellasreactiveoxygen tion of mucus, which subsequently increases the species (ROS)29 which can produce tissue damage. permeability of the epithelium.23 One way in These cytokines can also play a key role in regulat- which the IM is associated with increased tight junc- ing the phenotype and function of neighbouring tion permeability is through the presence of luminal parenchymal and non-parenchymal cells.29 For endotoxins.23 Endotoxins found on the outer mem- instance, cytokines have been shown to polarise brane of gram-negative bacteria increase tight junc- and activate the proinflammatory M1 phenotype tion permeability by increasing toll-like receptor in KCs.30 (TLR)4 expression.24 Widening of the tight junctions Natural killer (NK) and natural killer T (NKT) cells leads to increased intestinal permeability, resulting may also play a role in the pathogenesis of liver in increased translocation of bacterial fragments diseases and can be affected by the IM. Recent and endotoxins into the portal circulation and subse- murine studies have shown that IM-derived anti- quently the liver.25 This in turn can cause systemic gens could influence the composition and activation and hepatic inflammation and hepatic injury.25 of hepatic NKT cells.31,32 NK cells in the liver play a Bacterial fragments and products can also recruit role in linking the innate and adaptive immune and activate hepatic immune cells, further contribut- response.33 Activated NK cells were found to ing to liver disease progression.25 have anti-fibrotic effects, by releasing interferon-γ (IFN-γ) which induces hepatic stellate cell (HSC) Chronic inflammation cycle arrest and apoptosis.34 However, IFN-γ also The IM contributes to chronic inflammation not only results in hepatocyte apoptosis and thus causes through the production of endotoxins but also hepatic injury.34 NKT cells, which can be expressed through cytokines and inflammasome dysfunction. by hepatocytes and antigen presenting cells, share Translocation of IM-derived endotoxins into the properties of both T cells and NK cells.35 NKT cells circulatory system increases TLR4 expression, can secrete cytokines and therefore play a critical which activates the proinflammatory cytokines role in directing the immune system.35 They are tumour necrosis factor-alpha (TNF-a) and interleu- able to do this through their ability to produce kin (IL)-6,26 thus triggering systemic inflammation. T helper 1 cells, which are proinflammatory, and Inflammasomes, which consist of leucine-rich-repeat T helper 2 cells, which are anti-inflammatory.35 containing proteins and nucleotide-binding domains, Overall, the activation of hepatic immune cells by govern the cleavage of proinflammatory cytokines. the IM could contribute
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