Enlarged perivascular space burden associations with arterial stiffness and cognition

Bown, Corey W.; Khan, Omair A.; Liu, Dandan; Remedios, Samuel W.; Pechman, Kimberly R.; Terry, James G.; Nair, Sangeeta; Davis, L. Taylor; Landman, Bennett A.; Gifford, Katherine A.; Hohman, Timothy J.; Carr, J. Jeffrey; Jefferson, Angela L.

doi:10.1016/j.neurobiolaging.2022.10.014

Cited by 14 publications

(12 citation statements)

References 48 publications

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“…Small vessel disease could be a driver for the enlargement of perivascular spaces. This has been referred to as the blood-brain-barrier (BBB) leakage hypothesis ( Fisher, 1979 ; Wardlaw et al, 2013b ; Brown et al, 2018 ; Bown et al, 2022b ). Vascular risk factors, such as hypertension, could lead to endothelial dysfunction potentially resulting in BBB leakage, rarefaction of adjacent white matter, pericyte loss, arteriolar thrombosis, microbleeds, and finally failure of ISF drainage.…”

Section: Resultsmentioning

confidence: 99%

The etiology and evolution of magnetic resonance imaging-visible perivascular spaces: Systematic review and meta-analysis

Okar

Shinohara

et al. 2023

Front. Neurosci.

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ObjectivesPerivascular spaces have been involved in neuroinflammatory and neurodegenerative diseases. Upon a certain size, these spaces can become visible on magnetic resonance imaging (MRI), referred to as enlarged perivascular spaces (EPVS) or MRI-visible perivascular spaces (MVPVS). However, the lack of systematic evidence on etiology and temporal dynamics of MVPVS hampers their diagnostic utility as MRI biomarker. Thus, the goal of this systematic review was to summarize potential etiologies and evolution of MVPVS.MethodsIn a comprehensive literature search, out of 1,488 unique publications, 140 records assessing etiopathogenesis and dynamics of MVPVS were eligible for a qualitative summary. 6 records were included in a meta-analysis to assess the association between MVPVS and brain atrophy.ResultsFour overarching and partly overlapping etiologies of MVPVS have been proposed: (1) Impairment of interstitial fluid circulation, (2) Spiral elongation of arteries, (3) Brain atrophy and/or perivascular myelin loss, and (4) Immune cell accumulation in the perivascular space. The meta-analysis in patients with neuroinflammatory diseases did not support an association between MVPVS and brain volume measures [R: −0.15 (95%-CI −0.40–0.11)]. Based on few and mostly small studies in tumefactive MVPVS and in vascular and neuroinflammatory diseases, temporal evolution of MVPVS is slow.ConclusionCollectively, this study provides high-grade evidence for MVPVS etiopathogenesis and temporal dynamics. Although several potential etiologies for MVPVS emergence have been proposed, they are only partially supported by data. Advanced MRI methods should be employed to further dissect etiopathogenesis and evolution of MVPVS. This can benefit their implementation as an imaging biomarker.Systematic review registrationhttps://www.crd.york.ac.uk/prospero/display_record.php?RecordID=346564, identifier CRD42022346564.

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Section: Resultsmentioning

confidence: 99%

The etiology and evolution of magnetic resonance imaging-visible perivascular spaces: Systematic review and meta-analysis

Okar

Shinohara

et al. 2023

Front. Neurosci.

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“…On SEM, centrum semiovale PVS burden mediated 5% of the associations between sleep parameters and brain changes. (Bown et al, 2023) Explore relationship between baseline PVS burden and neuropsychological performance (cross-sectional and longitudinal) and aortic stiffness. (Remedios et al, 2020) T1w, 3T…”

Section: Lbc1936 N = 540mentioning

confidence: 99%

“…Huntington's disease (Valdés Hernández et al, 2019;Li et al, 2023), CADASIL (Karvelas et al, 2023), TBI (Hicks et al, 2023), MCI (Seperhband et al, 2021;Bown et al, 2023;Kamagata et al, 2023), frontotemporal dementia (Moses et al, 2022), and AD (Kamagata et al, 2023). One study involving elderly patients aged 65-84 enrolled in the LADIS study (Pantoni et al, 2005), also reported a positive association between PVS burden and cognition.…”

Section: Application Studiesmentioning

confidence: 99%

A Systematic Review and Meta-Analysis of Automated Methods for Quantifying Enlarged Perivascular Spaces in the Brain

Waymont,

Valdés Hernández,

Bernal

et al. 2024

Preprint

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Research into magnetic resonance imaging (MRI)- visible perivascular spaces (PVS) has recently increased, as results from studies in different diseases and populations are cementing their association with sleep, disease phenotypes, and overall health indicators. With the establishment of worldwide consortia and the availability of large databases, computational methods that allow to automatically process all this wealth of information are becoming increasingly relevant. Several computational approaches have been proposed to assess PVS from MRI, and efforts have been made to summarise and appraise the most widely applied ones. We systematically reviewed and meta-analysed all publications available up to September 2023 describing the development, improvement, or application of computational PVS quantification methods from MRI. We analysed 67 approaches and 60 applications of their implementation, from 112 publications. The two most widely applied were the use of a morphological filter to enhance PVS-like structures, with Frangi being the choice preferred by most, and the use of a U-Net configuration with or without residual connections. Older adults or population studies comprising adults from 18 years old onwards were, overall, more frequent than studies using clinical samples. PVS were mainly assessed from T2-weighted MRI acquired in 1.5T and/or 3T scanners, although combinations using it with T1-weighted and FLAIR images were also abundant. Common associations researched included age, sex, hypertension, diabetes, white matter hyperintensities, sleep and cognition, with occupation-related, ethnicity, and genetic/hereditable traits being also explored. Despite promising improvements to overcome barriers such as noise and differentiation from other confounds, a need for joined efforts for a wider testing and increasing availability of the most promising methods is now paramount.

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“…For example, hypertension and arterial pulsatility affect BBB integrity, PVS enlargement, and fluid movement through PVS. Higher PVS burden was found to be associated with increased arterial stiffness, 94 which leads to less damping of the arterial blood flow pulse. Impaired damping of this pulse has been measured in the arteries penetrating the BG and relates to PVS in the BG 15 .…”

Section: Insight Into the Pathophysiologymentioning

confidence: 99%

Blood–Brain Barrier Disruption and Perivascular Spaces in Small Vessel Disease and Neurodegenerative Diseases: A Review on MRI Methods and Insights

Voorter,

van Dinther,

Jansen

et al. 2023

Magnetic Resonance Imaging

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Perivascular spaces (PVS) and blood–brain barrier (BBB) disruption are two key features of cerebral small vessel disease (cSVD) and neurodegenerative diseases that have been linked to cognitive impairment and are involved in the cerebral waste clearance system. Magnetic resonance imaging (MRI) offers the possibility to study these pathophysiological processes noninvasively in vivo. This educational review provides an overview of the MRI techniques used to assess PVS functionality and BBB disruption. MRI‐visible PVS can be scored on structural images by either (subjectively) counting or (automatically) delineating the PVS. We highlight emerging (diffusion) techniques to measure proxies of perivascular fluid and its movement, which may provide a more comprehensive understanding of the role of PVS in diseases. For the measurement of BBB disruption, we explain the most commonly used MRI technique, dynamic contrast‐enhanced (DCE) MRI, as well as a more recently developed technique based on arterial spin labeling (ASL). DCE MRI and ASL are thought to measure complementary characteristics of the BBB. Furthermore, we describe clinical studies that have utilized these MRI techniques in cSVD and neurodegenerative diseases, particularly Alzheimer's disease (AD). These studies demonstrate the role of PVS and BBB dysfunction in these diseases and provide insight into the large overlap, but also into the differences between cSVD and AD. Overall, MRI techniques may provide valuable insights into the pathophysiological mechanisms underlying these diseases and have the potential to be used as markers for disease progression and treatment response.Level of Evidence3Technical EfficacyStage 2

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Enlarged perivascular space burden associations with arterial stiffness and cognition

Cited by 14 publications

References 48 publications

The etiology and evolution of magnetic resonance imaging-visible perivascular spaces: Systematic review and meta-analysis

The etiology and evolution of magnetic resonance imaging-visible perivascular spaces: Systematic review and meta-analysis

A Systematic Review and Meta-Analysis of Automated Methods for Quantifying Enlarged Perivascular Spaces in the Brain

Blood–Brain Barrier Disruption and Perivascular Spaces in Small Vessel Disease and Neurodegenerative Diseases: A Review on MRI Methods and Insights

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