Computational quantification of brain perivascular space morphologies: Associations with vascular risk factors and white matter hyperintensities. A study in the Lothian Birth Cohort 1936.


Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2020
Historique:
received: 09 05 2019
revised: 29 11 2019
accepted: 08 12 2019
pubmed: 31 12 2019
medline: 15 12 2020
entrez: 31 12 2019
Statut: ppublish

Résumé

Perivascular Spaces (PVS), also known as Virchow-Robin spaces, seen on structural brain MRI, are important fluid drainage conduits and are associated with small vessel disease (SVD). Computational quantification of visible PVS may enable efficient analyses in large datasets and increase sensitivity to detect associations with brain disorders. We assessed the associations of computationally-derived PVS parameters with vascular factors and white matter hyperintensities (WMH), a marker of SVD. Community dwelling individuals (n = 700) from the Lothian Birth Cohort 1936 who had multimodal brain MRI at age 72.6 years (SD = 0.7). We assessed PVS computationally in the centrum semiovale and deep corona radiata on T2-weighted images. The computationally calculated measures were the total PVS volume and count per subject, and the mean individual PVS length, width and size, per subject. We assessed WMH by volume and visual Fazekas scores. We compared PVS visual rating to PVS computational metrics, and tested associations between each PVS measure and vascular risk factors (hypertension, diabetes, cholesterol), vascular history (cardiovascular disease and stroke), and WMH burden, using generalized linear models, which we compared using coefficients, confidence intervals and model fit. In 533 subjects, the computational PVS measures correlated positively with visual PVS ratings (PVS count r = 0.59; PVS volume r = 0.61; PVS mean length r = 0.55; PVS mean width r = 0.52; PVS mean size r = 0.47). PVS size and width were associated with hypertension (OR 1.22, 95% CI [1.03 to 1.46] and 1.20, 95% CI [1.01 to 1.43], respectively), and stroke (OR 1.34, 95% CI [1.08 to 1.65] and 1.36, 95% CI [1.08 to 1.71], respectively). We found no association between other PVS measures and diabetes, hypercholesterolemia or cardiovascular disease history. Computational PVS volume, length, width and size were more strongly associated with WMH (PVS mean size versus WMH Fazekas score β = 0.66, 95% CI [0.59 to 0.74] and versus WMH volume β = 0.43, 95% CI [0.38 to 0.48]) than computational PVS count (WMH Fazekas score β = 0.21, 95% CI [0.11 to 0.3]; WMH volume β = 0.14, 95% CI [0.09 to 0.19]) or visual score. Individual PVS size showed the strongest association with WMH. Computational measures reflecting individual PVS size, length and width were more strongly associated with WMH, stroke and hypertension than computational count or visual PVS score. Multidimensional computational PVS metrics may increase sensitivity to detect associations of PVS with risk exposures, brain lesions and neurological disease, provide greater anatomic detail and accelerate understanding of disorders of brain fluid and waste clearance.

Sections du résumé

BACKGROUND AND PURPOSE
Perivascular Spaces (PVS), also known as Virchow-Robin spaces, seen on structural brain MRI, are important fluid drainage conduits and are associated with small vessel disease (SVD). Computational quantification of visible PVS may enable efficient analyses in large datasets and increase sensitivity to detect associations with brain disorders. We assessed the associations of computationally-derived PVS parameters with vascular factors and white matter hyperintensities (WMH), a marker of SVD.
PARTICIPANTS
Community dwelling individuals (n = 700) from the Lothian Birth Cohort 1936 who had multimodal brain MRI at age 72.6 years (SD = 0.7).
METHODS
We assessed PVS computationally in the centrum semiovale and deep corona radiata on T2-weighted images. The computationally calculated measures were the total PVS volume and count per subject, and the mean individual PVS length, width and size, per subject. We assessed WMH by volume and visual Fazekas scores. We compared PVS visual rating to PVS computational metrics, and tested associations between each PVS measure and vascular risk factors (hypertension, diabetes, cholesterol), vascular history (cardiovascular disease and stroke), and WMH burden, using generalized linear models, which we compared using coefficients, confidence intervals and model fit.
RESULTS
In 533 subjects, the computational PVS measures correlated positively with visual PVS ratings (PVS count r = 0.59; PVS volume r = 0.61; PVS mean length r = 0.55; PVS mean width r = 0.52; PVS mean size r = 0.47). PVS size and width were associated with hypertension (OR 1.22, 95% CI [1.03 to 1.46] and 1.20, 95% CI [1.01 to 1.43], respectively), and stroke (OR 1.34, 95% CI [1.08 to 1.65] and 1.36, 95% CI [1.08 to 1.71], respectively). We found no association between other PVS measures and diabetes, hypercholesterolemia or cardiovascular disease history. Computational PVS volume, length, width and size were more strongly associated with WMH (PVS mean size versus WMH Fazekas score β = 0.66, 95% CI [0.59 to 0.74] and versus WMH volume β = 0.43, 95% CI [0.38 to 0.48]) than computational PVS count (WMH Fazekas score β = 0.21, 95% CI [0.11 to 0.3]; WMH volume β = 0.14, 95% CI [0.09 to 0.19]) or visual score. Individual PVS size showed the strongest association with WMH.
CONCLUSIONS
Computational measures reflecting individual PVS size, length and width were more strongly associated with WMH, stroke and hypertension than computational count or visual PVS score. Multidimensional computational PVS metrics may increase sensitivity to detect associations of PVS with risk exposures, brain lesions and neurological disease, provide greater anatomic detail and accelerate understanding of disorders of brain fluid and waste clearance.

Identifiants

pubmed: 31887717
pii: S2213-1582(19)30467-X
doi: 10.1016/j.nicl.2019.102120
pmc: PMC6939098
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

102120

Subventions

Organisme : Medical Research Council
ID : G1001245
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M013111/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/R024065/1
Pays : United Kingdom

Informations de copyright

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest None.

Auteurs

Lucia Ballerini (L)

Division of Neuroimaging Sciences, Centre for Clinical Brain Sciences and Edinburgh Imaging, University of Edinburgh, Edinburgh, UK; UK Dementia Research Institute at the University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK. Electronic address: lucia.ballerini@ed.ac.uk.

Tom Booth (T)

Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK; Department of Psychology, University of Edinburgh, Edinburgh, UK.

Maria Del C Valdés Hernández (MDC)

Division of Neuroimaging Sciences, Centre for Clinical Brain Sciences and Edinburgh Imaging, University of Edinburgh, Edinburgh, UK; UK Dementia Research Institute at the University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK; Row Fogo Centre for Research into Ageing and the Brain, University of Edinburgh, Edinburgh, UK.

Stewart Wiseman (S)

Division of Neuroimaging Sciences, Centre for Clinical Brain Sciences and Edinburgh Imaging, University of Edinburgh, Edinburgh, UK; UK Dementia Research Institute at the University of Edinburgh, Edinburgh, UK.

Ruggiero Lovreglio (R)

School of Built Environment, Massey University, Auckland, New Zealand.

Susana Muñoz Maniega (S)

Division of Neuroimaging Sciences, Centre for Clinical Brain Sciences and Edinburgh Imaging, University of Edinburgh, Edinburgh, UK; UK Dementia Research Institute at the University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK.

Zoe Morris (Z)

Division of Neuroimaging Sciences, Centre for Clinical Brain Sciences and Edinburgh Imaging, University of Edinburgh, Edinburgh, UK.

Alison Pattie (A)

Department of Psychology, University of Edinburgh, Edinburgh, UK.

Janie Corley (J)

Department of Psychology, University of Edinburgh, Edinburgh, UK.

Alan Gow (A)

Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK; Department of Psychology, Heriot-Watt University, Edinburgh, UK.

Mark E Bastin (ME)

Division of Neuroimaging Sciences, Centre for Clinical Brain Sciences and Edinburgh Imaging, University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK.

Ian J Deary (IJ)

Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK; Department of Psychology, University of Edinburgh, Edinburgh, UK.

Joanna Wardlaw (J)

Division of Neuroimaging Sciences, Centre for Clinical Brain Sciences and Edinburgh Imaging, University of Edinburgh, Edinburgh, UK; UK Dementia Research Institute at the University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK. Electronic address: joanna.wardlaw@ed.ac.uk.

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