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November 01, 2016; 87 (18) Article

Cortical superficial siderosis predicts early recurrent lobar hemorrhage

Duangnapa Roongpiboonsopit, Andreas Charidimou, Christopher M. William, Arne Lauer, Guido J. Falcone, Sergi Martinez-Ramirez, Alessandro Biffi, Alison Ayres, Anastasia Vashkevich, Oluwole O. Awosika, Jonathan Rosand, M. Edip Gurol, Scott B. Silverman, Steven M. Greenberg, Anand Viswanathan
First published September 30, 2016, DOI: https://doi.org/10.1212/WNL.0000000000003281
Duangnapa Roongpiboonsopit
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Andreas Charidimou
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Christopher M. William
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Arne Lauer
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Guido J. Falcone
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Sergi Martinez-Ramirez
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Alessandro Biffi
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Alison Ayres
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Anastasia Vashkevich
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Oluwole O. Awosika
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
MD
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Jonathan Rosand
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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M. Edip Gurol
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Scott B. Silverman
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Steven M. Greenberg
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Anand Viswanathan
From The Hemorrhagic Stroke Research Program, J. Philip Kistler Stroke Research Center (D.R., A.C., A.L., G.J.F., S.M.-R., A.A., A. Vashkevich, M.E.G., S.B.S., S.M.G., A. Viswanathan), and Division of Behavioral Neurology (A.B.), Department of Neurology, Division of Neuropsychiatry, Department of Psychiatry (A.B.), Neuropathology Service, Department of Pathology (C.M.W.), and The Center for Human Genetic Research (G.J.F., J.R.), Massachusetts General Hospital, Harvard Medical School, Boston; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and Human Cortical Physiology and Stroke Neurorehabilitation Section (O.O.A.), NINDS/NIH, Bethesda, MD.
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Full PDF
Citation
Cortical superficial siderosis predicts early recurrent lobar hemorrhage
Duangnapa Roongpiboonsopit, Andreas Charidimou, Christopher M. William, Arne Lauer, Guido J. Falcone, Sergi Martinez-Ramirez, Alessandro Biffi, Alison Ayres, Anastasia Vashkevich, Oluwole O. Awosika, Jonathan Rosand, M. Edip Gurol, Scott B. Silverman, Steven M. Greenberg, Anand Viswanathan
Neurology Nov 2016, 87 (18) 1863-1870; DOI: 10.1212/WNL.0000000000003281

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Abstract

Objective: To identify predictors of early lobar intracerebral hemorrhage (ICH) recurrence, defined as a new ICH within 6 months of the index event, in patients with cerebral amyloid angiopathy (CAA).

Methods: Participants were consecutive survivors (age ≥55 years) of spontaneous symptomatic probable or possible CAA-related lobar ICH according to the Boston criteria, drawn from an ongoing single-center cohort study. Neuroimaging markers ascertained in CT or MRI included focal (≤3 sulci) or disseminated (>3 sulci) cortical superficial siderosis (cSS), acute convexity subarachnoid hemorrhage (cSAH), cerebral microbleeds, white matter hyperintensities burden and location, and baseline ICH volume. Participants were followed prospectively for recurrent symptomatic ICH. Cox proportional hazards models were used to identify predictors of early recurrent ICH adjusting for potential confounders.

Results: A total of 292 patients were enrolled. Twenty-one patients (7%) had early recurrent ICH. Of these, 24% had disseminated cSS on MRI and 19% had cSAH on CT scan. In univariable analysis, the presence of disseminated cSS, cSAH, and history of previous ICH were predictors of early recurrent ICH (p < 0.05 for all comparisons). After adjusting for age and history of previous ICH, disseminated cSS on MRI and cSAH on CT were independent predictors of early recurrent ICH (hazard ratio [HR] 3.92, 95% confidence interval [CI] 1.38–11.17, p = 0.011, and HR 3.48, 95% CI 1.13–10.73, p = 0.030, respectively).

Conclusions: Disseminated cSS on MRI and cSAH on CT are independent imaging markers of increased risk for early recurrent ICH. These markers may provide additional insights into the mechanisms of ICH recurrence in patients with CAA.

GLOSSARY

BP=
blood pressure;
CAA=
cerebral amyloid angiopathy;
CMB=
cerebral microbleed;
cSS=
cortical superficial siderosis;
CT-WMH=
CT-defined white matter hypodensity;
FLAIR=
fluid-attenuated inversion recovery;
HTN=
hypertension;
ICH=
intracerebral hemorrhage;
IQR=
interquartile range;
MGH=
Massachusetts General Hospital;
SWI=
susceptibility-weighted imaging;
T2*GRE=
T2*-weighted gradient-recalled echo;
VIF=
variance inflation factor

Footnotes

  • 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.

  • Supplemental data at Neurology.org

  • Editorial, page 1854

  • Received February 11, 2016.
  • Accepted in final form June 30, 2016.
  • © 2016 American Academy of Neurology
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