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      Distinct gut microbiota profiles in patients with primary sclerosing cholangitis and ulcerative colitis

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          Abstract

          AIM

          To characterize the gut bacterial microbiota of patients with primary sclerosing cholangitis (PSC) and ulcerative colitis (UC).

          METHODS

          Stool samples were collected and relevant clinical data obtained from 106 study participants, 43 PSC patients with ( n = 32) or without ( n = 11) concomitant inflammatory bowel disease, 32 UC patients, and 31 healthy controls. The V3 and V4 regions of the 16S ribosomal RNA gene were sequenced on Illumina MiSeq platform to cover low taxonomic levels. Data were further processed in QIIME employing MaAsLin and LEfSe tools for analysis of the output data.

          RESULTS

          Microbial profiles in both PSC and UC were characterized by low bacterial diversity and significant change in global microbial composition. Rothia, Enterococcus, Streptococcus, Veillonella, and three other genera were markedly overrepresented in PSC regardless of concomitant inflammatory bowel disease (IBD). Rothia, Veillonella and Streptococcus were tracked to the species level to identify Rothia mucilaginosa, Streptococcus infantus, S. alactolyticus, and S. equi along with Veillonella parvula and V. dispar. PSC was further characterized by decreased abundance of Adlercreutzia equolifaciens and Prevotella copri. Decrease in genus Phascolarctobacterium was linked to presence of colonic inflammation regardless of IBD phenotype. Akkermansia muciniphila, Butyricicoccus pullicaecorum and Clostridium colinum were decreased in UC along with genus Roseburia. Low levels of serum albumin were significantly correlated with enrichment of order Actinomycetales.

          CONCLUSION

          PSC is associated with specific gut microbes independently of concomitant IBD and several bacterial taxa clearly distinguish IBD phenotypes (PSC-IBD and UC).

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          Most cited references38

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          Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction.

          Real-time polymerase chain reaction (PCR) is a highly sensitive method that can be used for the detection and quantification of microbial populations without cultivating them in anaerobic processes and environmental samples. This work was conducted to design primer and probe sets for the detection of methanogens using a real-time PCR with the TaqMan system. Six group-specific methanogenic primer and probe sets were designed. These sets separately detect four orders (Methanococcales, Methanobacteriales, Methanomicrobiales, and Methanosarcinales) along with two families (Methanosarcinaceae and Methanosaetaceae) of the order Methanosarcinales. We also designed the universal primer and probe sets that specifically detect the 16S rDNA of prokaryotes and of the domain Bacteria and Archaea, and which are fully compatible with the TaqMan real-time PCR system. Target-group specificity of each primer and probe set was empirically verified by testing DNA isolated from 28 archaeal cultures and by analyzing potential false results. In general, each primer and probe set was very specific to the target group. The primer and probe sets designed in this study can be used to detect and quantify the order-level (family-level in the case of Methanosarcinales) methanogenic groups in anaerobic biological processes and various environments.
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            Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases.

            Gut microbiota metabolises bile acids (BA). As dysbiosis has been reported in inflammatory bowel diseases (IBD), we aim to investigate the impact of IBD-associated dysbiosis on BA metabolism and its influence on the epithelial cell inflammation response. Faecal and serum BA rates, expressed as a proportion of total BA, were assessed by high-performance liquid chromatography tandem mass spectrometry in colonic IBD patients (42) and healthy subjects (29). The faecal microbiota composition was assessed by quantitative real-time PCR. Using BA profiles and microbiota composition, cluster formation between groups was generated by ranking models. The faecal BA profiles in germ-free and conventional mice were compared. Direct enzymatic activities of BA biotransformation were measured in faeces. The impact of BA on the inflammatory response was investigated in vitro using Caco-2 cells stimulated by IL-1β. IBD-associated dysbiosis was characterised by a decrease in the ratio between Faecalibacterium prausntizii and Escherichia coli. Faecal-conjugated BA rates were significantly higher in active IBD, whereas, secondary BA rates were significantly lower. Interestingly, active IBD patients exhibited higher levels of faecal 3-OH-sulphated BA. The deconjugation, transformation and desulphation activities of the microbiota were impaired in IBD patients. In vitro, secondary BA exerted anti-inflammatory effects, but sulphation of secondary BAs abolished their anti-inflammatory properties. Impaired microbiota enzymatic activity observed in IBD-associated dysbiosis leads to modifications in the luminal BA pool composition. Altered BA transformation in the gut lumen can erase the anti-inflammatory effects of some BA species on gut epithelial cells and could participate in the chronic inflammation loop of IBD.
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              Primary sclerosing cholangitis is characterised by intestinal dysbiosis independent from IBD

              Objective Primary sclerosing cholangitis (PSC) is a chronic cholestatic liver disease often leading to end-stage liver disease. Its pathogenesis remains largely unknown, although frequent concomitant IBD hints towards common factors underlying gut and bile duct inflammation. Considering the mounting evidence on the involvement of the intestinal microbiota in initiating and determining IBD phenotype, we investigated intestinal microbiota composition in patients with PSC. Design Stool samples were collected from 147 individuals (52 patients with PSC, 52 age, gender and body mass index-matched healthy volunteers, 13 UC and 30 patients with Crohn's disease). An independent validation cohort of 14 PSC and 14 matched controls was recruited. 16S rDNA sequencing of faecal DNA was performed (Illumina MiSeq). Results The microbiota of patients with PSC was characterised by decreased microbiota diversity, and a significant overrepresentation of Enterococcus (p=3.76e-05), Fusobacterium (p=3.76e-05) and Lactobacillus (p=0.0002) genera. This dysbiosis was present in patients with PSC with and without concomitant IBD and was distinct from IBD, and independent of treatment with ursodeoxycholic acid. A decision tree based on abundances of these three genera allowed reliable classification in the validation cohort. In particular, one operational taxonomic unit belonging to the Enterococcus genus was associated with increased levels of serum alkaline phosphatase (p=0.048), a marker of disease severity. Conclusions We here present the first report of PSC-associated faecal dysbiosis, independent from IBD signatures, suggesting the intestinal microbiota could be a contributing factor in PSC pathogenesis. Further studies are needed to confirm these findings and assess causality.
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                Author and article information

                Journal
                World J Gastroenterol
                World J. Gastroenterol
                WJG
                World Journal of Gastroenterology
                Baishideng Publishing Group Inc
                1007-9327
                2219-2840
                7 July 2017
                7 July 2017
                : 23
                : 25
                : 4548-4558
                Affiliations
                Lukas Bajer, Peter Macinga, Jan Brezina, Pavel Wohl, Julius Spicak, Pavel Drastich, Department of Gastroenterology and Hepatology, Institute for Clinical and Experimental Medicine, 14021 Prague, Czech Republic
                Miloslav Kverka, Jiri Dvorak, Zuzana Stehlikova, Institute of Microbiology, the Czech Academy of Sciences, 14220 Prague, Czech Republic
                Miloslav Kverka, Institute of Experimental Medicine, the Czech Academy of Sciences, 14220 Prague, Czech Republic
                Martin Kostovcik, Department of Genetics and Microbiology, Faculty of Science, Charles University, 12844 Prague, Czech Republic
                Martin Kostovcik, BIOCEV, Institute of Microbiology, the Czech Academy of Sciences, 25242 Vestec, Czech Republic
                Author notes

                Author contributions: Bajer L, Kverka M and Drastich P wrote the paper; Bajer L, Dvorak J and Stehlikova Z performed the experiments; Kverka M designed the research; Bajer L and Kostovcik M analyzed the data; Kostovcik M reviewed statistical methods; Macinga P and Brezina J recruited patients; Wohl P assessed clinical data; Spicak J and Drastich P supervised the research and revised the report; all authors contributed to this manuscript.

                Supported by Ministry of Health of the Czech Republic, No. 15-28064A.

                Correspondence to: Pavel Drastich, MD, PhD, Associate Professor, Department of Gastroenterology and Hepatology, Institute for Clinical and Experimental Medicine, Videnska 1958/9, 14021 Prague, Czech Republic. pavel.drastich@ 123456ikem.cz

                Telephone: +420-2-61362266 Fax: +420-2-61362615

                Article
                jWJG.v23.i25.pg4548
                10.3748/wjg.v23.i25.4548
                5504370
                28740343
                2daac7e0-ca84-4238-a450-b61432cd17cf
                ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.

                This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial.

                History
                : 26 January 2017
                : 10 April 2017
                : 1 June 2017
                Categories
                Basic Study

                dysbiosis,inflammatory bowel disease,ulcerative colitis,gut microbiota,primary sclerosing cholangitis

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