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February 19, 2019; 92 (8) Article

Prognostic relevance of cortical superficial siderosis in cerebral amyloid angiopathy

Frank Arne Wollenweber, Christian Opherk, Marialuisa Zedde, Cihan Catak, Rainer Malik, Marco Duering, Marek Janusz Konieczny, Rosario Pascarella, Raquel Samões, Manuel Correia, Joan Martí-Fàbregas, Jennifer Linn, Martin Dichgans
First published January 23, 2019, DOI: https://doi.org/10.1212/WNL.0000000000006956
Frank Arne Wollenweber
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Christian Opherk
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Marialuisa Zedde
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Cihan Catak
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Rainer Malik
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Marco Duering
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Marek Janusz Konieczny
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Rosario Pascarella
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Raquel Samões
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Manuel Correia
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Joan Martí-Fàbregas
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Jennifer Linn
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Martin Dichgans
From the Institute for Stroke and Dementia Research (F.A.W., C.O., C.C., R.M., M. Duering, M.J.K., M. Dichgans), University Hospital, LMU Munich; Klinik für Neurologie (C.O.), SLK–Kliniken Heilbronn GmbH, Heilbronn, Germany; Stroke Unit–Neurology Unit and Neuroradiology Unit (M.Z., R.P.), Arcispedale Santa Maria Nuova, Azienda Unità Sanitaria Locale–IRCCS Reggio Emilia, Italy; Serviço de Neurologia (R.S., M.C.), Centro Hospitalar do Porto, Hospital de Santo António, Portugal; Hospital de la Santa Creu i Sant Pau (J.M.-F.), Biomedical Research Institute Sant Pau, IIB Sant Pau, Spain; Institut und Poliklinik für Neuroradiologie (J.L.), Universitätsklinikum Carl Gustav Carus, Dresden; Department of Neuroradiology (J.L.), Klinikum der Universität München, Ludwig-Maximilians-Universität LMU, Munich; Munich Cluster for Systems Neurology (SyNergy) (M. Dichgans); and German Center for Neurodegenerative Diseases (DZNE, Munich) (M. Dichgans), Germany.
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Prognostic relevance of cortical superficial siderosis in cerebral amyloid angiopathy
Frank Arne Wollenweber, Christian Opherk, Marialuisa Zedde, Cihan Catak, Rainer Malik, Marco Duering, Marek Janusz Konieczny, Rosario Pascarella, Raquel Samões, Manuel Correia, Joan Martí-Fàbregas, Jennifer Linn, Martin Dichgans
Neurology Feb 2019, 92 (8) e792-e801; DOI: 10.1212/WNL.0000000000006956

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Abstract

Objective To investigate the prognostic relevance of cortical superficial siderosis (cSS) in patients with cerebral amyloid angiopathy (CAA).

Methods A total of 302 patients fulfilling clinical and imaging criteria for probable or possible CAA were enrolled into a prospective, multicenter cohort study and followed for 12 months. cSS was assessed on T2*/susceptibility-weighted imaging MRI. The predefined primary composite endpoint was incident stroke or death in patients with cSS compared to those without. Secondary analyses included cerebrovascular events and functional outcome measured by the modified Rankin Scale (mRS). Multiple regression analysis was performed to adjust for possible confounders.

Results cSS prevalence was 40%. The primary endpoint occurred more frequently in patients with cSS (22%, 27/121) compared to those without (8%, 15/181, p = 0.001). Rates of CAA-related incident intracranial hemorrhage were 17% (cSS) and 4% (no cSS, p = 0.0003). The proportion of patients being functionally independent (mRS 0–2) 12 months from baseline were 59% (cSS) and 82% (no cSS, p = 0.00002). Presence of cSS was associated with the primary endpoint (adjusted odds ratio [OR] 1.2, 95% confidence interval [CI] 1.1–1.3, p = 0.0005), incident intracranial hemorrhage (adjusted OR 1.2, 95% CI 1.1–1.3, p = 0.0003), and less favorable outcome as assessed by the mRS (common OR 1.9, 95% CI 1.2–3.1, p = 0.009). Similar results were obtained in analyses restricted to patients with probable CAA and to patients with disseminated cSS (all p < 0.005).

Conclusions Patients with cSS and suspected CAA are at high risk for CAA-related incident intracranial hemorrhage and poor functional outcome. Both the presence and extent of cSS have prognostic relevance and may influence clinical decision-making.

Glossary

CAA=
cerebral amyloid angiopathy;
CI=
confidence interval;
CMB=
cerebral microbleeds;
cSS=
cortical superficial siderosis;
ICH=
intracerebral hemorrhage;
MMSE=
Mini-Mental State Examination;
mRS=
modified Rankin Scale;
OR=
odds ratio;
PVS=
perivascular spaces;
QC=
quality control;
SAH=
subarachnoid hemorrhage;
SVD=
small vessel disease;
SWI=
susceptibility-weighted imaging;
WMH=
white matter hyperintensities

Footnotes

  • ↵* These authors contributed equally to this work as first authors.

  • ↵† These authors contributed equally to this work as last authors.

  • 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.

  • Editorial, page 360

  • Received May 9, 2018.
  • Accepted in final form October 16, 2018.
  • © 2019 American Academy of Neurology
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