Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depression

Abstract The relationships of the gut microbiota-inflammation-brain axis in depressive bipolar disorder (BD) remains under-elaborated. Sixty-five unmedicated depressive patients with BD II and 58 controls (HCs) were prospectively enrolled. Resting-state functional MRI data of static and dynamic ampl...

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Main Authors: Zixuan Guo, Shu Xiao, Guanmao Chen, Shuming Zhong, Hui Zhong, Shilin Sun, Pan Chen, Xinyue Tang, Hengwen Yang, Yanbin Jia, Zhinan Yin, Li Huang, Ying Wang
Format: Article
Language:English
Published: Nature Publishing Group 2024-12-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-024-03207-0
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author Zixuan Guo
Shu Xiao
Guanmao Chen
Shuming Zhong
Hui Zhong
Shilin Sun
Pan Chen
Xinyue Tang
Hengwen Yang
Yanbin Jia
Zhinan Yin
Li Huang
Ying Wang
author_facet Zixuan Guo
Shu Xiao
Guanmao Chen
Shuming Zhong
Hui Zhong
Shilin Sun
Pan Chen
Xinyue Tang
Hengwen Yang
Yanbin Jia
Zhinan Yin
Li Huang
Ying Wang
author_sort Zixuan Guo
collection DOAJ
description Abstract The relationships of the gut microbiota-inflammation-brain axis in depressive bipolar disorder (BD) remains under-elaborated. Sixty-five unmedicated depressive patients with BD II and 58 controls (HCs) were prospectively enrolled. Resting-state functional MRI data of static and dynamic amplitude of low-frequency fluctuation (ALFF) was measured, and abnormal ALFF masks were subsequently set as regions of interest to calculate whole-brain static functional connectivity (sFC) and dynamic functional connectivity (dFC). Fecal samples were collected to assess gut diversity and enterotypes using 16S amplicon sequencing. Blood samples were also collected, serum was assayed for levels of cytokines (interleukin [IL]-2, IL-4, IL-6, IL-8, IL-10, tumor necrosis factor [TNF]-α). Patients with BD II exhibited decreased static ALFF values in the left cerebellum Crus II, and decreased cerebellar sFC and dFC to the right inferior parietal lobule and right superior frontal gyrus, respectively. Moreover, higher pro-inflammatory and anti-inflammatory cytokines levels, and increased proinflammatory bacteria and glutamate and gamma-aminobutyric acid metabolism related bacteria were identified in BD II. The interaction of Parabacteroides levels × IL-8 levels was an independent contributor to static ALFF in the left cerebellar Crus II. The findings bridged a gap in the underlying pathophysiological mechanism of the gut microbiota-inflammation-brain axis in BD II depression.
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spelling doaj-art-19533863991c4f268c8e39df895a5b122024-12-22T12:49:24ZengNature Publishing GroupTranslational Psychiatry2158-31882024-12-0114111010.1038/s41398-024-03207-0Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depressionZixuan Guo0Shu Xiao1Guanmao Chen2Shuming Zhong3Hui Zhong4Shilin Sun5Pan Chen6Xinyue Tang7Hengwen Yang8Yanbin Jia9Zhinan Yin10Li Huang11Ying Wang12Medical Imaging Center, First Affiliated Hospital of Jinan UniversityMedical Imaging Center, First Affiliated Hospital of Jinan UniversityMedical Imaging Center, First Affiliated Hospital of Jinan UniversityDepartment of Psychiatry, First Affiliated Hospital of Jinan UniversityBiomedical Translational Research Institute, Jinan UniversityMedical Imaging Center, First Affiliated Hospital of Jinan UniversityMedical Imaging Center, First Affiliated Hospital of Jinan UniversityMedical Imaging Center, First Affiliated Hospital of Jinan UniversityBiomedical Translational Research Institute, Jinan UniversityDepartment of Psychiatry, First Affiliated Hospital of Jinan UniversityBiomedical Translational Research Institute, Jinan UniversityMedical Imaging Center, First Affiliated Hospital of Jinan UniversityMedical Imaging Center, First Affiliated Hospital of Jinan UniversityAbstract The relationships of the gut microbiota-inflammation-brain axis in depressive bipolar disorder (BD) remains under-elaborated. Sixty-five unmedicated depressive patients with BD II and 58 controls (HCs) were prospectively enrolled. Resting-state functional MRI data of static and dynamic amplitude of low-frequency fluctuation (ALFF) was measured, and abnormal ALFF masks were subsequently set as regions of interest to calculate whole-brain static functional connectivity (sFC) and dynamic functional connectivity (dFC). Fecal samples were collected to assess gut diversity and enterotypes using 16S amplicon sequencing. Blood samples were also collected, serum was assayed for levels of cytokines (interleukin [IL]-2, IL-4, IL-6, IL-8, IL-10, tumor necrosis factor [TNF]-α). Patients with BD II exhibited decreased static ALFF values in the left cerebellum Crus II, and decreased cerebellar sFC and dFC to the right inferior parietal lobule and right superior frontal gyrus, respectively. Moreover, higher pro-inflammatory and anti-inflammatory cytokines levels, and increased proinflammatory bacteria and glutamate and gamma-aminobutyric acid metabolism related bacteria were identified in BD II. The interaction of Parabacteroides levels × IL-8 levels was an independent contributor to static ALFF in the left cerebellar Crus II. The findings bridged a gap in the underlying pathophysiological mechanism of the gut microbiota-inflammation-brain axis in BD II depression.https://doi.org/10.1038/s41398-024-03207-0
spellingShingle Zixuan Guo
Shu Xiao
Guanmao Chen
Shuming Zhong
Hui Zhong
Shilin Sun
Pan Chen
Xinyue Tang
Hengwen Yang
Yanbin Jia
Zhinan Yin
Li Huang
Ying Wang
Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depression
Translational Psychiatry
title Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depression
title_full Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depression
title_fullStr Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depression
title_full_unstemmed Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depression
title_short Disruption of the gut microbiota-inflammation-brain axis in unmedicated bipolar disorder II depression
title_sort disruption of the gut microbiota inflammation brain axis in unmedicated bipolar disorder ii depression
url https://doi.org/10.1038/s41398-024-03207-0
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