Primary sclerosing cholangitis is characterised by intestinal dysbiosis independent from IBD
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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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Recent studies support an association between changes in the microbiome and the progression of cholestatic liver disease in patients.
“Recent studies have further supported the association between changes in the microbiome and the progression of cholestatic liver disease in patients9–14.”
From Cholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice (2019) · cites this paper as [11]
Changes at genera level in cholestatic patients differ among studies and include enrichment in Veillonella, Akkermansia, Ruminococcaceae (undefined genus) and Clostridium and decrease in Prevotella.
“The changes described at genera level differ among studies9–12 and include the enrichment in Veillonella, Akkermansia, Ruminococcaceae (undefined genus) and Clostridium9 and the decrease in Prevotella10, overall supporting the association between changes in the microbiome and cholestatic disease.”
From Cholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice (2019) · cites this paper as [11]
Recent studies described that cholestatic patients with PSC have an overall less diverse microbiome composition.
“Recent studies described that cholestatic patients with PSC have an overall less diverse microbiome composition.”
From Cholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice (2019) · cites this paper as [11]
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phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
McMurdie, P. J., & Holmes, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061217 · Cited by 21,013 · see citing works
Search and clustering orders of magnitude faster than BLAST
Edgar, R. C. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq461 · Cited by 20,617 · see citing works
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00062-07 · Cited by 19,770 · see citing works
The WEKA data mining software: an update
Hall, M., Frank, E., Holmes, G., Pfahringer, B., Reutemann, P., & Witten, I. H. (2009) · ACM SIGKDD Explorations Newsletter · doi:10.1145/1656274.1656278 · Cited by 17,750 · see citing works
FLASH: fast length adjustment of short reads to improve genome assemblies
Magoč, T., & Salzberg, S. L. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr507 · Cited by 15,366 · see citing works
UCHIME improves sensitivity and speed of chimera detection
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr381 · Cited by 15,114 · see citing works
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01043-13 · Cited by 7,004 · see citing works
Changes of Intestinal Functions in Liver Cirrhosis
Fukui, H., & Wiest, R. (2016) · Inflammatory Intestinal Diseases · doi:10.1159/000444436 · Cited by 6,820 · see citing works
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J.-J., Blugeon, S., Bridonneau, C., Furet, J.-P., Corthier, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804812105 · Cited by 4,413 · see citing works
The Treatment-Naive Microbiome in New-Onset Crohn’s Disease
Gevers, D., Kugathasan, S., Denson, L. A., Vázquez-Baeza, Y., Van Treuren, W., Ren, B., Schwager, E., Knights, D., Song, S. J., Yassour, M., et al. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.02.005 · Cited by 3,220 · see citing works
Alterations of the human gut microbiome in liver cirrhosis
Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., Guo, J., Le Chatelier, E., Yao, J., Wu, L., et al. (2014) · Nature · doi:10.1038/nature13568 · Cited by 2,177 · see citing works
Genomic analysis identifies association of <i>Fusobacterium</i> with colorectal carcinoma
Kostic, A. D., Gevers, D., Pedamallu, C. S., Michaud, M., Duke, F., Earl, A. M., Ojesina, A. I., Jung, J., Bass, A. J., Tabernero, J., et al. (2012) · Genome Research · doi:10.1101/gr.126573.111 · Cited by 1,960 · see citing works
Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., Ballet, V., Claes, K., Van Immerseel, F., Verbeke, K., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-304833 · Cited by 1,904 · see citing works
Self-citationThe Microbiome in Inflammatory Bowel Disease: Current Status and the Future Ahead
Kostic, A. D., Xavier, R. J., & Gevers, D. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.02.009 · Cited by 1,789 · see citing works
Assche, G. V., Dignass, A. U., Panés, J., Beaugerie, L., Karagiannis, J. A., Allez, M., Ochsenkühn, T., Orchard, T., Rogler, G., Louis, E. J., et al. (2010) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2009.12.003 · Cited by 1,444 · see citing works
The ecology, epidemiology and virulence of Enterococcus
Fisher, K., & Phillips, C. A. (2009) · Microbiology · doi:10.1099/mic.0.026385-0 · Cited by 1,231 · see citing works
Dysbiosis of the faecal microbiota in patients with Crohn’s disease and their unaffected relatives
Joossens, M., Huys, G., Cnockaert, M., De Preter, V., Verbeke, K., Rutgeerts, P., Vandamme, P., & Vermeire, S. (2011) · Gut · doi:10.1136/gut.2010.223263 · Cited by 1,063 · see citing works
Self-citationCharacterization of fecal microbial communities in patients with liver cirrhosis
Chen, Y., Yang, F., Lu, H., Wang, B., Chen, Y., Lei, D., Wang, Y., Zhu, B., & Li, L. (2011) · Hepatology · doi:10.1002/hep.24423 · Cited by 1,038 · see citing works
Willing, B. P., Dicksved, J., Halfvarson, J., Andersson, A. F., Lucio, M., Zheng, Z., Järnerot, G., Tysk, C., Jansson, J. K., & Engstrand, L. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.08.049 · Cited by 1,032 · see citing works
Dignass, A. U., Eliakim, R., Magro, F., Maaser, C., Chowers, Y., Geboes, K., Mantzaris, G. J., Reinisch, W., Colombel, J., Vermeire, S., et al. (2012) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2012.09.003 · Cited by 885 · see citing works
Self-citationBoonstra, K., Weersma, R. K., van Erpecum, K. J., Rauws, E. A., Spanier, B. W. M., Poen, A. C., van Nieuwkerk, K. M., Drenth, J. P., Witteman, B. J., Tuynman, H. A., et al. (2013) · Hepatology · doi:10.1002/hep.26565 · Cited by 725 · see citing works
Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data
Eren, A. M., Maignien, L., Sul, W. J., Murphy, L. G., Grim, S. L., Morrison, H. G., & Sogin, M. L. (2013) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.12114 · Cited by 620 · see citing works
Primary sclerosing cholangitis
Hirschfield, G. M., Karlsen, T. H., Lindor, K. D., & Adams, D. (2013) · The Lancet · doi:10.1016/s0140-6736(13)60096-3 · Cited by 599 · see citing works
Strauss, J., Kaplan, G. G., Beck, P. L., Rioux, K. P., Panaccione, R., DeVinney, R., Lynch, T., & Allen‐Vercoe, E. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21606 · Cited by 574 · see citing works
ACG clinical guideline: primary sclerosing cholangitis
Lindor, K. D., Kowdley, K. V., & Harrison, E. M. (2015) · American Journal of Gastroenterology · doi:10.1038/ajg.2015.112 · Cited by 524 · see citing works
Kummen, M., Holm, K., Anmarkrud, J. A., Nygård, S., Vesterhus, M., Høivik, M. L., Trøseid, M., Marschall, H.-U., Schrumpf, E., Moum, B., et al. (2017) · Gut · doi:10.1136/gutjnl-2015-310500 · Cited by 426 · see citing works
The UK-PSCSC Consortium, Liu, J. Z., The International IBD Genetics Consortium, The International PSC Study Group, Hov, J. R., Folseraas, T., Ellinghaus, E., Rushbrook, S. M., Doncheva, N. T., Andreassen, O. A., et al. (2013) · Nature Genetics · doi:10.1038/ng.2616 · Cited by 391 · see citing works
Self-citationExtraintestinal manifestations and complications in IBD
Ott, C., & Schölmerich, J. (2013) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2013.117 · Cited by 352 · see citing works
Steck, N., Hoffmann, M., Sava, I. G., Kim, S. C., Hahne, H., Tonkonogy, S. L., Mair, K., Krueger, D., Pruteanu, M., Shanahan, F., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.05.035 · Cited by 343 · see citing works
Alabraba, E., Nightingale, P., Gunson, B., Hubscher, S., Olliff, S., Mirza, D., & Neuberger, J. (2009) · Liver Transplantation · doi:10.1002/lt.21679 · Cited by 298 · see citing works
Tabibian, J. H., O'Hara, S. P., Trussoni, C. E., Tietz, P. S., Splinter, P. L., Mounajjed, T., Hagey, L. R., & LaRusso, N. F. (2016) · Hepatology · doi:10.1002/hep.27927 · Cited by 223 · see citing works
Färkkilä, M., Karvonen, A., Nurmi, H., Nuutinen, H., Taavitsainen, M., Pikkarainen, P., & Kärkkäinen, P. (2004) · Hepatology · doi:10.1002/hep.20457 · Cited by 218 · see citing works
Mamari, S. A., Djordjevic, J., Halliday, J., & Chapman, R. W. (2012) · Journal of Hepatology · doi:10.1016/j.jhep.2012.10.013 · Cited by 202 · see citing works
Lindström, L., Hultcrantz, R. W., Boberg, K. M., Friis–Liby, I., & Bergquist, A. M. (2013) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2012.12.032 · Cited by 178 · see citing works
Wacklin, P., Tuimala, J., Nikkilä, J., Tims, S., Mäkivuokko, H., Alakulppi, N. S., Laine, P., Rajilić-Stojanović, M. D., Paulin, L. G., de Vos, W. M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094863 · Cited by 158 · see citing works
Bile duct bacterial isolates in primary sclerosing cholangitis: a study of explanted livers
Olsson, R., Björnsson, E., Bäckman, L., Friman, S., Höckerstedt, K., Kaijser, B., & Olausson, M. (1998) · Journal of Hepatology · doi:10.1016/s0168-8278(98)80316-4 · Cited by 133 · see citing works
Rossen, N. G., Fuentes, S., Boonstra, K., D’Haens, G. R., Heilig, H. G., Zoetendal, E. G., de Vos, W. M., & Ponsioen, C. Y. (2015) · Journal of Crohn's and Colitis · doi:10.1093/ecco-jcc/jju023 · Cited by 129 · see citing works
Pohl, J., Ring, A., Stremmel, W., & Stiehl, A. (2006) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-200601000-00012 · Cited by 111 · see citing works
Changing trend in bile microbiology and antibiotic susceptibilities: over 12 years of experience
Kwon, W., Jang, J.-Y., Kim, E.-C., Park, J. W., Han, I. W., Kang, M. J., & Kim, S.-W. (2012) · Infection · doi:10.1007/s15010-012-0358-y · Cited by 52 · see citing works
CD8 T Cells Primed in the Gut-Associated Lymphoid Tissue Induce Immune-Mediated Cholangitis in Mice
Seidel, D., Eickmeier, I., Kühl, A. A., Hamann, A., Loddenkemper, C., & Schott, E. (2013) · Hepatology · doi:10.1002/hep.26702 · Cited by 50 · see citing works
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Sorted by citations
Quantitative microbiome profiling links gut community variation to microbial load
Vandeputte, D., Kathagen, G., D’hoe, K., Vieira-Silva, S., Valles-Colomer, M., Sabino, J., Wang, J., Tito, R. Y., De Commer, L., Darzi, Y., et al. (2017) · Nature · doi:10.1038/nature24460 · Cited by 1,218 · see citing works
Self-citationPrimary sclerosing cholangitis – a comprehensive review
Karlsen, T. H., Folseraas, T., Thorburn, D., & Vesterhus, M. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.07.022 · Cited by 868 · see citing works
Optimizing methods and dodging pitfalls in microbiome research
Kim, D. J., Hofstaedter, C. E., Zhao, C., Mattei, L. M., Tanes, C., Clarke, E., Lauder, A. P., Sherrill-Mix, S. A., Chehoud, C., Kelsen, J. R., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0267-5 · Cited by 536 · see citing works
Gut microbiome and liver diseases
Tilg, H., Cani, P. D., & Mayer, E. A. (2016) · Gut · doi:10.1136/gutjnl-2016-312729 · Cited by 525 · see citing works
Gut microbiome, liver immunology, and liver diseases
Wang, R., Tang, R., Li, B., Ma, X., Schnabl, B., & Tilg, H. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-00592-6 · Cited by 466 · see citing works
Primary sclerosing cholangitis
Dyson, J. K., Beuers, U. H., Jones, D. E. J., Lohse, A. W., & Hudson, M. (2018) · The Lancet · doi:10.1016/s0140-6736(18)30300-3 · Cited by 479 · see citing works
Tang, R., Wei, Y., Li, Y., Chen, W., Chen, H., Wang, Q., Yang, F., Miao, Q., Xiao, X., Zhang, H., et al. (2018) · Gut · doi:10.1136/gutjnl-2016-313332 · Cited by 434 · see citing works
AASLD practice guidance on primary sclerosing cholangitis and cholangiocarcinoma
Bowlus, C. L., Arrivé, L., Bergquist, A. M., Deneau, M. R., Forman, L., Ilyas, S. I., Lunsford, K. E., Martínez, M., Sapisochín, G., Shroff, R. T., et al. (2022) · Hepatology · doi:10.1002/hep.32771 · Cited by 448 · see citing works
Nakamoto, N., Sasaki, N., Aoki, R., Miyamoto, K., Suda, W., Teratani, T., Suzuki, T., Koda, Y., Chu, P.-S., Taniki, N., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-018-0333-1 · Cited by 425 · see citing works
Targeting the gut-liver axis in liver disease
Wiest, R., Albillos, A., Trauner, M., Bajaj, J. S., & Jalan, R. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.05.007 · Cited by 423 · see citing works
Bajer, L., Kverka, M., Kostovčík, M., Mačinga, P., Dvořák, J., Stehlíková, Z., Březina, J., Wohl, P., Špičák, J., & Drastich, P. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i25.4548 · Cited by 360 · see citing works
Alterations of gut microbiome in autoimmune hepatitis
Wei, Y., Li, Y., Li, Y., Sun, C., Miao, Q., Wang, Q., Xiao, X., Lian, M., Li, B., Chen, Y., et al. (2019) · Gut · doi:10.1136/gutjnl-2018-317836 · Cited by 306 · see citing works
Fusobacterium nucleatum Secretes Outer Membrane Vesicles and Promotes Intestinal Inflammation
Engevik, M. A., Danhof, H. A., Ruan, W. H., Engevik, A. C., Chang‐Graham, A. L., Engevik, K. A., Shi, Z., Zhao, Y., Ardis, C. K., Krystofiak, E., et al. (2021) · mBio · doi:10.1128/mbio.02706-20 · Cited by 275 · see citing works
Vieira‐Silva, S., Sabino, J., Valles‐Colomer, M., Falony, G., Kathagen, G., Caenepeel, C., Cleynen, I., der Merwe, V., Vermeire, S., & Raes, J. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0483-9 · Cited by 263 · see citing works
Self-citationGut Microbiome Directs Hepatocytes to Recruit MDSCs and Promote Cholangiocarcinoma
Zhang, Q., Ma, C., Duan, Y., Heinrich, B., Rosato, U., Diggs, L. P., Ma, L., Roy, S., Fu, Q., Brown, Z. J., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0304 · Cited by 263 · see citing works
Bile acids and intestinal microbiota in autoimmune cholestatic liver diseases
Li, Y., Tang, R., Leung, P. S. C., Gershwin, M. E., & Ma, X. (2017) · Autoimmunity Reviews · doi:10.1016/j.autrev.2017.07.002 · Cited by 247 · see citing works
Wijnands, A. M., de Jong, M. E., Lutgens, M. W. M. D., Hoentjen, F., Elias, S. G., & Oldenburg, B. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.12.036 · Cited by 241 · see citing works
Allegretti, J. R., Kassam, Z., Carrellas, M., Mullish, B. H., Marchesi, J. R., Pechlivanis, A., Smith, M., Gerardin, Y., Timberlake, S., Pratt, D. S., et al. (2019) · American Journal of Gastroenterology · doi:10.14309/ajg.0000000000000115 · Cited by 234 · see citing works
The microbiome and autoimmunity: a paradigm from the gut–liver axis
Li, B., Selmi, C. F., Tang, R., Gershwin, M. E., & Ma, X. (2018) · Cellular and Molecular Immunology · doi:10.1038/cmi.2018.7 · Cited by 234 · see citing works
Gut–liver axis, cirrhosis and portal hypertension: the chicken and the egg
Arab, J. P., Martín‐Mateos, R., & Shah, V. H. (2017) · Hepatology International · doi:10.1007/s12072-017-9798-x · Cited by 229 · see citing works
Hedin, C. R. H., Vavricka, S., Stagg, A. J., Schoepfer, A. M., Raine, T., Puig, L., Pleyer, U., Navarini, A. A., Jong, A. E. V. D. M., Maul, J., et al. (2018) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjy191 · Cited by 232 · see citing works
Dysbiosis of small intestinal microbiota in liver cirrhosis and its association with etiology
Chen, Y., Ji, F., Guo, J., Shi, D., Fang, D., & Li, L. (2016) · Scientific Reports · doi:10.1038/srep34055 · Cited by 205 · see citing works
Fungi participate in the dysbiosis of gut microbiota in patients with primary sclerosing cholangitis
Lemoinne, S., Kemgang, A., Belkacem, K. B., Straube, M., Jégou, S., Corpechot, C., Saint-Antoine IBD Network, Chazouillères, O., Housset, C., & Sokol, H. (2019) · Gut · doi:10.1136/gutjnl-2018-317791 · Cited by 215 · see citing works
Woodhouse, C., Patel, V., Singanayagam, A., & Shawcross, D. L. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14397 · Cited by 207 · see citing works
Cheng, L., Qi, C., Zhuang, H., Fu, T., & Zhang, X. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz843 · Cited by 195 · see citing works
Immunology and immunotherapy of cholangiocarcinoma
Greten, T. F., Schwabe, R. F., Bardeesy, N. M., Ma, L., Goyal, L., Kelley, R. K., & Wang, X. W. (2023) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00741-4 · Cited by 193 · see citing works
Liao, L., Schneider, K. M., Gálvez, E. J. C., Frissen, M., Marschall, H., Su, H., Hatting, M., Wahlstrom, A. M., Haybaeck, J., Puchas, P., et al. (2019) · Gut · doi:10.1136/gutjnl-2018-316670 · Cited by 175 · see citing works
The gut microbiome and mental health: implications for anxiety- and trauma-related disorders
Malan-Muller, S., Valles-Colomer, M., Raes, J., Lowry, C. A., Seedat, S., & Hemmings, S. M. J. (2018) · OMICS: A Journal of Integrative Biology · doi:10.1089/omi.2017.0077 · Cited by 161 · see citing works
Self-citationThe role of the gut microbiome in chronic liver disease: the clinical evidence revised
Schwenger, K. J. P., Clermont‐Dejean, N. M., & Allard, J. P. (2019) · JHEP Reports · doi:10.1016/j.jhepr.2019.04.004 · Cited by 171 · see citing works
Microbiota changes and intestinal microbiota transplantation in liver diseases and cirrhosis
Bajaj, J. S., & Khoruts, A. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.01.017 · Cited by 170 · see citing works
Thomas, A. M., Jesus, E. C., Lopes, A., Aguiar, S., Begnami, M. D., Rocha, R. M., Carpinetti, P. A., Camargo, A. A., Hoffmann, C., Freitas, H., et al. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00179 · Cited by 165 · see citing works
Intestinal and fecal pH in human health
Yamamura, R., Inoue, K. Y., Nishino, K., & Yamasaki, S. (2023) · Frontiers in Microbiomes · doi:10.3389/frmbi.2023.1192316 · Cited by 172 · see citing works
Genetics of primary sclerosing cholangitis and pathophysiological implications
Jiang, X., & Karlsen, T. H. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.154 · Cited by 155 · see citing works
Autoantibodies in Autoimmune Liver Disease—Clinical and Diagnostic Relevance
Sebode, M., Weiler‐Normann, C., Liwinski, T., & Schramm, C. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00609 · Cited by 157 · see citing works
Alterations of the bile microbiome in primary sclerosing cholangitis
Liwinski, T., Zenouzi, R., John, C., Ehlken, H., Rühlemann, M. C., Bang, C., Groth, S., Lieb, W., Kantowski, M., Andersen, N., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-318416 · Cited by 149 · see citing works
Role of gut microbiota in liver disease
Albhaisi, S. A. M., Bajaj, J. S., & Sanyal, A. J. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00118.2019 · Cited by 153 · see citing works
Role of Gut Dysbiosis in Liver Diseases: What Have We Learned So Far?
Fukui, H. (2019) · Diseases · doi:10.3390/diseases7040058 · Cited by 151 · see citing works
Liver–Microbiome Axis in Health and Disease
Adolph, T. E., Grander, C., Moschen, A. R., & Tilg, H. (2018) · Trends in Immunology · doi:10.1016/j.it.2018.05.002 · Cited by 152 · see citing works
Tedesco, D., Thapa, M., Chin, C. Y., Ge, Y., Gong, M., Li, J., Gumber, S., Speck, P., Elrod, E. J., Burd, E. M., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.02.019 · Cited by 137 · see citing works
Zhao, M., Zhao, L., Xiong, X., He, Y. M., Huang, W., Liu, Z., Liang, J., Pan, B., Guo, X., Wang, L., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.02.033 · Cited by 135 · see citing works
The gut ecosystem and immune tolerance
Shao, T., Hsu, R., Rafizadeh, D. L., Wang, L., Bowlus, C. L., Kumar, N., Mishra, J., Timilsina, S., Ridgway, W. M., Gershwin, M. E., et al. (2023) · Journal of Autoimmunity · doi:10.1016/j.jaut.2023.103114 · Cited by 136 · see citing works
Altered gut microbial metabolism of essential nutrients in primary sclerosing cholangitis
Kummen, M., Thingholm, L. B., Rühlemann, M. C., Holm, K., Hansen, S. H., Moitinho-Silva, L., Liwinski, T., Zenouzi, R., Storm-Larsen, C., Midttun, Ø., et al. (2021) · Gastroenterology · doi:10.1053/j.gastro.2020.12.058 · Cited by 129 · see citing works
Gut microbiota depletion exacerbates cholestatic liver injury via loss of FXR signalling
Schneider, K. M., Candels, L. S., Hov, J. R., Myllys, M., Hassan, R. A. R. A., Schneider, C. V., Wahlstrom, A. M., Mohs, A., Zühlke, S., Liao, L., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00452-1 · Cited by 126 · see citing works
Gut microbiome in primary sclerosing cholangitis: A review
Little, R., Wine, E., Kamath, B. M., Griffiths, A. M., & Ricciuto, A. (2020) · World Journal of Gastroenterology · doi:10.3748/wjg.v26.i21.2768 · Cited by 125 · see citing works
Cheng, L., Qi, C., Zhuang, H., Fu, T., & Zhang, X. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa511 · Cited by 125 · see citing works
Torres, J., Palmela, C., Brito, H., Bao, X., Ruiqi, H., Moura-Santos, P., da Silva, J. P., Oliveira, A. A. S., Vieira, C. L., Pérez, K., et al. (2017) · United European Gastroenterology Journal · doi:10.1177/2050640617708953 · Cited by 121 · see citing works
Giuffrè, M., Campigotto, M., Campisciano, G., Comar, M., & Crocè, L. S. (2020) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00161.2019 · Cited by 121 · see citing works
The microbiota and the gut–liver axis in primary sclerosing cholangitis
Hov, J. R., & Karlsen, T. H. (2022) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00690-y · Cited by 121 · see citing works
Mechanisms and consequences of gut commensal translocation in chronic diseases
Fine, R. L., Vieira, S. M., Gilmore, M. S., & Kriegel, M. A. (2019) · Gut Microbes · doi:10.1080/19490976.2019.1629236 · Cited by 123 · see citing works
Composition and diverse differences of intestinal microbiota in ulcerative colitis patients
Zhu, S., Han, M., Liu, S., Fan, L., Shi, H., & Li, P. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.953962 · Cited by 117 · see citing works
Inflammatory bowel disease and primary sclerosing cholangitis: One disease or two?
van Munster, K. N., Bergquist, A. M., & Ponsioen, C. Y. (2023) · Journal of Hepatology · doi:10.1016/j.jhep.2023.09.031 · Cited by 115 · see citing works
Shah, S. C., ten Hove, J. R., Castaneda, D., Palmela, C., Mooiweer, E., Colombel, J.-F., Harpaz, N., Ullman, T. A., van Bodegraven, A. A., Jansen, J. M., et al. (2018) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.01.023 · Cited by 109 · see citing works
Cholestatic Liver Disease: Current Treatment Strategies and New Therapeutic Agents
Hasegawa, S., Yoneda, M., Kurita, Y., Nogami, A., Honda, Y., Hosono, K., & Nakajima, A. (2021) · Drugs · doi:10.1007/s40265-021-01545-7 · Cited by 114 · see citing works
Ichikawa, M., Nakamoto, N., Kredo‐Russo, S., Weinstock, E., Weiner, I. N., Khabra, E., Ben-Ishay, N., Inbar, D., Kowalsman, N., Mordoch, R., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39029-9 · Cited by 111 · see citing works
Gut microbiome in chronic rheumatic and inflammatory bowel diseases: Similarities and differences
Salem, F., Kindt, N., Marchesi, J. R., Netter, P., Lopez, A., Kökten, T., Danese, S., Jouzeau, J., Peyrin‐Biroulet, L., & Moulin, D. (2019) · United European Gastroenterology Journal · doi:10.1177/2050640619867555 · Cited by 106 · see citing works
Inflammation-independent TL1A-mediated intestinal fibrosis is dependent on the gut microbiome
Jacob, N., Jacobs, J. P., Kumagai, K., Ha, C. W. Y., Kanazawa, Y., Lagishetty, V., Altmayer, K., Hamill, A. M., Von Arx, A., Sartor, R. B., et al. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0055-y · Cited by 102 · see citing works
Mousa, O. Y. S., Juran, B. D., McCauley, B. M., Vesterhus, M. N., Folseraas, T., Turgeon, C. T., Ali, A. H., Schlicht, E. M., Atkinson, E. J., Hu, C., et al. (2020) · Hepatology · doi:10.1002/hep.31652 · Cited by 102 · see citing works
Rühlemann, M. C., Liwinski, T., Heinsen, F., Bang, C., Zenouzi, R., Kummen, M., Thingholm, L. B., Tempel, M., Lieb, W., Karlsen, T. H., et al. (2019) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15375 · Cited by 99 · see citing works
Critical roles of bile acids in regulating intestinal mucosal immune responses
Sun, R., Xu, C., Feng, B., Gao, X., & Liu, Z. (2021) · Therapeutic Advances in Gastroenterology · doi:10.1177/17562848211018098 · Cited by 99 · see citing works
Liu, Q., Li, B., Li, Y., Wei, Y., Huang, B., Liang, J., You, Z., Li, Y., Qian, Q., Wang, R., et al. (2021) · Gut · doi:10.1136/gutjnl-2020-323565 · Cited by 100 · see citing works
The Gut-Liver Axis in Cholestatic Liver Diseases
Blesl, A., & Stadlbauer, V. (2021) · Nutrients · doi:10.3390/nu13031018 · Cited by 99 · see citing works
Pereira, P. A. B., Aho, V. T. E., Arola, J. T., Boyd, S., Jokelainen, K., Paulin, L. G., Auvinen, P., & Färkkilä, M. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182924 · Cited by 97 · see citing works
Kunzmann, L. K., Schoknecht, T., Poch, T., Henze, L., Stein, S., Kriz, M., Grewe, I., Preti, M., Hartl, J., Pannicke, N., et al. (2020) · Hepatology · doi:10.1002/hep.31140 · Cited by 93 · see citing works
The IBD and PSC phenotypes of PSC-IBD
Ricciuto, A., Kamath, B. M., & Griffiths, A. M. (2018) · Current Gastroenterology Reports · doi:10.1007/s11894-018-0620-2 · Cited by 94 · see citing works
Characterization of Gut Microbiota in Children With Pulmonary Tuberculosis
Li, W., Zhu, Y., Liao, Q., Wang, Z., & Wan, C. (2019) · BMC Pediatrics · doi:10.1186/s12887-019-1782-2 · Cited by 94 · see citing works
Molecular and Cellular Mediators of the Gut-Liver Axis in the Progression of Liver Diseases
Bruneau, A., Hundertmark, J., Guillot, A., & Tacke, F. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.725390 · Cited by 88 · see citing works
The Role of Gut Microbiota in Some Liver Diseases: From an Immunological Perspective
Wang, L., Cao, Z.-M., Zhang, L., Li, J.-M., & Lv, W. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.923599 · Cited by 87 · see citing works
Trivedi, P. J., Tickle, J., Vesterhus, M. N., Eddowes, P. J., Bruns, T., Vainio, J., Parker, R., Smith, D., Liaskou, E., Thorbjørnsen, L. W., et al. (2017) · Gut · doi:10.1136/gutjnl-2016-312354 · Cited by 83 · see citing works
Rosacea and its association with enteral microbiota in Korean females
Nam, J., Yun, Y., Kim, H., Kim, H., Jung, H. J., Chang, Y., Ryu, S., Shin, H., Kim, H., & Kim, W. (2017) · Experimental Dermatology · doi:10.1111/exd.13398 · Cited by 82 · see citing works
BingRong, C., Fu, S., Lu, L., & Zhao, H. (2019) · BioMed Research International · doi:10.1155/2019/1092563 · Cited by 82 · see citing works
Commensal Lactobacillus Controls Immune Tolerance during Acute Liver Injury in Mice
Nakamoto, N., Amiya, T., Aoki, R., Taniki, N., Koda, Y., Miyamoto, K., Teratani, T., Suzuki, T., Chiba, S., Chu, P., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.022 · Cited by 79 · see citing works
Isaacs‐Ten, A., Echeandia, M., Moreno‐Gonzalez, M., Brion, A., Goldson, A. J., Philo, M. R., Patterson, A. M., Parker, A., Galduroz, M., Baker, D., et al. (2020) · Hepatology · doi:10.1002/hep.31228 · Cited by 80 · see citing works
TREM-2 plays a protective role in cholestasis by acting as a negative regulator of inflammation
Labiano, I., Agirre-Lizaso, A., Olaizola, P., Echebarria, A., Huici-Izagirre, M., Olaizola, I., Esparza-Baquer, A., Sharif, O., Hijona, E., Milkiewicz, P., et al. (2022) · Journal of Hepatology · doi:10.1016/j.jhep.2022.05.044 · Cited by 78 · see citing works
Acharya, C., & Bajaj, J. S. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.10.056 · Cited by 78 · see citing works
The gut microbiota contributes to a mouse model of spontaneous bile duct inflammation
Schrumpf, E., Kummen, M., Valestrand, L., Greiner, T. U., Holm, K., Arulampalam, V., Reims, H. M., Baines, J. F., Bäckhed, F., Karlsen, T. H., et al. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2016.09.020 · Cited by 78 · see citing works
Kim, Y. S., Hurley, E., Park, Y., & Ko, S. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01042-9 · Cited by 78 · see citing works
Damman, J., Rodríguez, E. A., Ali, A. H., Buness, C. W., Cox, K. L., Carey, E. J., & Lindor, K. D. (2018) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14540 · Cited by 77 · see citing works
Shah, A., Macdonald, G. A., Morrison, M., & Holtmann, G. (2020) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000000604 · Cited by 77 · see citing works
Intestinal virome and therapeutic potential of bacteriophages in liver disease
Hsu, C. L., Duan, Y., Fouts, D. E., & Schnabl, B. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.08.003 · Cited by 77 · see citing works
Wu, L., Zhou, J., Zhou, A., Lei, Y., Tang, L., Hu, S., Wang, S., Xu, X., Chen, Q., Tu, D., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2390176 · Cited by 78 · see citing works
Gut microbiota in liver disease: too much is harmful, nothing at all is not helpful either
Hartmann, P., Chu, H., Duan, Y., & Schnabl, B. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00370.2018 · Cited by 73 · see citing works
The gut microbial influence on cholestatic liver disease
Kummen, M., & Hov, J. R. (2019) · Liver International · doi:10.1111/liv.14153 · Cited by 74 · see citing works
Chung, B. K., Karlsen, T. H., & Folseraas, T. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.08.020 · Cited by 74 · see citing works
Sheng, Q., Du, H., Cheng, X., Cheng, X.-B., Tang, Y., Pan, L., Wang, Q., & Lin, J. (2019) · Oncology Letters · doi:10.3892/ol.2019.10841 · Cited by 70 · see citing works
Verstockt, B., Bressler, B. L., Martínez-Lozano, H., McGovern, D. P. B., & Silverberg, M. S. (2022) · Gastroenterology · doi:10.1053/j.gastro.2021.12.246 · Cited by 74 · see citing works
Gut microbiota translocation promotes autoimmune cholangitis
Ma, H.-D., Zhao, Z.-B., Ma, W.-T., Liu, Q.-Z., Gao, C., Li, L., Wang, J., Tsuneyama, K., Liu, B., Zhang, W., et al. (2018) · Journal of Autoimmunity · doi:10.1016/j.jaut.2018.09.010 · Cited by 73 · see citing works
Hata, K., Ishihara, S., Nozawa, H., Kawai, K., Kiyomatsu, T., Tanaka, T., Kishikawa, J., Anzai, H., & Watanabe, T. (2016) · Digestive Endoscopy · doi:10.1111/den.12744 · Cited by 71 · see citing works
Liu, R., Li, X., Huang, Z., Zhao, D., Sukka-Ganesh, B., Lai, G., Pandak, W. M., Hylemon, P. B., Bajaj, J. S., Sanyal, A. J., et al. (2017) · Hepatology · doi:10.1002/hep.29540 · Cited by 70 · see citing works
Iwasawa, K., Suda, W., Tsunoda, T., Oikawa‐Kawamoto, M., Umetsu, S., Inui, A., Fujisawa, T., Morita, H., Sogo, T., & Hattori, M. (2016) · Gut · doi:10.1136/gutjnl-2016-312533 · Cited by 66 · see citing works
Yu, L., Liu, Y., Wang, S., Zhang, Q., Zhao, J., Zhang, H., Narbad, A., Tian, F., Zhai, Q., & Chen, W. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2181930 · Cited by 68 · see citing works
The Microbiome in Primary Sclerosing Cholangitis: Current Evidence and Potential Concepts
Hov, J., & Karlsen, T. (2017) · Seminars in Liver Disease · doi:10.1055/s-0037-1608801 · Cited by 65 · see citing works
Celiac Disease and Liver Disorders: From Putative Pathogenesis to Clinical Implications
Hoffmanová, I., Sánchez, D., Tučková, L., & Tlaskalová‐Hogenová, H. (2018) · Nutrients · doi:10.3390/nu10070892 · Cited by 65 · see citing works
Gut Microbiota Dysbiosis Is Associated with Altered Bile Acid Metabolism in Infantile Cholestasis
Wang, Y., Gao, X., Zhang, X., Xiao, Y., Huang, J., Yu, D., Li, X., Hu, H., Ge, T., Li, D., et al. (2019) · mSystems · doi:10.1128/msystems.00463-19 · Cited by 64 · see citing works
Caenepeel, C., Tabib, N. S. S., Vieira‐Silva, S., & Vermeire, S. (2020) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.16096 · Cited by 63 · see citing works
Self-citationZhang, T., Zhang, S., Chen, J., Lin, Z., Deng, T., Xie, X., Deng, L., Li, X., Ma, J., Ding, X., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.751795 · Cited by 62 · see citing works
Cholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice
Cabrera-Rubio, R., Patterson, A. M., Cotter, P. D., & Beraza, N. (2019) · Scientific Reports · doi:10.1038/s41598-019-48784-z · Cited by 61 · see citing works
The Role of Microbiota in Primary Sclerosing Cholangitis and Related Biliary Malignancies
Özdirik, B., Müller, T., Wree, A., Tacke, F., & Sigal, M. J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136975 · Cited by 61 · see citing works
Iwasawa, K., Suda, W., Tsunoda, T., Oikawa‐Kawamoto, M., Umetsu, S., Takayasu, L., Inui, A., Fujisawa, T., Morita, H., Sogo, T., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-23870-w · Cited by 61 · see citing works
Fibrotic Events in the Progression of Cholestatic Liver Disease
Wu, H., Chen, C., Ziani, S., Nelson, L. J., Avila, M. A., Nevzorova, Y. A., & Cubero, F. J. (2021) · Cells · doi:10.3390/cells10051107 · Cited by 59 · see citing works
D’Onofrio, F., Renga, G., Puccetti, M., Pariano, M., Bellet, M. M., Santarelli, I., Stincardini, C., Mosci, P., Ricci, M., Giovagnoli, S., et al. (2021) · Cells · doi:10.3390/cells10071622 · Cited by 58 · see citing works
- Authors
- Sabino, J., Vieira-Silva, S., Machiels, K., Joossens, M., Falony, G., Ballet, V., Ferrante, M., Van Assche, G., Van der Merwe, S., Vermeire, S., & Raes, J.
- Affiliations
- KU Leuven (BE)
- Department of Microbiology and Immunology, Laboratory of Molecular Bacteriology, KU Leuven—University of Leuven, Rega Institute for Medical Research, Leuven, Belgium
- Vrije Universiteit Brussel (BE)
- Rega Institute for Medical Research (BE)
- Translational Research Center for Gastrointestinal Disorders (TARGID), University of Leuven, Leuven, Belgium
- Department of Microbiology and Immunology, Center for the Biology of Disease, REGA institute, KU Leuven—VIB, Leuven, Belgium
- Corresponding author
- Raes, Jeroen
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2016-05-20
- Volume
- 65
- Issue
- 10
- Pages
- 1681-1689
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC5036217
- OpenAlex
- W2408052000
- Cited by
- 413
- References
- 40
- Citations by year
- 2026: 28 · 2025: 28 · 2024: 46 · 2023: 46 · 2022: 42 · 2021: 52 · 2020: 44 · 2019: 45 · 2018: 33 · 2017: 34 · 2016: 13
- FWCI
- 21.65
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Gut (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion, cc-by-nc)
- Lirias (submittedVersion, cc-by-nc)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Digital Access to Libraries (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Fonds Wetenschappelijk Onderzoek
- KU Leuven
- Vlaamse regering
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Keywords
- primary sclerosing cholangitis, gut dysbiosis, gut microbiota, inflammatory bowel disease, Enterococcus, Fusobacterium, Lactobacillus, microbiome diversity, Crohn's disease, ulcerative colitis, ursodeoxycholic acid, alkaline phosphatase, disease severity
- MeSH terms
- Gastrointestinal Microbiome, Adult, Aged, Alkaline Phosphatase, Biopsy, Cholagogues and Choleretics, Colonoscopy, Feces, Female, Humans, Male, Middle Aged, Severity of Illness Index, Statistics as Topic, Ursodeoxycholic Acid, Cholangitis, Sclerosing, Inflammatory Bowel Diseases, Enterococcus, Dysbiosis
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