Skip to main content
AAN.com

Abstract

Objective:

To assess MRI-visible enlarged perivascular spaces (EPVS) burden and different topographical patterns (in the centrum semiovale [CSO] and basal ganglia [BG]) in 2 common microangiopathies: cerebral amyloid angiopathy (CAA) and hypertensive arteriopathy (HA).

Methods:

Consecutive patients with spontaneous intracerebral hemorrhage (ICH) from a prospective MRI cohort were included. Small vessel disease MRI markers, including cerebral microbleeds (CMBs), cortical superficial siderosis (cSS), and white matter hyperintensities (WMH), were rated. CSO-EPVS/BG-EPVS were assessed on a validated 4-point visual rating scale (0 = no EPVS, 1 = <10, 2 = 11–20, 3 = 21–40, and 4 = >40 EPVS). We tested associations of predefined high-degree (score >2) CSO-EPVS and BG-EPVS with other MRI markers in multivariable logistic regression. We subsequently evaluated associations with CSO-EPVS predominance (i.e., CSO-EPVS > BG-EPVS) and BG-EPVS predominance pattern (i.e., BG-EPVS > CSO-EPVS) in adjusted multinomial logistic regression (reference group, BG-EPVS = CSO-EPVS).

Results:

We included 315 patients with CAA-ICH and 137 with HA-ICH. High-degree CSO-EPVS prevalence was greater in CAA-related ICH vs HA-related ICH (43.8% vs 17.5%, p < 0.001). In multivariable logistic regression, high-degree CSO-EPVS was associated with lobar CMB (odds ratio [OR] 1.33, 95% confidence interval [CI] 1.10–1.61, p = 0.003) and cSS (OR 2.08, 95% CI 1.30–3.32, p = 0.002). Deep CMBs (OR 2.85, 95% CI 1.75–4.64, p < 0.0001) and higher WMH volume (OR 1.02, 95% CI 1.01–1.04, p = 0.010) were predictors of high-degree BG-EPVS. A CSO-EPVS–predominant pattern was more common in CAA-ICH than in HA-ICH (75.9% vs 39.4%, respectively, p < 0.0001). CSO-PVS predominance was associated with lobar CMB burden and cSS, while BG-EPVS predominance was associated with HA-ICH and WMH volumes.

Conclusions:

Different patterns of MRI-visible EPVS provide insights into the dominant underlying microangiopathy type in patients with spontaneous ICH.

Get full access to this article

View all available purchase options and get full access to this article.

REFERENCES

1.
Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010;9:689–701.
2.
Charidimou A, Pantoni L, Love S. The concept of sporadic cerebral small vessel disease: a road map on key definitions and current concepts. Int J Stroke 2016;11:6–18.
3.
Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry 2012;83:124–137.
4.
Viswanathan A, Greenberg SM. Cerebral amyloid angiopathy in the elderly. Ann Neurol 2011;70:871–880.
5.
Fisher CM. Pathological observations in hypertensive cerebral hemorrhage. J Neuropathol Exp Neurol 1971;30:536–550.
6.
Greenberg SM, Vernooij MW, Cordonnier C, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 2009;8:165–174.
7.
Charidimou A, Linn J, Vernooij MW, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain 2015;138:2126–2139.
8.
Smith EE, Nandigam KR, Chen YW, et al. MRI markers of small vessel disease in lobar and deep hemispheric intracerebral hemorrhage. Stroke 2010;41:1933–1938.
9.
Gurol ME, Viswanathan A, Gidicsin C, et al. Cerebral amyloid angiopathy burden associated with leukoaraiosis: a positron emission tomography/magnetic resonance imaging study. Ann Neurol 2013;73:529–536.
10.
Martinez-Ramirez S, Pontes-Neto OM, Dumas AP, et al. Topography of dilated perivascular spaces in subjects from a memory clinic cohort. Neurology 2013;80:1551–1556.
11.
Charidimou A, Meegahage R, Fox Z, et al. Enlarged perivascular spaces as a marker of underlying arteriopathy in intracerebral haemorrhage: a multicentre MRI cohort study. J Neurol Neurosurg Psychiatry 2013;84:624–629.
12.
Koo HW, Jo KI, Yeon JY, Kim JS, Hong SC. Clinical features of high-degree centrum semiovale-perivascular spaces in cerebral amyloid angiopathy. J Neurol Sci 2016;367:89–94.
13.
Charidimou A, Jaunmuktane Z, Baron JC, et al. White matter perivascular spaces: an MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology 2014;82:57–62.
14.
Wardlaw JM, Smith EE, Biessels GJ, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013;12:822–838.
15.
Auriel E, Gurol ME, Ayres A, et al. Characteristic distributions of intracerebral hemorrhage-associated diffusion-weighted lesions. Neurology 2012;79:2335–2341.
16.
O'Donnell HC, Rosand J, Knudsen KA, et al. Apolipoprotein E genotype and the risk of recurrent lobar intracerebral hemorrhage. N Engl J Med 2000;342:240–245.
17.
Charidimou A, Boulouis G, Haley K, et al. White matter hyperintensity patterns in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology 2016;86:505–511.
18.
Knudsen KA, Rosand J, Karluk D, Greenberg SM. Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 2001;56:537–539.
19.
Gurol ME, Irizarry MC, Smith EE, et al. Plasma beta-amyloid and white matter lesions in AD, MCI, and cerebral amyloid angiopathy. Neurology 2006;66:23–29.
20.
Biffi A, Halpin A, Towfighi A, et al. Aspirin and recurrent intracerebral hemorrhage in cerebral amyloid angiopathy. Neurology 2010;75:693–698.
21.
Linn J, Halpin A, Demaerel P, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 2010;74:1346–1350.
22.
Charidimou A, Jager RH, Fox Z, et al. Prevalence and mechanisms of cortical superficial siderosis in cerebral amyloid angiopathy. Neurology 2013;81:626–632.
23.
Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke 2010;41:450–454.
24.
Maclullich AM, Wardlaw JM, Ferguson KJ, Starr JM, Seckl JR, Deary IJ. Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry 2004;75:1519–1523.
25.
Heijer T, Skoog I, Oudkerk M, et al. Association between blood pressure levels over time and brain atrophy in the elderly. Neurobiol Aging 2003;24:307–313.
26.
Zhu YC, Tzourio C, Soumare A, Mazoyer B, Dufouil C, Chabriat H. Severity of dilated Virchow-Robin spaces is associated with age, blood pressure, and MRI markers of small vessel disease: a population-based study. Stroke 2010;41:2483–2490.
27.
von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007;370:1453–1457.
28.
Smith EE. Leukoaraiosis and stroke. Stroke 2010;41:S139–S143.
29.
Ozturk MH, Aydingoz U. Comparison of MR signal intensities of cerebral perivascular (Virchow-Robin) and subarachnoid spaces. J Comput Assist Tomogr 2002;26:902–904.
30.
Marin-Padilla M, Knopman DS. Developmental aspects of the intracerebral microvasculature and perivascular spaces: insights into brain response to late-life diseases. J Neuropathol Exp Neurol 2011;70:1060–1069.
31.
Carare RO, Bernardes-Silva M, Newman TA, et al. Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 2008;34:131–144.
32.
Arbel-Ornath M, Hudry E, Eikermann-Haerter K, et al. Interstitial fluid drainage is impaired in ischemic stroke and Alzheimer's disease mouse models. Acta Neuropathol 2013;126:353–364.
33.
Hawkes CA, Hartig W, Kacza J, et al. Perivascular drainage of solutes is impaired in the ageing mouse brain and in the presence of cerebral amyloid angiopathy. Acta Neuropathol 2011;121:431–443.
34.
Roher AE, Kuo YM, Esh C, et al. Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer's disease. Mol Med 2003;9:112–122.
35.
Rouhl RP, van Oostenbrugge RJ, Knottnerus IL, Staals JE, Lodder J. Virchow-Robin spaces relate to cerebral small vessel disease severity. J Neurol 2008;255:692–696.

Information & Authors

Information

Published In

Neurology®
Volume 88Number 12March 21, 2017
Pages: 1157-1164
PubMed: 28228568

Publication History

Received: September 20, 2016
Accepted: December 20, 2016
Published online: February 22, 2017
Published in print: March 21, 2017

Permissions

Request permissions for this article.

Disclosure

The authors report no disclosures relevant to the manuscript. Go to Neurology.org for full disclosures.

Study Funding

This study was supported by the following NIH grants: 5K23NS083711 (M.E.G.), R01 NS070834, and 2R01 AG26484 (S.M.G.). A Charidimou is supported by the Bodossaki Foundation postdoctoral research scheme.

Authors

Affiliations & Disclosures

Andreas Charidimou, MD, PhD, MSc (Clinical Neurology)
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
Bodossaki Faoundation, Greece
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Gregoire Boulouis, MD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
(1) William J. Fulbright 2014-2015 Scholarship (2) Monahan Foundation 2014-2015 Grant for Medical Research
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Marco Pasi, MD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Eitan Auriel, MD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Ellis S. van Etten, MD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Kellen Haley, BSc
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Alison Ayres, BA
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
National Institutes of Health
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Kristin M. Schwab, BA
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Sergi Martinez-Ramirez, MD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Joshua N. Goldstein, MD, PhD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
Bristol Myers Squibb, Prolong Pharmaceuticals
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
International Journal of Emergency Medicine, member of Editorial Board since 2009. International and Emergency Medicine, Editorial Board since 2015.
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
Massachusetts General Hospital
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
Boehringer Ingelheim, Pfizer, CSL Behring
Research Support, Government Entities:
1.
NINDS - research grants, participated in clinical trials.
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
Consultant - Pfizer
Jonathan Rosand, MD, MSc
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
Pfizer, DSMB
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Lancet Neurology, editorial board member Stroke, editorial board member
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NIH/NINDS
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Anand Viswanathan, MD, PhD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
Has served on a Data safety monitoring board for Roche Pharmaceuticals.
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
Dr. Viswanathan has served as consultant for Athena Diagnostics.
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
(1) NIA 2P50AG005134-268382, investigator; (2) 1K23AG028726-01A2, investigator (3) 1R01AG047975-01, investigator
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Steven M. Greenberg, MD, PhD
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
1) Hoffman-LaRoche, MRI Review Committee 2) Biogen, Data Monitoring Committee 3) Washington University/Quintiles, Data Safety Monitoring Board
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
1) Frontiers in Stroke, Associate Editor, 2010-present 2) Stroke, Editorial Board 2009-present, Section Editor 2014-present 3) Cerebrovascular Disease, Editorial Board, 2008-present 4) Neurology, Editorial Board, 2005-2016 5) J Alzheimer's Disease and Other Dementias, Editorial Board, 2005- present
Patents:
1.
NONE
Publishing Royalties:
1.
1) UpToDate, Cerebral Amyloid Angiopathy 2) MedLink, Cerebral Amyloid Angiopathy
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
1) NIH, CoPI, R01NS096730 2016-2021 2) NIH, PI, R01AG026484, 2005-2020 3) NIH, PI, R01NS070834, 2010-2015 4) NIH, PI, U10NS077360, 2011-2018
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
M. Edip Gurol, MD, MSc
From the Hemorrhagic Stroke Research Program (A.C., G.B., M.P., E.A., E.S.v.E., K.H., A.A., K.M.S., S.M.-R., A.V., S.M.G., M.E.G.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Université Paris-Descartes (G.B.), INSERM UMR 894, Department of Neuroradiology, Centre Hospitalier Sainte-Anne, Paris, France; and Division of Neurocritical Care and Emergency Neurology (J.N.G., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE

Notes

Correspondence to Dr. Charidimou: [email protected]
Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Author Contributions

A. Charidimou: project concept, data collection imaging analysis, data analysis, statistical analysis, write-up. G. Boulouis: data collection, imaging analysis, critical revisions. M. Pasi, E. Auriel, E.S. van Etten, and K. Haley: imaging analysis, critical revisions. A. Ayres, and K.M. Schwab: data collection and management. Sergi Martinez-Ramirez and Joshua N. Goldstein: critical revisions. J. Rosand and A. Viswanathan: data collection, critical revisions. S.M. Greenberg: funding, data collection, critical revisions. M.E. Gurol: project concept and design, data collection, data analysis, write-up, critical revisions.

Metrics & Citations

Metrics

Citations

Download Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Select your manager software from the list below and click Download.

Cited By
  1. MRI-visible enlarged perivascular spaces in basal ganglia rather than centrum semiovale was associated with aneurysmal subarachnoid hemorrhage, Frontiers in Neurology, 15, (2024).https://doi.org/10.3389/fneur.2024.1341499
    Crossref
  2. Risk factors for intracerebral hemorrhage in small-vessel disease and non-small-vessel disease etiologies—an observational proof-of-concept study, Frontiers in Neurology, 15, (2024).https://doi.org/10.3389/fneur.2024.1322442
    Crossref
  3. Regional Burden of Enlarged Perivascular Spaces and Cognition and Neuropsychiatric Symptoms in Drug-Naive Patients With Parkinson Disease, Neurology, 102, 12, (2024)./doi/10.1212/WNL.0000000000209483
    Abstract
  4. Left atrial appendage closure for patients with atrial fibrillation at high intracranial haemorrhagic risk, Stroke and Vascular Neurology, (svn-2024-003142), (2024).https://doi.org/10.1136/svn-2024-003142
    Crossref
  5. Cross‐sectional association of continuous glucose monitoring‐derived metrics with cerebral small vessel disease in older adults with type 2 diabetes, Diabetes, Obesity and Metabolism, (2024).https://doi.org/10.1111/dom.15659
    Crossref
  6. Cerebral tau pathology in cerebral amyloid angiopathy, Brain Communications, 6, 2, (2024).https://doi.org/10.1093/braincomms/fcae086
    Crossref
  7. Perivascular spaces and where to find them – MR imaging and evaluation methods, RöFo - Fortschritte auf dem Gebiet der Röntgenstrahlen und der bildgebenden Verfahren, (2024).https://doi.org/10.1055/a-2254-5651
    Crossref
  8. Cerebrovascular disease emerges with age and Alzheimer’s disease in adults with Down syndrome, Scientific Reports, 14, 1, (2024).https://doi.org/10.1038/s41598-024-61962-y
    Crossref
  9. Clinical features and associated factors of coexisting intracerebral hemorrhage in patients with cerebral small vessel disease: a cross-sectional study, Scientific Reports, 14, 1, (2024).https://doi.org/10.1038/s41598-024-55968-9
    Crossref
  10. Differences in lobar microbleed topography in cerebral amyloid angiopathy and hypertensive arteriopathy, Scientific Reports, 14, 1, (2024).https://doi.org/10.1038/s41598-024-54243-1
    Crossref
  11. See more
Loading...

View Options

Get Access

Login options

Check if you have access through your login credentials or your institution to get full access on this article.

Personal login Institutional Login
Purchase Options

Purchase this article to access the full text.

Purchase Access, $39 for 24hr of access

View options

Full Text

View Full Text

Full Text HTML

View Full Text HTML

Media

Figures

Other

Tables

Share

Share

Share article link

Share