Cargando…

Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus

The occurrence of significant Alzheimer’s disease (AD) pathology was described in approximately 30% of normal pressure hydrocephalus (NPH) cases, leading to the distinction between neurodegenerative and idiopathic forms of this disorder. Whether or not there is a specific MRI signature of NPH remain...

Descripción completa

Detalles Bibliográficos
Autores principales: Haller, Sven, Montandon, Marie-Louise, Rodriguez, Cristelle, Herrmann, François R., Giannakopoulos, Panteleimon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10655029/
https://www.ncbi.nlm.nih.gov/pubmed/38020768
http://dx.doi.org/10.3389/fnagi.2023.1242158
_version_ 1785136737846034432
author Haller, Sven
Montandon, Marie-Louise
Rodriguez, Cristelle
Herrmann, François R.
Giannakopoulos, Panteleimon
author_facet Haller, Sven
Montandon, Marie-Louise
Rodriguez, Cristelle
Herrmann, François R.
Giannakopoulos, Panteleimon
author_sort Haller, Sven
collection PubMed
description The occurrence of significant Alzheimer’s disease (AD) pathology was described in approximately 30% of normal pressure hydrocephalus (NPH) cases, leading to the distinction between neurodegenerative and idiopathic forms of this disorder. Whether or not there is a specific MRI signature of NPH remains a matter of debate. The present study focuses on asymptomatic cases at risk for NPH as defined with automatic machine learning tools and combines automatic MRI assessment of cortical and white matter volumetry, risk of AD (AD-RAI), and brain age gap estimation (BrainAge). Our hypothesis was that brain aging and AD process-independent volumetric changes occur in asymptomatic NPH-positive cases. We explored the volumetric changes in normal aging-sensitive (entorhinal cortex and parahippocampal gyrus/PHG) and AD-signature areas (hippocampus), four control cortical areas (frontal, parietal, occipital, and temporal), and cerebral and cerebellar white matter in 30 asymptomatic cases at risk for NPH (NPH probability >30) compared to 30 NPH-negative cases (NPH probability <5) with preserved cognition. In univariate regression models, NPH positivity was associated with decreased volumes in the hippocampus, parahippocampal gyrus (PHG), and entorhinal cortex bilaterally. The strongest negative association was found in the left hippocampus that persisted when adjusting for AD-RAI and Brain Age values. A combined model including the three parameters explained 36.5% of the variance, left hippocampal volumes, and BrainAge values, which remained independent predictors of the NPH status. Bilateral PHG and entorhinal cortex volumes were negatively associated with NPH-positive status in univariate models but this relationship did not persist when adjusting for BrainAge, the latter remaining the only predictor of the NPH status. We also found a negative association between bilateral cerebral and cerebellar white matter volumes and NPH status that persisted after controlling for AD-RAI or Brain Age values, explaining between 50 and 65% of its variance. These observations support the idea that in cases at risk for NPH, as defined by support vector machine assessment of NPH-related MRI markers, brain aging-related and brain aging and AD-independent volumetric changes coexist. The latter concerns volume loss in restricted hippocampal and white matter areas that could be considered as the MRI signature of idiopathic forms of NPH.
format Online
Article
Text
id pubmed-10655029
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-106550292023-01-01 Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus Haller, Sven Montandon, Marie-Louise Rodriguez, Cristelle Herrmann, François R. Giannakopoulos, Panteleimon Front Aging Neurosci Aging Neuroscience The occurrence of significant Alzheimer’s disease (AD) pathology was described in approximately 30% of normal pressure hydrocephalus (NPH) cases, leading to the distinction between neurodegenerative and idiopathic forms of this disorder. Whether or not there is a specific MRI signature of NPH remains a matter of debate. The present study focuses on asymptomatic cases at risk for NPH as defined with automatic machine learning tools and combines automatic MRI assessment of cortical and white matter volumetry, risk of AD (AD-RAI), and brain age gap estimation (BrainAge). Our hypothesis was that brain aging and AD process-independent volumetric changes occur in asymptomatic NPH-positive cases. We explored the volumetric changes in normal aging-sensitive (entorhinal cortex and parahippocampal gyrus/PHG) and AD-signature areas (hippocampus), four control cortical areas (frontal, parietal, occipital, and temporal), and cerebral and cerebellar white matter in 30 asymptomatic cases at risk for NPH (NPH probability >30) compared to 30 NPH-negative cases (NPH probability <5) with preserved cognition. In univariate regression models, NPH positivity was associated with decreased volumes in the hippocampus, parahippocampal gyrus (PHG), and entorhinal cortex bilaterally. The strongest negative association was found in the left hippocampus that persisted when adjusting for AD-RAI and Brain Age values. A combined model including the three parameters explained 36.5% of the variance, left hippocampal volumes, and BrainAge values, which remained independent predictors of the NPH status. Bilateral PHG and entorhinal cortex volumes were negatively associated with NPH-positive status in univariate models but this relationship did not persist when adjusting for BrainAge, the latter remaining the only predictor of the NPH status. We also found a negative association between bilateral cerebral and cerebellar white matter volumes and NPH status that persisted after controlling for AD-RAI or Brain Age values, explaining between 50 and 65% of its variance. These observations support the idea that in cases at risk for NPH, as defined by support vector machine assessment of NPH-related MRI markers, brain aging-related and brain aging and AD-independent volumetric changes coexist. The latter concerns volume loss in restricted hippocampal and white matter areas that could be considered as the MRI signature of idiopathic forms of NPH. Frontiers Media S.A. 2023-11-03 /pmc/articles/PMC10655029/ /pubmed/38020768 http://dx.doi.org/10.3389/fnagi.2023.1242158 Text en Copyright © 2023 Haller, Montandon, Rodriguez, Herrmann and Giannakopoulos. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Aging Neuroscience
Haller, Sven
Montandon, Marie-Louise
Rodriguez, Cristelle
Herrmann, François R.
Giannakopoulos, Panteleimon
Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus
title Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus
title_full Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus
title_fullStr Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus
title_full_unstemmed Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus
title_short Automatic MRI volumetry in asymptomatic cases at risk for normal pressure hydrocephalus
title_sort automatic mri volumetry in asymptomatic cases at risk for normal pressure hydrocephalus
topic Aging Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10655029/
https://www.ncbi.nlm.nih.gov/pubmed/38020768
http://dx.doi.org/10.3389/fnagi.2023.1242158
work_keys_str_mv AT hallersven automaticmrivolumetryinasymptomaticcasesatriskfornormalpressurehydrocephalus
AT montandonmarielouise automaticmrivolumetryinasymptomaticcasesatriskfornormalpressurehydrocephalus
AT rodriguezcristelle automaticmrivolumetryinasymptomaticcasesatriskfornormalpressurehydrocephalus
AT herrmannfrancoisr automaticmrivolumetryinasymptomaticcasesatriskfornormalpressurehydrocephalus
AT giannakopoulospanteleimon automaticmrivolumetryinasymptomaticcasesatriskfornormalpressurehydrocephalus