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October 04, 2016; 87 (14) Article

Microbleeds on MRI are associated with microinfarcts on autopsy in cerebral amyloid angiopathy

Arne Lauer, Susanne J. van Veluw, Christopher M. William, Andreas Charidimou, Duangnapa Roongpiboonsopit, Anastasia Vashkevich, Alison Ayres, Sergi Martinez-Ramirez, Edip M. Gurol, Geert Jan Biessels, Matthew Frosch, Steven M. Greenberg, Anand Viswanathan
First published September 9, 2016, DOI: https://doi.org/10.1212/WNL.0000000000003184
Arne Lauer
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Susanne J. van Veluw
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Christopher M. William
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Andreas Charidimou
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Duangnapa Roongpiboonsopit
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Anastasia Vashkevich
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Alison Ayres
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Sergi Martinez-Ramirez
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Edip M. Gurol
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Geert Jan Biessels
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Matthew Frosch
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Steven M. Greenberg
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Anand Viswanathan
From the Hemorrhagic Stroke Research Program (A.L., S.J.v.V., A.C., D.R., A.V., A.A., S.M.-R., E.M.G., S.M.G., A.V.), Department of Neurology, Massachusetts General Hospital Stroke Research Center, Harvard Medical School, Boston; Department of Neurology (S.J.v.V., G.J.B.), Brain Center Rudolf Magnus, University Medical Center Utrecht, the Netherlands; Department of Pathology (C.M.W.), New York University Langone Medical Center, New York University School of Medicine; Department of Medicine (D.R.), Faculty of Medicine, Naresuan University, Phitsanulok, Thailand; and C.S. Kubik Laboratory for Neuropathology (M.F.), Massachusetts General Hospital, Harvard Medical School, Boston.
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Full PDF
Citation
Microbleeds on MRI are associated with microinfarcts on autopsy in cerebral amyloid angiopathy
Arne Lauer, Susanne J. van Veluw, Christopher M. William, Andreas Charidimou, Duangnapa Roongpiboonsopit, Anastasia Vashkevich, Alison Ayres, Sergi Martinez-Ramirez, Edip M. Gurol, Geert Jan Biessels, Matthew Frosch, Steven M. Greenberg, Anand Viswanathan
Neurology Oct 2016, 87 (14) 1488-1492; DOI: 10.1212/WNL.0000000000003184

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Abstract

Objectives: To identify in vivo MRI markers that might correlate with cerebral microinfarcts (CMIs) on autopsy in patients with cerebral amyloid angiopathy (CAA).

Methods: We included patients with neuropathologic evidence of CAA on autopsy and available antemortem brain MRI. Clinical characteristics and in vivo MRI markers of CAA-related small vessel disease were recorded, including white matter hyperintensities, cerebral microbleeds, cortical superficial siderosis, and centrum semiovale perivascular spaces. In addition, the presence of intracerebral hemorrhage on MRI was assessed. Evaluation of the presence and number of CMIs was performed in 9 standard histology sections.

Results: Of 49 analyzed patients with CAA, CMIs were present in 36.7%. The presence of ≥1 CMIs on autopsy was associated with higher numbers of microbleeds on antemortem MRI (median 8 [interquartile range 2.5–33.0] vs 1 [interquartile range 0–3], p = 0.003) and with the presence of intracerebral hemorrhage (44.4% vs 16.1%, p = 0.03). No associations between CMIs and other in vivo MRI markers of CAA were found. In a multivariable model adjusted for severe CAA pathology, higher numbers of microbleeds were independent predictors of the presence of CMIs on pathology.

Conclusions: CMIs are a common finding at autopsy in patients with CAA. The strong association between MRI-observed microbleeds and CMIs at autopsy may suggest a shared underlying pathophysiologic mechanism between these lesions.

GLOSSARY

Aβ=
β-amyloid;
CAA=
cerebral amyloid angiopathy;
CMI=
cerebral microinfarct;
CS-PVS=
centrum semiovale perivascular space;
cSS=
cortical superficial siderosis;
PVS=
perivascular space;
SVD=
small vessel disease;
WMH=
white matter hyperintensity

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.

  • Received March 24, 2016.
  • Accepted in final form June 20, 2016.
  • © 2016 American Academy of Neurology
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