Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairment

Abstract Background Microbiota-gut-brain axis interacts with one another to regulate brain functions. However, whether the impacts of gut dysbiosis on limbic white matter (WM) tracts contribute to the neuropsychiatric symptoms (NPS) in patients with amyloid-positive amnestic mild cognitive impairmen...

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Main Authors: Chun-Che Hung, Yi-Ping Chao, Yejin Lee, Chi-Wei Huang, Shu-Hua Huang, Chiung-Chih Chang, Chia-Hsiung Cheng
Format: Article
Language:English
Published: BMC 2023-11-01
Series:BMC Geriatrics
Subjects:
Online Access:https://doi.org/10.1186/s12877-023-04417-9
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author Chun-Che Hung
Yi-Ping Chao
Yejin Lee
Chi-Wei Huang
Shu-Hua Huang
Chiung-Chih Chang
Chia-Hsiung Cheng
author_facet Chun-Che Hung
Yi-Ping Chao
Yejin Lee
Chi-Wei Huang
Shu-Hua Huang
Chiung-Chih Chang
Chia-Hsiung Cheng
author_sort Chun-Che Hung
collection DOAJ
description Abstract Background Microbiota-gut-brain axis interacts with one another to regulate brain functions. However, whether the impacts of gut dysbiosis on limbic white matter (WM) tracts contribute to the neuropsychiatric symptoms (NPS) in patients with amyloid-positive amnestic mild cognitive impairment (aMCI+), have not been explored yet. This study aimed to investigate the mediation effects of limbic WM integrity on the association between gut microbiota and NPS in patients with aMCI+. Methods Twenty patients with aMCI + and 20 healthy controls (HCs) were enrolled. All subjects underwent neuropsychological assessments and their microbial compositions were characterized using 16S rRNA Miseq sequencing technique. Amyloid deposition inspected by positron emission tomography imaging and limbic WM tracts (i.e., fornix, cingulum, and uncinate fasciculus) detected by diffusion tensor imaging were additionally measured in patients with aMCI+. We employed a regression-based mediation analysis using Hayes’s PROCESS macro in this study. Results The relative abundance of genera Ruminococcus and Lactococcus was significantly decreased in patients with aMCI + versus HCs. The relative abundance of Ruminococcus was negatively correlated with affective symptom cluster in the aMCI + group. Notably, this association was mediated by WM integrity of the left cingulate gyrus. Conclusions Our findings suggest Ruminococcus as a potential target for the management of affective impairments in patients with aMCI+.
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spelling doaj.art-8d2e3f319f87490bbdfae2c54e8e7c962023-11-12T12:29:37ZengBMCBMC Geriatrics1471-23182023-11-0123111310.1186/s12877-023-04417-9Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairmentChun-Che Hung0Yi-Ping Chao1Yejin Lee2Chi-Wei Huang3Shu-Hua Huang4Chiung-Chih Chang5Chia-Hsiung Cheng6Department of Occupational Therapy and Graduate Institute of Behavioral Sciences, Chang Gung UniversityDepartment of Computer Science and Information Engineering, Chang Gung UniversityProgram in Occupational Therapy, Washington University School of MedicineDepartment of Neurology, Institute for Translational Research in Biomedicine, Kaohsiung Chang Gung Memorial Hospital, Chang Gung university College of MedicineDepartment of Nuclear Medicine, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of MedicineDepartment of Neurology, Institute for Translational Research in Biomedicine, Kaohsiung Chang Gung Memorial Hospital, Chang Gung university College of MedicineDepartment of Occupational Therapy and Graduate Institute of Behavioral Sciences, Chang Gung UniversityAbstract Background Microbiota-gut-brain axis interacts with one another to regulate brain functions. However, whether the impacts of gut dysbiosis on limbic white matter (WM) tracts contribute to the neuropsychiatric symptoms (NPS) in patients with amyloid-positive amnestic mild cognitive impairment (aMCI+), have not been explored yet. This study aimed to investigate the mediation effects of limbic WM integrity on the association between gut microbiota and NPS in patients with aMCI+. Methods Twenty patients with aMCI + and 20 healthy controls (HCs) were enrolled. All subjects underwent neuropsychological assessments and their microbial compositions were characterized using 16S rRNA Miseq sequencing technique. Amyloid deposition inspected by positron emission tomography imaging and limbic WM tracts (i.e., fornix, cingulum, and uncinate fasciculus) detected by diffusion tensor imaging were additionally measured in patients with aMCI+. We employed a regression-based mediation analysis using Hayes’s PROCESS macro in this study. Results The relative abundance of genera Ruminococcus and Lactococcus was significantly decreased in patients with aMCI + versus HCs. The relative abundance of Ruminococcus was negatively correlated with affective symptom cluster in the aMCI + group. Notably, this association was mediated by WM integrity of the left cingulate gyrus. Conclusions Our findings suggest Ruminococcus as a potential target for the management of affective impairments in patients with aMCI+.https://doi.org/10.1186/s12877-023-04417-9Amnestic mild cognitive impairmentDiffusion tensor imagingGut microbiotaLimbic systemNeuropsychiatric symptomsRuminococcus
spellingShingle Chun-Che Hung
Yi-Ping Chao
Yejin Lee
Chi-Wei Huang
Shu-Hua Huang
Chiung-Chih Chang
Chia-Hsiung Cheng
Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairment
BMC Geriatrics
Amnestic mild cognitive impairment
Diffusion tensor imaging
Gut microbiota
Limbic system
Neuropsychiatric symptoms
Ruminococcus
title Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairment
title_full Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairment
title_fullStr Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairment
title_full_unstemmed Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairment
title_short Cingulate white matter mediates the effects of fecal Ruminococcus on neuropsychiatric symptoms in patients with amyloid-positive amnestic mild cognitive impairment
title_sort cingulate white matter mediates the effects of fecal ruminococcus on neuropsychiatric symptoms in patients with amyloid positive amnestic mild cognitive impairment
topic Amnestic mild cognitive impairment
Diffusion tensor imaging
Gut microbiota
Limbic system
Neuropsychiatric symptoms
Ruminococcus
url https://doi.org/10.1186/s12877-023-04417-9
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