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February 16, 2021; 96 (7) Article

Long-Term Vascular Outcomes in Patients With Mixed Location Intracerebral Hemorrhage and Microbleeds

View ORCID ProfileHsin-Hsi Tsai, Szu-Ju Chen, Li-Kai Tsai, View ORCID ProfileMarco Pasi, Yen-Ling Lo, Ya-Fang Chen, Sung-Chun Tang, Jiann-Shing Jeng
First published December 22, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011378
Hsin-Hsi Tsai
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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  • ORCID record for Hsin-Hsi Tsai
Szu-Ju Chen
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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Li-Kai Tsai
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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Marco Pasi
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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Yen-Ling Lo
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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Ya-Fang Chen
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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Sung-Chun Tang
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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Jiann-Shing Jeng
From the Department of Neurology (H.-H.T., S.-J.C., Y.-L.L.), National Taiwan University Hospital Bei-Hu Branch; Departments of Neurology (H.-H.T., S.-J.C., L.-K.T., S.-C.T., J.-S.J.) and Medical Imaging (Y.-F.C.) and Graduate Institute of Clinical Medicine (H.-H.T.), National Taiwan University College of Medicine and Hospital, Taipei; and U1172-LilNCog-Lille Neuroscience & Cognition (M.P.), CHU Lille, Inserm, Univ Lille, France.
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Long-Term Vascular Outcomes in Patients With Mixed Location Intracerebral Hemorrhage and Microbleeds
Hsin-Hsi Tsai, Szu-Ju Chen, Li-Kai Tsai, Marco Pasi, Yen-Ling Lo, Ya-Fang Chen, Sung-Chun Tang, Jiann-Shing Jeng
Neurology Feb 2021, 96 (7) e995-e1004; DOI: 10.1212/WNL.0000000000011378

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Abstract

Objective To determine whether mixed location intracerebral hemorrhages/microbleeds (mixed ICH) is a risk factor for vascular unfavorable outcome compared to cerebral amyloid angiopathy–related ICH (CAA-ICH) or strictly deep hypertensive ICH/microbleeds (HTN-ICH).

Methods A total of 300 patients with spontaneous ICH were included. Clinical data, neuroimaging markers, and follow-up outcomes (recurrent ICH, ischemic stroke, and vascular death) were compared among mixed ICH (n = 148), CAA-ICH (n = 32), and HTN-ICH (n = 120). The association between follow-up events and neuroimaging markers was explored using multivariable Cox regression models.

Results Patients with mixed ICH were older (65.6 ± 12.1 years vs 58.1 ± 13.3 years, p < 0.001) than patients with HTN-ICH, but younger than patients with CAA-ICH (73.3 ± 13.8 years, p = 0.001). Compared to CAA-ICH, mixed ICH had similar incidence of vascular events (all p > 0.05). Compared to HTN-ICH, mixed ICH is associated with higher ICH recurrence (hazard ratio [HR] 3.0, 95% confidence interval [CI] 1.2–7.7), more ischemic stroke (HR 8.2, 95% CI 1.0–65.8), and vascular composite outcome (HR 3.5, 95% CI 1.5–8.2) after adjustment for age and sex. In patients with mixed ICH, the presence of cortical superficial siderosis (cSS) is associated the development of ICH recurrence (HR 4.8, 95% CI 1.0–23.2), ischemic stroke (HR 8.8, 95% CI 1.7–45.5), and vascular composite outcome (HR 6.2, 95% CI 1.9–20.2). The association between cSS and ischemic stroke (p = 0.01) or vascular composite outcome (p = 0.003) remained significant after further adjustment for other radiologic markers.

Conclusions Mixed ICH harbors higher risk of unfavorable vascular outcome than HTN-ICH. Presence of cSS in mixed ICH independently predicts vascular event, suggesting the contribution of detrimental effect due to coexisting CAA.

Glossary

BG=
basal ganglia;
CAA=
cerebral amyloid angiopathy;
CI=
confidence interval;
cSS=
cortical superficial siderosis;
CSO=
centrum semiovale;
CSVD=
cerebral small vessel disease;
EPVS=
enlarged perivascular spaces;
HR=
hazard ratio;
HTN-SVD=
hypertensive small vessel disease;
ICH=
intracerebral hemorrhage;
MB=
microbleed;
NTUH=
National Taiwan University Hospital;
SWI=
susceptibility-weighted imaging

Footnotes

  • Go to Neurology.org/Nhttps://n.neurology.org/lookup/doi/10.1212/WNL.0000000000011378 for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Received July 20, 2020.
  • Accepted in final form October 15, 2020.
  • © 2020 American Academy of Neurology
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