Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia

Accumulation of pathological tau is one of the primary causes of Primary Progressive Aphasia (PPA). The glymphatic system is crucial for removing metabolite waste from the brain whereas impairments in glymphatic clearance in PPA are poorly understood. Thus, this study aims to investigate the role of...

Full description

Saved in:
Bibliographic Details
Main Authors: Xinglin Zeng, Lin Hua, Guolin Ma, Zhiying Zhao, Zhen Yuan
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S105381192400421X
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850266259532283904
author Xinglin Zeng
Lin Hua
Guolin Ma
Zhiying Zhao
Zhen Yuan
author_facet Xinglin Zeng
Lin Hua
Guolin Ma
Zhiying Zhao
Zhen Yuan
author_sort Xinglin Zeng
collection DOAJ
description Accumulation of pathological tau is one of the primary causes of Primary Progressive Aphasia (PPA). The glymphatic system is crucial for removing metabolite waste from the brain whereas impairments in glymphatic clearance in PPA are poorly understood. Thus, this study aims to investigate the role of dysregulated macroscopic cerebrospinal fluid (CSF) movement in PPA. Fifty-six PPA individuals and ninety-four healthy controls were included in our analysis after excluding those with excessive head motions during the scan. The coupling strength between blood-oxygen-level-dependent (BOLD) signals in the gray matter and CSF flow was calculated using Pearson correlation and compared between the groups. Its associations with clinical characteristics including scores from Clinical Dementia Rating (CDR), Mini-Mental State Exam, Geriatric Depression Scale and with morphological measures in the hippocampus and entorhinal cortex were examined. PPA subjects exhibited weaker global BOLD-CSF coupling compared to HCs, indicating impairments in glymphatic function in the patients (p = 0.01). In the PPA but not HC group, global BOLD-CSF coupling correlated with the CDR scores (p = 0.04) and hippocampal volume (p = 0.009). The observed decoupling between global brain activity and CSF flow and its association with symptomatology and brain structural changes in PPA converges with previous reports on the same measure in other neurodegenerative diseases. These findings support the potential role of global BOLD-CSF coupling as a noninvasive marker for glymphatic dysregulation in PPA.
format Article
id doaj-art-fb3af861ea9042d2af0f9ba656866b81
institution OA Journals
issn 1095-9572
language English
publishDate 2024-12-01
publisher Elsevier
record_format Article
series NeuroImage
spelling doaj-art-fb3af861ea9042d2af0f9ba656866b812025-08-20T01:54:12ZengElsevierNeuroImage1095-95722024-12-0130312092410.1016/j.neuroimage.2024.120924Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasiaXinglin Zeng0Lin Hua1Guolin Ma2Zhiying Zhao3Zhen Yuan4Faculty of Health Sciences, University of Macau, Macau SAR, China; Centre for Cognitive and Brain Sciences, University of Macau, Macau SAR, ChinaFaculty of Health Sciences, University of Macau, Macau SAR, China; Centre for Cognitive and Brain Sciences, University of Macau, Macau SAR, ChinaDepartment of Radiology, China-Japan Friendship Hospital, Beijing, PR ChinaCentre for Cognitive and Brain Sciences, University of Macau, Macau SAR, China; Corresponding authors: Centre for Cognitive and Brain Sciences, N21 Building, University of Macau, Macau SAR, 999078, PR China.Faculty of Health Sciences, University of Macau, Macau SAR, China; Centre for Cognitive and Brain Sciences, University of Macau, Macau SAR, China; Corresponding authors: Centre for Cognitive and Brain Sciences, N21 Building, University of Macau, Macau SAR, 999078, PR China.Accumulation of pathological tau is one of the primary causes of Primary Progressive Aphasia (PPA). The glymphatic system is crucial for removing metabolite waste from the brain whereas impairments in glymphatic clearance in PPA are poorly understood. Thus, this study aims to investigate the role of dysregulated macroscopic cerebrospinal fluid (CSF) movement in PPA. Fifty-six PPA individuals and ninety-four healthy controls were included in our analysis after excluding those with excessive head motions during the scan. The coupling strength between blood-oxygen-level-dependent (BOLD) signals in the gray matter and CSF flow was calculated using Pearson correlation and compared between the groups. Its associations with clinical characteristics including scores from Clinical Dementia Rating (CDR), Mini-Mental State Exam, Geriatric Depression Scale and with morphological measures in the hippocampus and entorhinal cortex were examined. PPA subjects exhibited weaker global BOLD-CSF coupling compared to HCs, indicating impairments in glymphatic function in the patients (p = 0.01). In the PPA but not HC group, global BOLD-CSF coupling correlated with the CDR scores (p = 0.04) and hippocampal volume (p = 0.009). The observed decoupling between global brain activity and CSF flow and its association with symptomatology and brain structural changes in PPA converges with previous reports on the same measure in other neurodegenerative diseases. These findings support the potential role of global BOLD-CSF coupling as a noninvasive marker for glymphatic dysregulation in PPA.http://www.sciencedirect.com/science/article/pii/S105381192400421XPrimary progressive aphasiaFrontotemporal dementiaCerebrospinal fluidGlymphatic functionGlobal brain activity
spellingShingle Xinglin Zeng
Lin Hua
Guolin Ma
Zhiying Zhao
Zhen Yuan
Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia
NeuroImage
Primary progressive aphasia
Frontotemporal dementia
Cerebrospinal fluid
Glymphatic function
Global brain activity
title Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia
title_full Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia
title_fullStr Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia
title_full_unstemmed Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia
title_short Dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia
title_sort dysregulated neurofluid coupling as a new noninvasive biomarker for primary progressive aphasia
topic Primary progressive aphasia
Frontotemporal dementia
Cerebrospinal fluid
Glymphatic function
Global brain activity
url http://www.sciencedirect.com/science/article/pii/S105381192400421X
work_keys_str_mv AT xinglinzeng dysregulatedneurofluidcouplingasanewnoninvasivebiomarkerforprimaryprogressiveaphasia
AT linhua dysregulatedneurofluidcouplingasanewnoninvasivebiomarkerforprimaryprogressiveaphasia
AT guolinma dysregulatedneurofluidcouplingasanewnoninvasivebiomarkerforprimaryprogressiveaphasia
AT zhiyingzhao dysregulatedneurofluidcouplingasanewnoninvasivebiomarkerforprimaryprogressiveaphasia
AT zhenyuan dysregulatedneurofluidcouplingasanewnoninvasivebiomarkerforprimaryprogressiveaphasia