Cited by 26Gut microbiota and healthLiver Diseases and ImmunityInflammatory Bowel Disease

Gut microbial profile of treatment-naive patients with primary biliary cholangitis

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Zhou, Yi-jun, Ying, Gao-xiang, Dong, Shi-lei, Xiang, Bo, Jin, Qiao-fei·2023·Frontiers in Immunology

Abstract

Background and aims: The pathogenesis of primary biliary cholangitis (PBC) is associated with alterations of gut microbiota. We compared the gut microbiota of PBC patients and healthy controls from Zhejiang Province and assessed the use of these data for the diagnosis of PBC. Methods: First, 16S rRNA gene sequencing was used to characterize the gut microbiota of treatment-naive PBC patients (n=25) and matched healthy controls (n=25). Then, the value of gut microbiota composition for the diagnosis of PBC and assessment of PBC severity was determined. Results: The gut microbiota of PBC patients had lower diversity based on three different metrics of alpha-diversity (ace, Chao1, and observed features) and fewer overall genera (all p<0.01). PBC patients had significant enrichment of four genera and significant depletion of eight genera. We identified six amplicon sequence variants (Serratia, Oscillospirales, Ruminococcaceae, Faecalibacterium, Sutterellaceae, and Coprococcus) as optimal biomarkers to distinguish PBC patients from controls based on receiver operating characteristic analysis (area under the curve [AUC] = 0.824). PBC patients who were anti-gp210-positive had lower levels of Oscillospiraceae than those who were anti-gp210-negative. KEGG functional annotation suggested the major changes in the gut microbiota of PBC patients were related to lipid metabolism and biosynthesis of secondary metabolites. Conclusion: We characterized the gut microbiota of treatment-naive PBC patients and healthy controls from Zhejiang Province. The PBC patients had significant alterations in their gut microbiota, suggesting that gut microbiota composition could be useful as a non-invasive tool for the diagnosis of PBC.

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  • Oscillospiraceae and Faecalibacterium are negatively correlated with the presence of the primary biliary cholangitis-specific anti-nuclear antibody anti-gp210.

    “Oscillospiraceae and Faecalibacterium are negatively correlated with the presence of the primary biliary cholangitis-specific anti-nuclear antibody anti-gp210.34,35”

    From Primary biliary cholangitis. (2024) · cites this paper as [35]

    The Results section, “Correlation of fecal microbiome characteristics and PBC disease severity,” reports that Oscillospiraceae enrichment was negatively related to anti-gp210 antibody status. The paper reports reduced Faecalibacterium in PBC patients relative to controls, but the supplied passages do not link it to anti-gp210 status. Page numbers were not supplied. (LLM, conf=0.90)

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  • The diversity of the intestinal microbiome is decreased in treatment-naive primary biliary cholangitis patients with a unique intestinal microbiota composed of elevated levels of Enterobacteriaceae, Pseudomonas, Veillonella, and Clostridium, along with reduced levels of Oscillospira and Suterella.

    “diversity of the intestinal microbiome is decreased in treatment-naive primary biliary cholangitis patients 34,35 with a unique intestinal microbiota composed of elevated levels of Enterobacteriaceae, Pseudomonas, Veillonella, and Clostridium, along with reduced levels of Oscillospira and Suterella.33”

    From Primary biliary cholangitis. (2024) · cites this paper as [35]

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  • The diversity of the intestinal microbiome is diminished in individuals with primary biliary cholangitis.

    “Notably, the diversity of the intestinal microbiome is diminished in individuals with primary biliary cholangitis.”

    From Primary biliary cholangitis. (2024) · cites this paper as [35]

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  1. [1]Tsuneyama K Baba H Morimoto Y Tsunematsu T Ogawa H. Primary biliary cholangitis: its pathological characteristics and immunopathological mechanisms. J Med Invest (2017) 64(1.2): 7– 13. doi: 10.2152/jmi.64.7 28373632 · DOI
  2. [2]Li Y Tang R Ma X. Epigenetics of primary biliary cholangitis. Adv Exp Med Biol (2020) 1253: 259–83. doi: 10.1007/978-981-15-3449-2_10 32445099 · DOI
  3. [3]Tanaka A Leung PS Gershwin ME. Environmental basis of primary biliary cholangitis. Exp Biol Med (Maywood) (2018) 243(2): 184–9. doi: 10.1177/1535370217748893 PMC5788149 29307284 · DOI
  4. [4]Lleo A Leung PSC Hirschfield GM Gershwin EM. The pathogenesis of primary biliary cholangitis: a comprehensive review. Semin Liver Dis (2020) 40(1): 34– 48. doi: 10.1055/s-0039-1697617 31537031 · DOI
  5. [5]Milosevic I Vujovic A Barac A Djelic M Korac M Radovanovic Spurnic A. Gut-liver axis, gut microbiota, and its modulation in the management of liver diseases: a review of the literature. Int J Mol Sci (2019) 20(2): 395. doi: 10.3390/ijms20020395 30658519 PMC6358912 · DOI · Paper page
  6. [6]Qian Q He W Tang R Ma X. Implications of gut microbiota in autoimmune liver diseases. Minerva Gastroenterol (Torino) (2021) 69(1): 95– 106. doi: 10.23736/S2724-5985.21.02860-9 33793160 · DOI
  7. [7]Albillos A de Gottardi A Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy. J Hepatol (2020) 72(3): 558–77. doi: 10.1016/j.jhep.2019.10.003 31622696 · DOI · Paper page
  8. [8]Tranah TH Edwards LA Schnabl B Shawcross DL. Targeting the gut-liver-immune axis to treat cirrhosis. Gut (2021) 70(5): 982–94. doi: 10.1136/gutjnl-2020-320786 33060124 · DOI
  9. [9]Otani T Furuse M. Tight junction structure and function revisited. Trends Cell Biol (2020) 30(10): 805–17. doi: 10.1016/j.tcb.2020.08.004 32891490 · DOI
  10. [10]Roehlen N Roca Suarez AA El Saghire H Saviano A Schuster C Lupberger J. Tight junction proteins and the biology of hepatobiliary disease. Int J Mol Sci (2020) 21(3): 825. doi: 10.3390/ijms21030825 32012812 PMC7038100 · DOI
  11. [11]Mu Q Kirby J Reilly CM Luo XM. Leaky gut as a danger signal for autoimmune diseases. Front Immunol (2017) 23: 598. doi: 10.3389/fimmu.2017.00598 PMC5440529 28588585 · DOI
  12. [12]Furukawa M Moriya K Nakayama J Inoue T Momoda R Kawaratani H. Gut dysbiosis associated with clinical prognosis of patients with primary biliary cholangitis. Hepatol Res (2020) 50(7): 840–52. doi: 10.1111/hepr.13509 32346970 · DOI
  13. [14]Ludwig J. The pathology of primary biliary cirrhosis and autoimmune cholangitis. Baillieres Best Pract Res Clin Gastroenterol (2000) 14(4): 601–13. doi: 10.1053/bega.2000.0106 10976017 · DOI
  14. [15]Chazouillères O Wendum D Serfaty L Montembault S Rosmorduc O Poupon R. Primary biliary cirrhosis-autoimmune hepatitis overlap syndrome: clinical features and response to therapy. Hepatology (1998) 28(2): 296– 301. doi: 10.1002/hep.510280203 9695990 · DOI · Paper page
  15. [16]Langille MG Zaneveld J Caporaso JG McDonald D Knights D Reyes JA. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol (2013) 31(9): 814–21. doi: 10.1038/nbt.2676 PMC3819121 23975157 · DOI · Paper page
  16. [17]Nakamura M. Clinical significance of autoantibodies in primary biliary cirrhosis. Semin Liver Dis (2014) 34(3): 334–40. doi: 10.1055/s-0034-1383732 25057956 · DOI
  17. [18]Takano K Saeki C Oikawa T Hidaka A Mizuno Y Ishida J. IgM response is a prognostic biomarker of primary biliary cholangitis treated with ursodeoxycholic acid and bezafibrate. J Gastroenterol Hepatol (2020) 35(4): 663–72. doi: 10.1111/jgh.14900 31677185 · DOI
  18. [19]Zeng X Li S Tang S Li X Zhang G Li M. Changes of serum IgG glycosylation patterns in primary biliary cholangitis patients. Front Immunol (2021) 12: 669137. doi: 10.3389/fimmu.2021.669137 34248947 PMC8267527 · DOI
  19. [20]Lin D Wang R Luo J Ren F Gu Z Zhao Y. The core and distinction of the gut microbiota in Chinese populations across geography and ethnicity. Microorganisms (2020) 8(10): 1579. doi: 10.3390/microorganisms8101579 33066420 PMC7602275 · DOI
  20. [21]Han W Huang C Zhang Q Tao S Hu X Xu J. Alterations in gut microbiota and elevated serum bilirubin in primary biliary cholangitis patients treated with ursodeoxycholic acid. Eur J Clin Invest (2022) 52(2): e13714. doi: 10.1111/eci.13714 34800290 · DOI
  21. [22]Winston JA Theriot CM. Diversification of host bile acids by members of the gut microbiota. Gut Microbes (2020) 11(2): 158–71. doi: 10.1080/19490976.2019.1674124 PMC7053883 31595814 · DOI
  22. [23]Abe K Fujita M Hayashi M Okai K Takahashi A Ohira H. Gut and oral microbiota in autoimmune liver disease. Fukushima J Med Sci (2020) 65(3): 71–5. doi: 10.5387/fms PMC7012591 31564673 · DOI
  23. [24]Stemerowicz R Hopf U Möller B Wittenbrink C Rodloff A Reinhardt R. Are antimitochondrial antibodies in primary biliary cirrhosis induced by r(rough)-mutants of enterobacteriaceae? Lancet (1988) 2(8621): 1166–70. doi: 10.1016/s0140-6736(88)90235-8 2903378 · DOI
  24. [25]Shoenfeld Y Blank M Abu-Shakra M Amital H Barzilai O Berkun Y. The mosaic of autoimmunity: prediction, autoantibodies, and therapy in autoimmune diseases–2008. Isr Med Assoc J (2008) 10(1): 13–9. 18300564
  25. [26]Louis P Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett (2009) 294(1): 1– 8. doi: 10.1111/j.1574-6968.2009.01514.x 19222573 · DOI · Paper page
  26. [27]Xu HM Huang HL Xu J He J Zhao C Peng Y. Cross-talk between butyric acid and gut microbiota in ulcerative colitis following fecal microbiota transplantation. Front Microbiol (2021) 12: 658292. doi: 10.3389/fmicb.2021.658292 33912150 PMC8071877 · DOI
  27. [28]Yoo HY Park SY Chang SY Kim SH. Regulation of butyrate-induced resistance through AMPK signaling pathway in human colon cancer cells. Biomedicines (2021) 9(11): 1604. doi: 10.3390/biomedicines9111604 34829834 PMC8615665 · DOI
  28. [29]Salvi PS Cowles RA. Butyrate and the intestinal epithelium: modulation of proliferation and inflammation in homeostasis and disease. Cells (2021) 10(7): 1775. doi: 10.3390/cells10071775 34359944 PMC8304699 · DOI
  29. [30]Parada Venegas D de la Fuente MK Landskron G González MJ Quera R Dijkstra G. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol (2019) 10: 277. doi: 10.3389/fimmu.2019.00277 30915065 PMC6421268 · DOI · Paper page
  30. [32]Li G Lin J Zhang C Gao H Lu H Gao X. Microbiota metabolite butyrate constrains neutrophil functions and ameliorates mucosal inflammation in inflammatory bowel disease. Gut Microbes (2021) 13(1): 1968257. doi: 10.1080/19490976.2021.1968257 34494943 PMC8437544 · DOI
  31. [33]Kakiyama G Pandak WM Gillevet PM Hylemon PB Heuman DM Daita K. Modulation of the fecal bile acid profile by gut microbiota in cirrhosis. J Hepatol (2013) 58(5): 949–55. doi: 10.1016/j.jhep.2013.01.003 PMC3936319 23333527 · DOI
  32. [34]Lázár B László SB Hutka B Tóth AS Mohammadzadeh A Berekméri E. A comprehensive time course and correlation analysis of indomethacin-induced inflammation, bile acid alterations and dysbiosis in the rat small intestine. Biochem Pharmacol (2021) 190: 114590. doi: 10.1016/j.bcp.2021.114590 33940029 · DOI
  33. [35]Sinha SR Haileselassie Y Nguyen LP Tropini C Wang M Becker LS. Dysbiosis-induced secondary bile acid deficiency promotes intestinal inflammation. Cell Host Microbe (2020) 27(4): 659– 670.e5. doi: 10.1016/j.chom.2020.01.021 32101703 PMC8172352 · DOI
  34. [37]Tan J McKenzie C Vuillermin PJ Goverse G Vinuesa CG Mebius RE. Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep (2016) 15(12): 2809–24. doi: 10.1016/j.celrep.2016.05.047 27332875 · DOI
  35. [38]Portincasa P Bonfrate L Vacca M De Angelis M Farella I Lanza E. Gut microbiota and short chain fatty acids: implications in glucose homeostasis. Int J Mol Sci (2022) 23(3): 1105. doi: 10.3390/ijms23031105 35163038 PMC8835596 · DOI
  36. [39]Morrison DJ Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes (2016) 7(3): 189– 200. doi: 10.1080/19490976.2015.1134082 26963409 PMC4939913 · DOI · Paper page
  37. [40]Lammert C Shin A Xu H Hemmerich C O’Connell TM Chalasani N. Short-chain fatty acid and fecal microbiota profiles are linked to fibrosis in primary biliary cholangitis. FEMS Microbiol Lett (2021) 368(6): fnab038. doi: 10.1093/femsle/fnab038 33836051 PMC8062329 · DOI

Cited by

Sorted by citations

Authors
Zhou, Y.-J., Ying, G.-X., Dong, S.-L., Xiang, B., & Jin, Q.-F.
Affiliations
Hangzhou Xixi hospital (CN)
Venue
Frontiers in Immunology
Published
2023-05-08
Volume
14
Pages
1126117-1126117
ISSN
1664-3224 (ISSN-L)
OpenAlex
W4375866985
Cited by
26
References
4
Citations by year
2026: 8 · 2025: 6 · 2024: 10 · 2023: 2
FWCI
2.32
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Immunology (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
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 biliary cirrhosis, gut microbiota, biomarkers, alpha diversity, Serratia, Oscillospiraceae, Faecalibacterium, Ruminococcaceae, Coprococcus, lipid metabolism, secondary metabolite biosynthesis, disease severity
MeSH terms
Clostridiales, Eubacteriales, Gastrointestinal Microbiome, Humans, Liver Cirrhosis, Biliary, RNA, Ribosomal, 16S, Area Under Curve, Benchmarking, Lactobacillales

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