Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects

Background: Perivascular Spaces (PVS) become increasingly visible with advancing age on brain MRI, yet their relationship to morphological changes in the underlying microvessels remains poorly understood. Retinal and cerebral microvessels share morphological and physiological properties. We compared...

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Main Authors: Lucia Ballerini, Sarah McGrory, Maria del C. Valdés Hernández, Ruggiero Lovreglio, Enrico Pellegrini, Tom MacGillivray, Susana Muñoz Maniega, Ross Henderson, Adele Taylor, Mark E. Bastin, Fergus Doubal, Emanuele Trucco, Ian J. Deary, Joanna Wardlaw
Format: Article
Language:English
Published: Elsevier 2020-01-01
Series:Cerebral Circulation, Cognition and Behavior
Subjects:
MRI
Online Access:http://www.sciencedirect.com/science/article/pii/S2666245020300027
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language English
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author Lucia Ballerini
Sarah McGrory
Maria del C. Valdés Hernández
Ruggiero Lovreglio
Enrico Pellegrini
Tom MacGillivray
Susana Muñoz Maniega
Ross Henderson
Adele Taylor
Mark E. Bastin
Fergus Doubal
Emanuele Trucco
Ian J. Deary
Joanna Wardlaw
spellingShingle Lucia Ballerini
Sarah McGrory
Maria del C. Valdés Hernández
Ruggiero Lovreglio
Enrico Pellegrini
Tom MacGillivray
Susana Muñoz Maniega
Ross Henderson
Adele Taylor
Mark E. Bastin
Fergus Doubal
Emanuele Trucco
Ian J. Deary
Joanna Wardlaw
Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects
Cerebral Circulation, Cognition and Behavior
MRI
Ageing
Perivascular spaces
Retina
author_facet Lucia Ballerini
Sarah McGrory
Maria del C. Valdés Hernández
Ruggiero Lovreglio
Enrico Pellegrini
Tom MacGillivray
Susana Muñoz Maniega
Ross Henderson
Adele Taylor
Mark E. Bastin
Fergus Doubal
Emanuele Trucco
Ian J. Deary
Joanna Wardlaw
author_sort Lucia Ballerini
title Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects
title_short Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects
title_full Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects
title_fullStr Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects
title_full_unstemmed Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects
title_sort quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjects
publisher Elsevier
series Cerebral Circulation, Cognition and Behavior
issn 2666-2450
publishDate 2020-01-01
description Background: Perivascular Spaces (PVS) become increasingly visible with advancing age on brain MRI, yet their relationship to morphological changes in the underlying microvessels remains poorly understood. Retinal and cerebral microvessels share morphological and physiological properties. We compared computationally-derived PVS morphologies with retinal vessel morphologies in older people. Methods: We analysed data from community-dwelling individuals who underwent multimodal brain MRI and retinal fundus camera imaging at mean age 72.55 years (SD=0.71). We assessed centrum semiovale PVS computationally to determine PVS total volume and count, and mean per-subject individual PVS length, width and size. We analysed retinal images using the VAMPIRE software suite, obtaining the Central Retinal Artery and Vein Equivalents (CRVE and CRAE), Arteriole-to-Venule ratio (AVR), and fractal dimension (FD) of both eyes. We investigated associations using general linear models, adjusted for age, gender, and major vascular risk factors. Results: In 381 subjects with all measures, increasing total PVS volume and count were associated with decreased CRAE in the left eye (volume β=−0.170, count β=−0.184, p<0.001). No associations of PVS with CRVE were found. The PVS total volume, individual width and size increased with decreasing FD of the arterioles (a) and venules (v) of the left eye (total volume: FDa β=−0.137, FDv β=−0.139, p<0.01; width: FDa β=−0.144, FDv β=−0.158, p<0.01; size: FDa β=−0.157, FDv β=−0.162, p<0.01). Conclusions: Increase in PVS number and size visible on MRI reflect arteriolar narrowing and lower retinal arteriole and venule branching complexity, both markers of impaired microvascular health. Computationally-derived PVS metrics may be an early indicator of failing vascular health and should be tested in longitudinal studies.
topic MRI
Ageing
Perivascular spaces
Retina
url http://www.sciencedirect.com/science/article/pii/S2666245020300027
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spelling doaj-69e1ce205ed647c8850168a7eae0bfbf2021-07-08T04:04:30ZengElsevierCerebral Circulation, Cognition and Behavior2666-24502020-01-011100002Quantitative measurements of enlarged perivascular spaces in the brain are associated with retinal microvascular parameters in older community-dwelling subjectsLucia Ballerini0Sarah McGrory1Maria del C. Valdés Hernández2Ruggiero Lovreglio3Enrico Pellegrini4Tom MacGillivray5Susana Muñoz Maniega6Ross Henderson7Adele Taylor8Mark E. Bastin9Fergus Doubal10Emanuele Trucco11Ian J. Deary12Joanna Wardlaw13Department of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UK; Dementia Research Institute, University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UKDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UKDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UK; Dementia Research Institute, University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UKSchool of Built Environment, Massey University, Auckland, New ZealandDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UKDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UK; Dementia Research Institute, University of Edinburgh, Edinburgh, UKDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UK; Dementia Research Institute, University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UKCentre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UKDepartment of Psychology, University of Edinburgh, Edinburgh, UKDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UKDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UK; Dementia Research Institute, University of Edinburgh, Edinburgh, UKVAMPIRE Project, Computing (SSEN), University of Dundee, Dundee, UKCentre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK; Department of Psychology, University of Edinburgh, Edinburgh, UKDepartment of Neuroimaging Sciences, Centre for Clinical Brain Sciences, and VAMPIRE Project, University of Edinburgh, Edinburgh, EH16 4SB, UK; Dementia Research Institute, University of Edinburgh, Edinburgh, UK; Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK; Corresponding author at: Department of Neuroimaging Sciences, Centre for Clinical Brain Sciences, University of Edinburgh, 49 Little France Crescent, Chancellor's Building, Edinburgh EH16 4SB, UK.Background: Perivascular Spaces (PVS) become increasingly visible with advancing age on brain MRI, yet their relationship to morphological changes in the underlying microvessels remains poorly understood. Retinal and cerebral microvessels share morphological and physiological properties. We compared computationally-derived PVS morphologies with retinal vessel morphologies in older people. Methods: We analysed data from community-dwelling individuals who underwent multimodal brain MRI and retinal fundus camera imaging at mean age 72.55 years (SD=0.71). We assessed centrum semiovale PVS computationally to determine PVS total volume and count, and mean per-subject individual PVS length, width and size. We analysed retinal images using the VAMPIRE software suite, obtaining the Central Retinal Artery and Vein Equivalents (CRVE and CRAE), Arteriole-to-Venule ratio (AVR), and fractal dimension (FD) of both eyes. We investigated associations using general linear models, adjusted for age, gender, and major vascular risk factors. Results: In 381 subjects with all measures, increasing total PVS volume and count were associated with decreased CRAE in the left eye (volume β=−0.170, count β=−0.184, p<0.001). No associations of PVS with CRVE were found. The PVS total volume, individual width and size increased with decreasing FD of the arterioles (a) and venules (v) of the left eye (total volume: FDa β=−0.137, FDv β=−0.139, p<0.01; width: FDa β=−0.144, FDv β=−0.158, p<0.01; size: FDa β=−0.157, FDv β=−0.162, p<0.01). Conclusions: Increase in PVS number and size visible on MRI reflect arteriolar narrowing and lower retinal arteriole and venule branching complexity, both markers of impaired microvascular health. Computationally-derived PVS metrics may be an early indicator of failing vascular health and should be tested in longitudinal studies.http://www.sciencedirect.com/science/article/pii/S2666245020300027MRIAgeingPerivascular spacesRetina