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July 07, 2020; 95 (1) Article

White matter hyperintensity burden in acute stroke patients differs by ischemic stroke subtype

View ORCID ProfileAnne-Katrin Giese, View ORCID ProfileMarkus D. Schirmer, Adrian V. Dalca, Ramesh Sridharan, Kathleen L. Donahue, Marco Nardin, Robert Irie, Elissa C. McIntosh, Steven J.T. Mocking, Huichun Xu, John W. Cole, Eva Giralt-Steinhauer, Jordi Jimenez-Conde, Christina Jern, Dawn O. Kleindorfer, Robin Lemmens, View ORCID ProfileJohan Wasselius, Arne Lindgren, View ORCID ProfileTatjana Rundek, Ralph L. Sacco, Reinhold Schmidt, Pankaj Sharma, Agnieszka Slowik, View ORCID ProfileVincent Thijs, View ORCID ProfileBradford B. Worrall, Daniel Woo, Steven J. Kittner, Patrick F. McArdle, Braxton D. Mitchell, Jonathan Rosand, View ORCID ProfileJames F. Meschia, Ona Wu, Polina Golland, Natalia S. Rost; on behalf of the International Stroke Genetics Consortium and the MRI-GENIE Investigators
First published June 3, 2020, DOI: https://doi.org/10.1212/WNL.0000000000009728
Anne-Katrin Giese
From the Department of Neurology (A.-K.G., M.D.S., K.L.D., M.N., J.R., O.W., N.S.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Program in Medical and Population Genetics (A.K.-G, J.R.), Broad Institute of MIT and Harvard; Computer Science and Artificial Intelligence Lab (M.D.S., A.V.D., R. Sridharan, P.G.), Massachusetts Institute of Technology, Cambridge; Department of Population Health Sciences (M.D.S.), German Centre for Neurodegenerative Diseases, Bonn, Germany; Athinoula A. Martinos Center for Biomedical Imaging (A.V.D., R.I., E.C.M., S.J.T.M., J.R., O.W.), Department of Radiology, Massachusetts General Hospital, Charlestown; Division of Endocrinology, Diabetes and Nutrition (H.X., P.F.M., B.D.M.), Department of Medicine, University of Maryland School of Medicine; Department of Neurology (J.W.C., S.J.K.), University of Maryland School of Medicine and Veterans Affairs Maryland Health Care System, Baltimore; Department of Neurology (E.G.-S., J.J.-C.), Neurovascular Research Group, IMIM-Hospital del Mar (Institut Hospital del Mar d’Investigacions Mèdiques), Universitat Autonoma de Barcelona, Spain; Institute of Biomedicine (C.J.), Sahlgrenska Academy at University of Gothenburg, Sweden; Department of Neurology and Rehabilitation Medicine (D.O.K., D.W.), University of Cincinnati College of Medicine, OH; KU Leuven–University of Leuven (R.L.), Department of Neurosciences, Experimental Neurology; VIB (R.L.), Vesalius Research Center, Laboratory of Neurobiology, University Hospitals Leuven, Department of Neurology, Belgium; Department of Clinical Sciences Lund (J.W., A.L.), Neurology, Lund University; Department of Neurology and Rehabilitation Medicine (A.L.), Neurology, Skåne University Hospital, Lund, Sweden; Department of Neurology (T.R., R.L.S.), Miller School of Medicine, University of Miami, The Evelyn F. McKnight Brain Institute, FL; Department of Neurology (R. Schmidt), Clinical Division of Neurogeriatrics, Medical University Graz, Austria; Institute of Cardiovascular Research (P.S.), Royal Holloway University of London, Egham, UK; Ashford and St Peter's Hospital (P.S.), UK; Department of Neurology (A.S.), Jagiellonian University Medical College, Krakow, Poland; Stroke Division (V.T.), Florey Institute of Neuroscience and Mental Health, University of Melbourne Heidelberg; Department of Neurology (V.T.), Austin Health, Heidelberg, Victoria, Australia; Departments of Neurology and Public Health Sciences (B.B.W.), University of Virginia, Charlottesville; Center for Genomic Medicine (J.R.), Massachusetts General Hospital; Henry and Allison McCance Center for Brain Health (J.R.), Boston, MA; and Department of Neurology (J.F.M.), Mayo Clinic, Jacksonville, FL.
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Markus D. Schirmer
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Adrian V. Dalca
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Ramesh Sridharan
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Kathleen L. Donahue
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Marco Nardin
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Robert Irie
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Elissa C. McIntosh
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Steven J.T. Mocking
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Huichun Xu
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John W. Cole
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Eva Giralt-Steinhauer
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Jordi Jimenez-Conde
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Christina Jern
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Dawn O. Kleindorfer
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Robin Lemmens
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Johan Wasselius
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Arne Lindgren
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Tatjana Rundek
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Ralph L. Sacco
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Reinhold Schmidt
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Pankaj Sharma
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Agnieszka Slowik
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Vincent Thijs
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Bradford B. Worrall
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Daniel Woo
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Steven J. Kittner
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Patrick F. McArdle
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Braxton D. Mitchell
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Jonathan Rosand
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James F. Meschia
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Ona Wu
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Polina Golland
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Natalia S. Rost
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Citation
White matter hyperintensity burden in acute stroke patients differs by ischemic stroke subtype
Anne-Katrin Giese, Markus D. Schirmer, Adrian V. Dalca, Ramesh Sridharan, Kathleen L. Donahue, Marco Nardin, Robert Irie, Elissa C. McIntosh, Steven J.T. Mocking, Huichun Xu, John W. Cole, Eva Giralt-Steinhauer, Jordi Jimenez-Conde, Christina Jern, Dawn O. Kleindorfer, Robin Lemmens, Johan Wasselius, Arne Lindgren, Tatjana Rundek, Ralph L. Sacco, Reinhold Schmidt, Pankaj Sharma, Agnieszka Slowik, Vincent Thijs, Bradford B. Worrall, Daniel Woo, Steven J. Kittner, Patrick F. McArdle, Braxton D. Mitchell, Jonathan Rosand, James F. Meschia, Ona Wu, Polina Golland, Natalia S. Rost
Neurology Jul 2020, 95 (1) e79-e88; DOI: 10.1212/WNL.0000000000009728

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Abstract

Objective To examine etiologic stroke subtypes and vascular risk factor profiles and their association with white matter hyperintensity (WMH) burden in patients hospitalized for acute ischemic stroke (AIS).

Methods For the MRI Genetics Interface Exploration (MRI-GENIE) study, we systematically assembled brain imaging and phenotypic data for 3,301 patients with AIS. All cases underwent standardized web tool–based stroke subtyping with the Causative Classification of Ischemic Stroke (CCS). WMH volume (WMHv) was measured on T2 brain MRI scans of 2,529 patients with a fully automated deep-learning trained algorithm. Univariable and multivariable linear mixed-effects modeling was carried out to investigate the relationship of vascular risk factors with WMHv and CCS subtypes.

Results Patients with AIS with large artery atherosclerosis, major cardioembolic stroke, small artery occlusion (SAO), other, and undetermined causes of AIS differed significantly in their vascular risk factor profile (all p < 0.001). Median WMHv in all patients with AIS was 5.86 cm3 (interquartile range 2.18–14.61 cm3) and differed significantly across CCS subtypes (p < 0.0001). In multivariable analysis, age, hypertension, prior stroke, smoking (all p < 0.001), and diabetes mellitus (p = 0.041) were independent predictors of WMHv. When adjusted for confounders, patients with SAO had significantly higher WMHv compared to those with all other stroke subtypes (p < 0.001).

Conclusion In this international multicenter, hospital-based cohort of patients with AIS, we demonstrate that vascular risk factor profiles and extent of WMH burden differ by CCS subtype, with the highest lesion burden detected in patients with SAO. These findings further support the small vessel hypothesis of WMH lesions detected on brain MRI of patients with ischemic stroke.

Glossary

AIS=
acute ischemic stroke;
CAD=
coronary artery disease;
CCS=
Causative Classification of Ischemic Stroke;
CE major=
major cardioembolic stroke;
CI=
confidence interval;
FLAIR=
fluid-attenuated inversion recovery;
IQR=
interquartile range;
LAA=
large artery atherosclerosis;
MRI-GENIE=
MRI-Genetics Interface Exploration;
QC=
quality control;
SAO=
small artery occlusion;
SiGN=
Stroke Genetics Network;
TOAST=
Trial of Org 10172 in Acute Stroke Treatment;
WMH=
white matter hyperintensity;
WMHv=
WMH volume

Footnotes

  • Coinvestigators are listed at links.lww.com/WNL/B100.

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Received April 5, 2019.
  • Accepted in final form December 12, 2019.
  • © 2020 American Academy of Neurology
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