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The coexistence of PVS with other CSVD manifestations likely increases the risk of adverse neurological outcomes. We related PVS to other CSVD manifestations and brain volumes that are markers of vascular brain injury and neurodegeneration. Framingham Heart Study (FHS) participants with CSVD ratings on brain MRI were included. PVS were rated in the basal ganglia (BG) and centrum semiovale (CSO) into grades I\u2013IV and a category reflecting high burden in single or mixed CSO-BG regions. We related PVS to covert brain infarcts (CBI), white matter hyperintensities (WMH), cerebral microbleeds (CMB), total brain, hippocampal, and cortical gray matter volumes using adjusted multivariable regression analyses. In 2454 participants (mean age 54 \u00b1 12 years), we observed that higher PVS burden in both BG and CSO was related to CMB in lobar and deep brain regions and increased WMH. Greater CSO PVS burden was associated with decreased total cortical gray volumes. PVS are associated with ischemic markers of CSVD and neurodegeneration markers. Further studies should elucidate the causality between PVS and other CSVD manifestations.<\/jats:p>","DOI":"10.3390\/brainsci13091323","type":"journal-article","created":{"date-parts":[[2023,9,15]],"date-time":"2023-09-15T02:54:13Z","timestamp":1694746453000},"page":"1323","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Relation of MRI-Visible Perivascular Spaces and Other MRI Markers of Cerebral Small Vessel Disease"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2497-8965","authenticated-orcid":false,"given":"Frances","family":"Rodriguez Lara","sequence":"first","affiliation":[{"name":"Chobanian & Avedisian School of Medicine, Boston University, Boston, MA 02118, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arturo Ruben","family":"Toro","sequence":"additional","affiliation":[{"name":"Chobanian & Avedisian School of Medicine, Boston University, 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(2014). White Matter Disease as a Biomarker for Long-Term Cerebrovascular Disease and Dementia. Curr. Treat. Options Cardiovasc. Med., 16.","DOI":"10.1007\/s11936-013-0292-z"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1136\/jnnp.2003.030858","article-title":"Enlarged perivascular spaces are associated with cognitive function in healthy elderly men","volume":"75","author":"MacLullich","year":"2004","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Martinez-Ramirez, S., Greenberg, S.M., and Viswanathan, A. (2014). Cerebral microbleeds: Overview and implications in cognitive impairment. Alzheimer\u2019s Res. Ther., 6.","DOI":"10.1186\/alzrt263"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1148\/rg.274065722","article-title":"Virchow-Robin Spaces at MR Imaging","volume":"27","author":"Kwee","year":"2007","journal-title":"Radiographics"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1016\/j.jtbi.2005.07.005","article-title":"Mechanisms to explain the reverse perivascular transport of solutes out of the brain","volume":"238","author":"Schley","year":"2006","journal-title":"J. Theor. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1016\/S1474-4422(13)70124-8","article-title":"Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration","volume":"12","author":"Wardlaw","year":"2013","journal-title":"Lancet Neurol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1159\/000331466","article-title":"Cerebral Microbleeds: Histopathological Correlation of Neuroimaging","volume":"32","author":"Shoamanesh","year":"2011","journal-title":"Cerebrovasc. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"113","DOI":"10.3233\/JAD-201536","article-title":"Cerebral Amyloid Angiopathy Burden and Cerebral Microbleeds: Pathological Evidence for Distinct Phenotypes","volume":"81","author":"Lesnick","year":"2021","journal-title":"J. Alzheimer\u2019s Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1161\/STROKEAHA.119.027445","article-title":"Covert Brain Infarcts: Look at Extra and Intracranial Vessels","volume":"51","author":"Chabriat","year":"2020","journal-title":"Stroke"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1002\/sim.1743","article-title":"Managing and analysing data from a large-scale study on Framingham Offspring relating brain structure to cognitive function","volume":"23","author":"Massaro","year":"2004","journal-title":"Stat. Med."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Fletcher, E., DeCarli, C., Fan, A.P., and Knaack, A. (2021). Convolutional Neural Net Learning Can Achieve Production-Level Brain Segmentation in Structural Magnetic Resonance Imaging. Front. 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Instrumental validation of free water, peak-width of skeletonized mean diffusivity, and white matter hyperintensities: MarkVCID neuroimaging kits. Alzheimer\u2019s Dement., 14.","DOI":"10.1002\/dad2.12261"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Fletcher, E., Carmichael, O., and DeCarli, C. (September, January 28). MRI non-uniformity correction through interleaved bias estimation and B-spline deformation with a template. Proceedings of the 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, San Diego, CA, USA.","DOI":"10.1109\/EMBC.2012.6345882"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.jalz.2013.12.019","article-title":"Harmonized benchmark labels of the hippocampus on magnetic resonance: The EADC-ADNI project","volume":"11","author":"Bocchetta","year":"2014","journal-title":"Alzheimer\u2019s Dement."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Rueckert, D., Aljabar, P., Heckemann, R.A., Hajnal, J.V., and Hammers, A. (2006, January 1\u20136). Diffeomorphic Registration Using B-Splines. Proceedings of the Medical Image Computing and Computer-Assisted Intervention\u2014MICCAI 2006, Copenhagen, Denmark.","DOI":"10.1007\/11866763_86"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1016\/j.neuroimage.2006.01.021","article-title":"An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest","volume":"31","author":"Desikan","year":"2006","journal-title":"NeuroImage"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1016\/j.neuroimage.2009.02.018","article-title":"Multi-atlas based segmentation of brain images: Atlas selection and its effect on accuracy","volume":"46","author":"Aljabar","year":"2009","journal-title":"NeuroImage"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/j.neurobiolaging.2004.05.004","article-title":"Measures of brain morphology and infarction in the framingham heart study: Establishing what is normal","volume":"26","author":"DeCarli","year":"2005","journal-title":"Neurobiol. Aging"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1001\/archneur.63.2.246","article-title":"Association of White Matter Hyperintensity Volume With Decreased Cognitive Functioning: The Framingham Heart Study","volume":"63","author":"Au","year":"2006","journal-title":"Arch. Neurol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"6844","DOI":"10.18632\/aging.204181","article-title":"Aging, prevalence and risk factors of MRI-visible enlarged perivascular spaces","volume":"14","author":"Lara","year":"2022","journal-title":"Aging"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1159\/000375153","article-title":"Cerebral Perivascular Spaces Visible on Magnetic Resonance Imaging: Development of a Qualitative Rating Scale and its Observer Reliability","volume":"39","author":"Potter","year":"2015","journal-title":"Cerebrovasc. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/S1474-4422(09)70013-4","article-title":"Cerebral microbleeds: A guide to detection and interpretation","volume":"8","author":"Greenberg","year":"2009","journal-title":"Lancet Neurol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.neurobiolaging.2017.02.018","article-title":"Cerebral microbleeds and risk of incident dementia: The Framingham Heart Study","volume":"54","author":"Romero","year":"2017","journal-title":"Neurobiol. Aging"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1161\/01.STR.0000049766.26453.E9","article-title":"Visual Rating of Age-Related White Matter Changes on Magnetic Resonance Imaging: Scale comparison, interrater agreement, and correlations with quantitative measurements","volume":"34","author":"Kapeller","year":"2003","journal-title":"Stroke"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.1161\/STROKEAHA.116.013193","article-title":"Silent Brain Infarction in Patients With Asymptomatic Carotid Artery Atherosclerotic Disease","volume":"47","author":"Baradaran","year":"2016","journal-title":"Stroke"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1111\/1467-9868.00346","article-title":"A direct approach to false discovery rates","volume":"64","author":"Storey","year":"2002","journal-title":"J. R. Statist. Soc. Ser. B-Stat. Methodol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1212\/WNL.0b013e31828f1876","article-title":"Topography of dilated perivascular spaces in subjects from a memory clinic cohort","volume":"80","author":"Dumas","year":"2013","journal-title":"Neurology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2116","DOI":"10.1212\/WNL.0000000000001054","article-title":"Topography and associations of perivascular spaces in healthy adults: The Kashima Scan Study","volume":"83","author":"Yakushiji","year":"2014","journal-title":"Neurology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2483","DOI":"10.1161\/STROKEAHA.110.591586","article-title":"Severity of Dilated Virchow-Robin Spaces Is Associated With Age, Blood Pressure, and MRI Markers of Small Vessel Disease: A population-based study","volume":"41","author":"Zhu","year":"2010","journal-title":"Stroke"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1001\/jamaneurol.2017.1397","article-title":"Large Perivascular Spaces Visible on Magnetic Resonance Imaging, Cerebral Small Vessel Disease Progression, and Risk of Dementia: The Age, Gene\/Environment Susceptibility-Reykjavik Study","volume":"74","author":"Ding","year":"2017","journal-title":"JAMA Neurol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1161\/STROKEAHA.109.564914","article-title":"Enlarged Perivascular Spaces on MRI Are a Feature of Cerebral Small Vessel Disease","volume":"41","author":"Doubal","year":"2010","journal-title":"Stroke"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"871","DOI":"10.2147\/CIA.S204269","article-title":"The relationship between blood\u2013brain barrier permeability and enlarged perivascular spaces: A cross-sectional study","volume":"14","author":"Li","year":"2019","journal-title":"Clin. Interv. Aging"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2825","DOI":"10.1161\/STROKEAHA.120.029388","article-title":"Neuropathologic and Cognitive Correlates of Enlarged Perivascular Spaces in a Community-Based Cohort of Older Adults","volume":"51","author":"Schneider","year":"2020","journal-title":"Stroke"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1391","DOI":"10.1161\/01.STR.0000221308.94473.14","article-title":"White Matter Lesions in an Unselected Cohort of the Elderly: Molecular pathology suggests origin from chronic hypoperfusion injury","volume":"37","author":"Fernando","year":"2006","journal-title":"Stroke"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Kuriakose, M., Younger, D., Ravula, A.R., Alay, E., Rao, K.V.R., and Chandra, N. (2019). Synergistic Role of Oxidative Stress and Blood-Brain Barrier Permeability as Injury Mechanisms in the Acute Pathophysiology of Blast-induced Neurotrauma. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-44147-w"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3516","DOI":"10.1161\/STROKEAHA.113.002813","article-title":"Oxidative Stress Interferes With White Matter Renewal After Prolonged Cerebral Hypoperfusion in Mice","volume":"44","author":"Miyamoto","year":"2013","journal-title":"Stroke"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1177\/2396987318805905","article-title":"Small vessel disease and biomarkers of endothelial dysfunction after ischaemic stroke","volume":"4","author":"Arba","year":"2018","journal-title":"Eur. Stroke J."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1161\/STROKEAHA.113.004059","article-title":"Circulating Inflammatory Markers Are Associated With Magnetic Resonance Imaging-Visible Perivascular Spaces But Not Directly With White Matter Hyperintensities","volume":"45","author":"Aribisala","year":"2014","journal-title":"Stroke"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2904","DOI":"10.1523\/JNEUROSCI.3390-16.2017","article-title":"Cortical Spreading Depression Closes Paravascular Space and Impairs Glymphatic Flow: Implications for Migraine Headache","volume":"37","author":"Schain","year":"2017","journal-title":"J. Neurosci."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Vilor-Tejedor, N., Ciampa, I., Operto, G., Falc\u00f3n, C., Su\u00e1rez-Calvet, M., Crous-Bou, M., Shekari, M., Arenaza-Urquijo, E.M., Mil\u00e0-Alom\u00e0, M., and Grau-Rivera, O. (2021). Perivascular spaces are associated with tau pathophysiology and synaptic dysfunction in early Alzheimer\u2019s continuum. Alzheimer\u2019s Res. Ther., 13.","DOI":"10.1002\/alz.051799"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1136\/jnnp-2017-316724","article-title":"Prevalence of hippocampal enlarged perivascular spaces in a sample of patients with hypertension and their relation with vascular risk factors and cognitive function","volume":"89","author":"Garde","year":"2018","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1111\/ene.12979","article-title":"Assessment of enlarged perivascular spaces and their relation to target organ damage and mild cognitive impairment in patients with hypertension","volume":"23","author":"Mundet","year":"2016","journal-title":"Eur. J. Neurol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Bae, J., Kim, J., Park, K., and Han, S. (2021). Association between arterial stiffness and the presence of cerebral small vessel disease markers. Brain Behav., 11.","DOI":"10.1002\/brb3.1935"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Zhang, X., Ding, L., Yang, L., Qin, W., Yuan, J., Li, S., and Hu, W. (2016). Brain Atrophy Correlates with Severe Enlarged Perivascular Spaces in Basal Ganglia among Lacunar Stroke Patients. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0149593"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Liu, S., Hou, B., You, H., Zhang, Y., Zhu, Y., Ma, C., Zuo, Z., and Feng, F. (2021). The Association Between Perivascular Spaces and Cerebral Blood Flow, Brain Volume, and Cardiovascular Risk. Front. Aging Neurosci., 13.","DOI":"10.3389\/fnagi.2021.599724"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1177\/0271678X19888967","article-title":"Brain atrophy in cerebral small vessel diseases: Extent, consequences, technical limitations and perspectives: The HARNESS initiative","volume":"40","author":"Duering","year":"2020","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Jie, W., Lin, G., Liu, Z., Zhou, H., Lin, L., Liang, G., Ou, M., and Lin, M. (2020). The Relationship Between Enlarged Perivascular Spaces and Cognitive Function: A Meta-Analysis of Observational Studies. Front. Pharmacol., 11.","DOI":"10.3389\/fphar.2020.00715"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e1501","DOI":"10.1212\/WNL.0000000000011537","article-title":"Association of Dilated Perivascular Spaces With Cognitive Decline and Incident Dementia","volume":"96","author":"Paradise","year":"2021","journal-title":"Neurology"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e2561","DOI":"10.1212\/WNL.0000000000201293","article-title":"MRI-Visible Perivascular Spaces and Risk of Incident Dementia","volume":"99","author":"Romero","year":"2022","journal-title":"Neurology"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"K\u00f6vari, E., Charidimou, A., Herrmann, F.R., Giannakopoulos, P., Bouras, C., and Gold, G. (2015). No neuropathological evidence for a direct topographical relation between microbleeds and cerebral amyloid angiopathy: The Framingham Heart Study. Acta Neuropathol. Commun., 3.","DOI":"10.1186\/s40478-015-0228-9"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1002\/jmri.28369","article-title":"Automated Methods for Detecting and Quantitation of Enlarged Perivascular spaces on MRI","volume":"57","author":"Moses","year":"2023","journal-title":"J. Magn. Reson. Imaging"}],"container-title":["Brain Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3425\/13\/9\/1323\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:50:59Z","timestamp":1760129459000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3425\/13\/9\/1323"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,14]]},"references-count":54,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,9]]}},"alternative-id":["brainsci13091323"],"URL":"https:\/\/doi.org\/10.3390\/brainsci13091323","relation":{},"ISSN":["2076-3425"],"issn-type":[{"value":"2076-3425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,14]]}}}