Hepatology International

, Volume 13, Issue 4, pp 482–489 | Cite as

Bacteroides in colonic mucosa-associated microbiota affects the development of minimal hepatic encephalopathy in patients with cirrhosis

  • Masafumi Haraguchi
  • Satoshi MiumaEmail author
  • Hiroshi Masumoto
  • Tatsuki Ichikawa
  • Yasuko Kanda
  • Ryu Sasaki
  • Masanori Fukushima
  • Hisamitsu Miyaaki
  • Naota Taura
  • Kazuhiko Nakao
Original Article



Gut microbiota has been associated with liver cirrhosis and, possibly, hepatic encephalopathy. However, only a few studies have examined the link between mucosa-associated microbiota (MAM) and minimal hepatic encephalopathy (MHE). Our aim was to investigate this relationship.


Twenty-four patients with cirrhosis underwent colon biopsies at our institution, between January 2014 and April 2015. Patterns of microbial colonization were examined using 16S rRNA gene sequences. MHE was diagnosed using the Neuropsychological Test.


Ten (41.7%) of the 24 patients were diagnosed as having MHE. There was no significant difference in the diversity of gut microbiota by sampling locations between those with and without MHE. However, the diversity of the gut microbiota and the proportion of the genus Bacteroides decreased as a function of declining liver function. We divided patients into those with the highest proportion of the genus Bacteroides (Bacteroides-dominant group; n = 9) and into a Bacteroides non-dominant group (n = 15). In the Bacteroides-dominant group, only 1 patient (11.1%) was diagnosed as having MHE, with the incidence rate of MHE being significantly lower in the Bacteroides-dominant group than in the non-dominant group (p = 0.019). The Child–Pugh score (p = 0.05) and use of proton-pump inhibitors (p = 0.015) were negatively correlated to the proportion of Bacteroides. Furthermore, the proportion of the family Clostridiaceae was significantly higher in the Bacteroides-dominant group than in the non-dominant group (p = 0.078).


The decrease in microbial diversity and genus Bacteroides in MAM is a risk factor for MHE in patients with liver cirrhosis.


Microbiota Cirrhosis Minimal hepatic encephalopathy Next-generation sequencing 


Compliance with ethical standards

Conflict of interest

Authors Dr. Haraguchi, Dr. Miuma, Dr. Masumoto, Dr. Ichikawa, Dr. Kanda, Dr. Sasaki, Dr. Fukushima, Dr. Miyaaki, Dr. Taura, and Dr. Nakao declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All patients provided informed consent, and our study protocol conformed to the guidelines of the Declaration of Helsinki and was approved by the Nagasaki University Ethics Committee (approval no. 13120201).

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

12072_2019_9963_MOESM1_ESM.docx (142 kb)
Supplementary material 1 (DOCX 142 kb)
12072_2019_9963_MOESM2_ESM.docx (36 kb)
Supplementary material 2 (DOCX 35 kb)


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Copyright information

© Asian Pacific Association for the Study of the Liver 2019

Authors and Affiliations

  • Masafumi Haraguchi
    • 1
  • Satoshi Miuma
    • 1
    Email author
  • Hiroshi Masumoto
    • 2
  • Tatsuki Ichikawa
    • 3
  • Yasuko Kanda
    • 1
  • Ryu Sasaki
    • 1
  • Masanori Fukushima
    • 1
  • Hisamitsu Miyaaki
    • 1
  • Naota Taura
    • 1
  • Kazuhiko Nakao
    • 1
  1. 1.Department of Gastroenterology and HepatologyNagasaki University Graduate School of Biomedical SciencesNagasakiJapan
  2. 2.Biomedical Research Support CenterNagasaki University School of MedicineNagasakiJapan
  3. 3.Department of GastroenterologyNagasaki Harbor Medical Center City HospitalNagasakiJapan

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