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Cited by 127Gut microbiota and healthLiver Disease and TransplantationClostridium difficile and Clostridium perfringens research

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Predicting Clinical Outcomes of Cirrhosis Patients With Hepatic Encephalopathy From the Fecal Microbiome

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Sung, Chang Mu, Lin, Yu-fei, Chen, Kuan-Fu, Ke, Huei-mien, Huang, Hao-Yi, Gong, Yu-Nong, Tsai, Wen-Sy, You, Jeng-Fu, Lu, Meiyeh J., Cheng, Hao-Tsai, Lin, Cheng-Yu, Kuo, Chia-Jung, Tsai, Isheng J., Hsieh, Sen-Yung·2019·Cellular and Molecular Gastroenterology and Hepatology
DOI 10.1016/j.jcmgh.2019.04.008PMC PMC6718362
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Abstract

BACKGROUND & AIMS: Gut dysbiosis plays a role in hepatic encephalopathy (HE), while its relationship at the acute episode of overt HE (AHE), the disease progression and clinical outcomes remains unclear. We aimed to identify AHE-specific microbiome and its association to patients' outcomes. METHODS: We profiled fecal microbiome changes for a cohort of 62 patients with cirrhosis and AHE i) before treatment, ii) 2-3 days after medication and iii) 2-3 months after recovery, and three control cohorts i) healthy individuals, patients with ii) compensated or iii) decompensated cirrhosis. RESULTS: Comparison of the microbiome shift from compensated, decompensated cirrhosis, AHE to recovery revealed the AHE-specific gut-dysbiosis. The gut microbiome diversity was decreased during AHE, further reduced after medication, and only partially reversed during the recovery. The relative abundance of Bacteroidetes phylum in the microbiome decreased, whereas that of Firmicute, Proteobacteria and Actinobacteria increased in patients during AHE compared with those with compensated cirrhosis. A total of 70 operational taxonomic units (OTUs) were significantly different between AHE and decompensated cirrhosis abundances. Of them, the abundance of Veillonella parvula increased the most during AHE via a metagenomics recovery of the genomes. Moreover, the relative abundances of three (Alistipes, Bacteroides, Phascolarctobacterium) and five OTUs (Clostridium-XI, Bacteroides, Bacteroides, Lactobacillus, Clostridium-sedis) at AHE were respectively associated with HE recurrence and overall survival during the subsequent one-year follow-up. CONCLUSIONS: AHE-specific gut OTUs were identified that may be involved in HE development and able to predict clinical outcomes, providing new strategies for the prevention and treatment of HE recurrence in patients with cirrhosis.

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Graphical abstract CC BY-NC-ND · PubMed Central
Figure 1 Rarefaction curves of all 16S amplicon samples from patients.
Figure 1 Rarefaction curves of all 16S amplicon samples from patients.CC BY-NC-ND · PubMed Central
Figure 2 (A) Alpha diversity pattern with control groups (C1, C2, and C3) and AHE patients at different stages (D1, D2, and D3). Significances of different diversity between samples were assessed by Tukey’s HSD (*P < .05; **P < .01; ***P < .001; ****P < .0001). (B) AHE patients at different stages shift microbial community structure. Samples from both control groups are not distinct from each other (C1 and C2). Samples from AHE patients were shifted away from control groups according to their disease status (D1, D2, and D3). D3 is relatively overlapping with C3 (decompensated cirrhosis without recent HE).
Figure 2 (A) Alpha diversity pattern with control groups (C1, C2, and C3) and AHE patients at different stages (D1, D2, and D3). Significances of different diversity between samples were assessed by Tukey’s HSD (*P < .05; **P < .01; ***P < .001; ****P < .0001). (B) AHE patients at different stages shift microbial community structure. Samples from both control groups are not distinct from each other (C1 and C2). Samples from AHE patients were shifted away from control groups according to their disease status (D1, D2, and D3). D3 is relatively overlapping with C3 (decompensated cirrhosis without recent HE).CC BY-NC-ND · PubMed Central
Figure 3 Relative abundance of OTUs in healthy patients (top, C1), control cirrhosis patients (middle, C2), and advanced cirrhosis patients (bottom, C3) at the phylum and genus levels. Only the top 30 most abundant OTUs in each group are shown.
Figure 3 Relative abundance of OTUs in healthy patients (top, C1), control cirrhosis patients (middle, C2), and advanced cirrhosis patients (bottom, C3) at the phylum and genus levels. Only the top 30 most abundant OTUs in each group are shown.CC BY-NC-ND · PubMed Central
Figure 4 Relative abundance of OTUs in AHE patients (top), AHE patients during treatment (middle), and recovered AHE patients (bottom) at the phylum and genus levels. Only the top 30 most abundant OTUs in each group are shown.
Figure 4 Relative abundance of OTUs in AHE patients (top), AHE patients during treatment (middle), and recovered AHE patients (bottom) at the phylum and genus levels. Only the top 30 most abundant OTUs in each group are shown.CC BY-NC-ND · PubMed Central
Figure 5 (A) Relative abundances at the 4 major phylum levels between groups. Boxplots show the median and interquartile range of relative abundances (%). Dots represent the relative abundances of samples. (B) Different combinations of phyla/Bacteroidetes ratios in distinguishing D1 from C2 and C3.
Figure 5 (A) Relative abundances at the 4 major phylum levels between groups. Boxplots show the median and interquartile range of relative abundances (%). Dots represent the relative abundances of samples. (B) Different combinations of phyla/Bacteroidetes ratios in distinguishing D1 from C2 and C3.CC BY-NC-ND · PubMed Central
Figure 6 Distribution of relative abundances for 16 signature OTUs at the C2, C3, D1, and D3 stages. Boxplots show the median and interquartile range of relative abundance (%). Red dots denote mean relative abundances of each category, the raw values of which are listed in Table 3. Arrowheads indicate those whose abundances related to clinical outcomes.
Figure 6 Distribution of relative abundances for 16 signature OTUs at the C2, C3, D1, and D3 stages. Boxplots show the median and interquartile range of relative abundance (%). Red dots denote mean relative abundances of each category, the raw values of which are listed in Table 3. Arrowheads indicate those whose abundances related to clinical outcomes.CC BY-NC-ND · PubMed Central
Figure 7 Phylogenetic tree of Veillonella species.
Figure 7 Phylogenetic tree of Veillonella species.CC BY-NC-ND · PubMed Central
Figure 8 Whole genome alignment between the reconstructed OTU3 genome vs the Te3 Veillonella parvula type strain. Dashed line indicates scaffold boundaries and purple dots/line denote matched alignment.
Figure 8 Whole genome alignment between the reconstructed OTU3 genome vs the Te3 Veillonella parvula type strain. Dashed line indicates scaffold boundaries and purple dots/line denote matched alignment.CC BY-NC-ND · PubMed Central
Figure 9 (A) Boxplots of relative abundances for 3 OTUs at the AHE stage from patients with or without recurrences. (B) Scatterplot of the relative abundances of OTU7 at AHE stage against the number of recurrence (Pearson’s r = –0.26, P = .046). (C) Boxplots of relative abundances for 5 OTUs that were with significantly different abundance between patients with different mortality outcome.
Figure 9 (A) Boxplots of relative abundances for 3 OTUs at the AHE stage from patients with or without recurrences. (B) Scatterplot of the relative abundances of OTU7 at AHE stage against the number of recurrence (Pearson’s r = –0.26, P = .046). (C) Boxplots of relative abundances for 5 OTUs that were with significantly different abundance between patients with different mortality outcome.CC BY-NC-ND · PubMed Central
Figure 10 The abundances of control cirrhosis–enriched and AHE-enriched KEGG functional terms. Abundances were plotted as transformed values from counts of inferred KEGG orthologues. For visualization comparison, abundances from healthy individuals were also plotted.
Figure 10 The abundances of control cirrhosis–enriched and AHE-enriched KEGG functional terms. Abundances were plotted as transformed values from counts of inferred KEGG orthologues. For visualization comparison, abundances from healthy individuals were also plotted.CC BY-NC-ND · PubMed Central

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Metadata

Authors
Sung, C. M., Lin, Y.-F., Chen, K.-F., Ke, H.-M., Huang, H.-Y., Gong, Y.-N., Tsai, W.-S., You, J.-F., Lu, M. J., Cheng, H.-T., Lin, C.-Y., Kuo, C.-J., Tsai, I. J., & Hsieh, S.-Y.
Affiliations
  • Chang Gung University (TW)
  • Biodiversity Research Center, Academia Sinica (TW)
  • Chang Gung Memorial Hospital (TW)
Corresponding author
  • Tsai, Isheng J.
  • Hsieh, Sen-Yung
ORCID
Venue
Cellular and Molecular Gastroenterology and Hepatology
Publisher
Elsevier BV
Published
2019
Volume
8
Issue
2
Pages
301-318.e2
ISSN
2352-345X (ISSN-L)
DOI
10.1016/j.jcmgh.2019.04.008
PMC
PMC6718362
OpenAlex
W2938740358
Cited by
127
References
45
Citations by year
2026: 9 · 2025: 16 · 2024: 17 · 2023: 22 · 2022: 24 · 2021: 21 · 2020: 13 · 2019: 5
FWCI
5.21
Type
journal article
Language
en
Open access
Licence
Locations
  • Cellular and Molecular Gastroenterology and Hepatology (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Health Research Institutes (NHRI-EX106-10619SC)
  • Chang Gung Medical Foundation (CMRPG 3E1411-3, 3H1031-3)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Hepatology › Liver Disease and Transplantation
  • Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
Keywords
hepatic encephalopathy, liver cirrhosis, gut microbiota, gut dysbiosis, fecal microbiota, decompensated cirrhosis, clinical outcome prediction, Veillonella parvula, Bacteroides, Phascolarctobacterium, Clostridium, Lactobacillus, overall survival, microbiome diversity
MeSH terms
Gastrointestinal Microbiome, Adult, Aged, Bacteria, Feces, Female, Hepatic Encephalopathy, Humans, Liver Cirrhosis, Male, Middle Aged, Prognosis, Dysbiosis

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