Microbial Players in Primary Sclerosing Cholangitis: Current Evidence and Concepts

Abstract

Primary sclerosing cholangitis (PSC) is a rare cholestatic liver disease with progressive biliary inflammation, destruction of the biliary tract, and fibrosis, resulting in liver cirrhosis and end-stage liver disease. To date, liver transplantation is the only definitive treatment option for PSC. The precise etiology of PSC remains elusive, but it is widely accepted to involve a complex interplay between genetic predisposition, immunologic dysfunction, and environmental influence. In recent years, the gut-liver axis has emerged as a crucial pathway contributing to the pathogenesis of PSC, with particular focus on the role of gut microbiota. However, the role of the fungal microbiome or mycobiome has been overlooked for years, resulting in a lack of comprehensive studies on its involvement in PSC. In this review, we clarify the present clinical and mechanistic data and concepts concerning the gut bacterial and fungal microbiota in the context of PSC. This review sheds light on the role of specific microbes and elucidates the dynamics of bacterial and fungal populations. Moreover, we discuss the latest insights into microbe-altering therapeutic approaches involving the gut-liver axis and bile acid metabolism. Primary sclerosing cholangitis (PSC) is a rare cholestatic liver disease with progressive biliary inflammation, destruction of the biliary tract, and fibrosis, resulting in liver cirrhosis and end-stage liver disease. To date, liver transplantation is the only definitive treatment option for PSC. The precise etiology of PSC remains elusive, but it is widely accepted to involve a complex interplay between genetic predisposition, immunologic dysfunction, and environmental influence. In recent years, the gut-liver axis has emerged as a crucial pathway contributing to the pathogenesis of PSC, with particular focus on the role of gut microbiota. However, the role of the fungal microbiome or mycobiome has been overlooked for years, resulting in a lack of comprehensive studies on its involvement in PSC. In this review, we clarify the present clinical and mechanistic data and concepts concerning the gut bacterial and fungal microbiota in the context of PSC. This review sheds light on the role of specific microbes and elucidates the dynamics of bacterial and fungal populations. Moreover, we discuss the latest insights into microbe-altering therapeutic approaches involving the gut-liver axis and bile acid metabolism. SummaryThis review provides an overview of the current knowledge on the gut bacterial and fungal microbiota in primary sclerosing cholangitis. It highlights the importance of certain microbes and explains the changes in bacterial and fungal populations. Additionally, it discusses recent advancements in microbe-altering therapeutic approaches involving the gut-liver axis and bile acid metabolism. This review provides an overview of the current knowledge on the gut bacterial and fungal microbiota in primary sclerosing cholangitis. It highlights the importance of certain microbes and explains the changes in bacterial and fungal populations. Additionally, it discusses recent advancements in microbe-altering therapeutic approaches involving the gut-liver axis and bile acid metabolism. Primary sclerosing cholangitis (PSC) is a rare cholestatic liver disease with progressive biliary inflammation, intrahepatic and extrahepatic strictures, and fibrosis, leading to liver cirrhosis and end-stage liver disease. It is associated with a high risk of biliary and colorectal carcinoma, and concomitant inflammatory bowel disease (IBD), most commonly ulcerative colitis (UC), has been reported in up to 80% of patients with PSC.1Hov J.R. Karlsen T.H. The microbiota and the gut-liver axis in primary sclerosing cholangitis.Nat Rev Gastroenterol Hepatol. 2023; 20: 135-154Crossref PubMed Scopus (16) Google Scholar,2Karlsen T.H. Folseraas T. Thorburn D. et al.Primary sclerosing cholangitis: a comprehensive review.J Hepatol. 2017; 67: 1298-1323Abstract Full Text Full Text PDF PubMed Scopus (468) Google Scholar It has even been proposed that PSC-associated colitis presents a distinct IBD entity alongside Crohn’s disease (CD) and UC.3Loftus E.V. Harewood G.C. Loftus C.G. et al.PSC-IBD: a unique form of inflammatory bowel disease associated with primary sclerosing cholangitis.Gut. 2005; 54: 91-96Crossref PubMed Scopus (602) Google Scholar To date, no effective medical treatment has been proven to increase survival and the only definitive treatment option is liver transplantation. Even though outcome after liver transplantation is excellent, the risk of recurrent PSC in the new liver is considerably high (up to 30%).1Hov J.R. Karlsen T.H. The microbiota and the gut-liver axis in primary sclerosing cholangitis.Nat Rev Gastroenterol Hepatol. 2023; 20: 135-154Crossref PubMed Scopus (16) Google Scholar,4Lindström L. Jørgensen K.K. Boberg K.M. et al.Risk factors and prognosis for recurrent primary sclerosing cholangitis after liver transplantation: a Nordic Multicentre Study.Scand J Gastroenterol. 2018; 53: 297-304Crossref PubMed Scopus (58) Google Scholar The development of prognostic markers and more effective treatment modalities have been limited partly by a lack of studies aiming to understand the disease pathogenesis of this rare but serious disease. In addition to small patient numbers, the absence of in vitro and in vivo models that accurately represent the disease constitutes a limitation in this field.2Karlsen T.H. Folseraas T. Thorburn D. et al.Primary sclerosing cholangitis: a comprehensive review.J Hepatol. 2017; 67: 1298-1323Abstract Full Text Full Text PDF PubMed Scopus (468) Google Scholar Within this framework, the gut microbiota, encompassing bacteria, viruses, fungi, and archaea, play an emerging role. Understanding the composition and dynamics of the gut microbiota in PSC holds great promise for improving the comprehension of disease pathogenesis and identifying potential therapeutic targets. In this review, we clarify the present clinical and mechanistic data and concepts concerning the gut bacterial and fungal microbiota in the context of PSC. Moreover, we elucidate the latest insights into microbe-altering therapeutic approaches involving the gut-liver axis and bile acid metabolism. The precise etiology of PSC remains elusive, but it is widely accepted to involve a complex interplay between genetic predisposition, immunologic dysfunction, and environmental factors.2Karlsen T.H. Folseraas T. Thorburn D. et al.Primary sclerosing cholangitis: a comprehensive review.J Hepatol. 2017; 67: 1298-1323Abstract Full Text Full Text PDF PubMed Scopus (468) Google Scholar In recent years, the gut-liver axis has emerged as a crucial pathway contributing to the pathogenesis of PSC, with particular focus on the role of the gut microbiota.1Hov J.R. Karlsen T.H. The microbiota and the gut-liver axis in primary sclerosing cholangitis.Nat Rev Gastroenterol Hepatol. 2023; 20: 135-154Crossref PubMed Scopus (16) Google Scholar The high prevalence of IBD in patients with PSC suggests a significant involvement of the gut-liver axis. The concept of the gut-liver axis revolves around the bidirectional interaction between the gut and the liver, facilitated by the portal blood circulation to the liver and the flow of bile to the intestine.5Tripathi A. Debelius J. Brenner D.A. et al.The gut-liver axis and the intersection with the microbiome.Nat Rev Gastroenterol Hepatol. 2018; 15: 397-411Crossref PubMed Scopus (814) Google Scholar,6Albillos A. de Gottardi A. Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy.J Hepatol. 2020; 72: 558-577Abstract Full Text Full Text PDF PubMed Scopus (827) Google Scholar In addition, liver metabolites from dietary or xenobiotic substances (eg, free fatty acids, ethanol metabolites, choline metabolites) pass from the liver to the intestine through the systemic circulation (Figure 1A).5Tripathi A. Debelius J. Brenner D.A. et al.The gut-liver axis and the intersection with the microbiome.Nat Rev Gastroenterol Hepatol. 2018; 15: 397-411Crossref PubMed Scopus (814) Google Scholar,7Seo Y.S. Shah V.H. The role of gut-liver axis in the pathogenesis of liver cirrhosis and portal hypertension.Clin Mol Hepatol. 2012; 18: 337-346Crossref PubMed Scopus (0) Google Scholar The gut barrier has the delicate function to allow nutrient absorption, it microbes and the gut barrier function in (eg, and (eg, A. Debelius J. Brenner D.A. et al.The gut-liver axis and the intersection with the microbiome.Nat Rev Gastroenterol Hepatol. 2018; 15: 397-411Crossref PubMed Scopus (814) Google Scholar barrier with an barrier (eg, by inflammation, or portal of microbes and to as to the liver, an inflammatory A. de Gottardi A. Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy.J Hepatol. 2020; 72: 558-577Abstract Full Text Full Text PDF PubMed Scopus (827) Google Scholar This and and in of inflammatory and and barrier to the development of biliary and inflammation, of Y.S. Shah V.H. 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