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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BMC
2023-11-01
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Series: | BMC Geriatrics |
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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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issn | 1471-2318 |
language | English |
last_indexed | 2024-03-11T11:01:15Z |
publishDate | 2023-11-01 |
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series | BMC Geriatrics |
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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