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May 21, 2019; 92 (21) Article

MRI predicts intracranial hemorrhage in patients who receive long-term oral anticoagulation

View ORCID ProfileJoan Martí-Fàbregas, Santiago Medrano-Martorell, Elisa Merino, Luis Prats-Sánchez, Rebeca Marín, Raquel Delgado-Mederos, Alejandro Martínez-Domeño, Pol Camps-Renom, Elena Jiménez-Xarrié, Mariluisa Zedde, Manuel Gómez-Choco, Lidia Lara, Amèlia Boix, View ORCID ProfileAna Calleja, Ana María De Arce-Borda, Yolanda Bravo, Blanca Fuentes, María Hernández-Pérez, David Cánovas, Laura Llull, Beatriz Zandio, Marimar Freijo, Ignacio Casado-Naranjo, Jordi Sanahuja, Dolores Cocho, Jerzy Krupinski, Ana Rodríguez-Campello, Ernest Palomeras, Alicia De Felipe, Marta Serrano, Elena Zapata-Arriaza, Josep Zaragoza-Brunet, Inmaculada Díaz-Maroto, Jessica Fernández-Domínguez, Aida Lago, José Maestre, Manuel Rodríguez-Yáñez, Ignasi Gich, for the HERO study investigators
First published April 19, 2019, DOI: https://doi.org/10.1212/WNL.0000000000007532
Joan Martí-Fàbregas
From the Department of Neurology (J.M.-F., L.P.-S., R.M., R.D.-M., A.M.-D., P.C.-R., E.J.-X.) and Epidemiology (I.G.), Hospital de la Santa Creu i Sant Pau, Biomedical Research Institute, Barcelona; Departments of Radiology (S.M.-M.) and Neurology (A.R.-C.), Hospital del Mar-Parc de Salut Mar, Barcelona; Unitat RM IDI (E.M.) and Department of Neurosciences (M.H.-P.), Hospital Germans Trias i Pujol, Badalona; Department of Neurology (M.Z.), Arcispedale Santa Maria Nuova IRCCS, Reggio Emilia, Italy; Department of Neurology (M.G.-C.), Hospital de Sant Joan Despí Moises Broggi, Sant Joan Despí, Spain; Department of Neurology (L. Lara), Hospital de León; Department of Neurology (A.B.), Hospital Universitari Son Espases, Palma de Mallorca; Department of Neurology (A.C.), Hospital de Valladolid; Department of Neurology (A.M.D.A.-B.), Hospital de Donostia; Department of Neurology (Y.B.), Hospital de Burgos; Department of Neurology (B.F.), Hospital Universitario La Paz, Universidad Autónoma de Madrid, Instituto de Investigación IdiPaz, Madrid; Department of Neurology (D. Cánovas), Hospital Parc Taulí, Sabadell; Department of Neurology (L. Llull), Hospital Clínic, Barcelona; Department of Neurology (B.Z.), Hospital de Navarra, Pamplona; Department of Neurology (M.F.), Hospital de Basurto, Bilbao; Department of Neurology (I.C.-N.), Hospital San Pedro de Alcántara, Cáceres; Department of Neurology (J.S.), Hospital Arnau de Vilanova, Lleida; Department of Neurology (D. Cocho), Hospital de Granollers; Department of Neurology (J.K.), F.Ass. Mutua Terrassa; Department of Neurology (E.P.), Hospital de Mataró; Department of Neurology (A.D.F.), Hospital Ramón y Cajal, Madrid; Department of Neurology (M.S.), Hospital La Rioja, Logroño; Department of Neurology (E.Z.-A.), Hospital Virgen del Rocío, Sevilla; Department of Neurology (J.Z.-B.), Hospital Verge de la Cinta, Tortosa; Department of Neurology (I.D.-M.), Hospital de Albacete; Department of Neurology (J.F.-D.), Centro Médico Asturias, Oviedo; Department of Neurology (A.L.), Hospital La Fe, Valencia; Department of Neurology (J.M.), Hospital Virgen de las Nieves, Granada; and Department of Neurology (M.R.-Y.), Hospital Santiago de Compostela, Santiago de Compostela, Spain.
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Santiago Medrano-Martorell
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Citation
MRI predicts intracranial hemorrhage in patients who receive long-term oral anticoagulation
Joan Martí-Fàbregas, Santiago Medrano-Martorell, Elisa Merino, Luis Prats-Sánchez, Rebeca Marín, Raquel Delgado-Mederos, Alejandro Martínez-Domeño, Pol Camps-Renom, Elena Jiménez-Xarrié, Mariluisa Zedde, Manuel Gómez-Choco, Lidia Lara, Amèlia Boix, Ana Calleja, Ana María De Arce-Borda, Yolanda Bravo, Blanca Fuentes, María Hernández-Pérez, David Cánovas, Laura Llull, Beatriz Zandio, Marimar Freijo, Ignacio Casado-Naranjo, Jordi Sanahuja, Dolores Cocho, Jerzy Krupinski, Ana Rodríguez-Campello, Ernest Palomeras, Alicia De Felipe, Marta Serrano, Elena Zapata-Arriaza, Josep Zaragoza-Brunet, Inmaculada Díaz-Maroto, Jessica Fernández-Domínguez, Aida Lago, José Maestre, Manuel Rodríguez-Yáñez, Ignasi Gich, for the HERO study investigators
Neurology May 2019, 92 (21) e2432-e2443; DOI: 10.1212/WNL.0000000000007532

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This article has a correction. Please see:

  • MRI predicts intracranial hemorrhage in patients who receive long-term oral anticoagulation - September 03, 2019
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Abstract

Objective We tested the hypothesis that the risk of intracranial hemorrhage (ICH) in patients with cardioembolic ischemic stroke who are treated with oral anticoagulants (OAs) can be predicted by evaluating surrogate markers of hemorrhagic-prone cerebral angiopathies using a baseline MRI.

Methods Patients were participants in a multicenter and prospective observational study. They were older than 64 years, had a recent cardioembolic ischemic stroke, and were new users of OAs. They underwent a baseline MRI analysis to evaluate microbleeds, white matter hyperintensities, and cortical superficial siderosis. We collected demographic variables, clinical characteristics, risk scores, and therapeutic data. The primary endpoint was ICH that occurred during follow-up. We performed bivariate and multivariate Cox regression analyses.

Results We recruited 937 patients (aged 77.6 ± 6.5 years; 47.9% were men). Microbleeds were detected in 207 patients (22.5%), moderate/severe white matter hyperintensities in 419 (45.1%), and superficial siderosis in 28 patients (3%). After a mean follow-up of 23.1 ± 6.8 months, 18 patients (1.9%) experienced an ICH. In multivariable analysis, microbleeds (hazard ratio 2.7, 95% confidence interval [CI] 1.1–7, p = 0.034) and moderate/severe white matter hyperintensities (hazard ratio 5.7, 95% CI 1.6–20, p = 0.006) were associated with ICH (C index 0.76, 95% CI 0.66–0.85). Rate of ICH was highest in patients with both microbleed and moderate/severe WMH (3.76 per 100 patient-years, 95% CI 1.62–7.4).

Conclusion Patients taking OAs who have advanced cerebral small vessel disease, evidenced by microbleeds and moderate to severe white matter hyperintensities, had an increased risk of ICH. Our results should help to determine the risk of prescribing OA for a patient with cardioembolic stroke.

ClinicalTrials.gov identifier NCT02238470.

Glossary

AF=
atrial fibrillation;
CAA=
cerebral amyloid angiopathy;
CHA=
cerebral hypertensive angiopathy;
CHA2DS2-VASc=
congestive heart failure (or left ventricular systolic dysfunction), hypertension: blood pressure consistently above 140/90 mm Hg (or treated hypertension on medication), age ≥75 years, diabetes mellitus, prior stroke or TIA or thromboembolism, vascular disease (e.g., peripheral artery disease, myocardial infarction, aortic plaque), age 65–74 years, sex category (i.e., female sex);
CI=
confidence interval;
CROMIS-2=
Clinical Relevance of Microbleeds in Stroke–2;
cSS=
cortical superficial siderosis;
DOAC=
direct oral anticoagulant;
FLAIR=
fluid-attenuated inversion recovery;
GRE=
gradient-recalled echo;
HAS-BLED=
hypertension, abnormal renal and liver function, stroke, bleeding, labile INR, elderly, drugs or alcohol;
HERO=
Hemorrhage Predicted by Resonance in Patients Receiving Oral Anticoagulants;
HR=
hazard ratio;
ICH=
intracranial hemorrhage;
INR=
international normalized ratio;
MB=
microbleed;
OA=
oral anticoagulant;
SS=
superficial siderosis;
SWI=
susceptibility-weighted imaging;
VKA=
vitamin K antagonist;
WMH=
white matter hyperintensity;
WML=
white matter lesion

Footnotes

  • 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.

  • HERO coinvestigators are listed in appendix 2.

  • Editorial, page 981

  • Received August 25, 2018.
  • Accepted in final form January 24, 2019.
  • © 2019 American Academy of Neurology
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Letters: Rapid online correspondence

  • Author response: MRI predicts intracranial hemorrhage in patients who receive long-term oral anticoagulation
    • Joan Martí-Fàbregas, Neurologist, Hospital de la Santa Creu i Sant Pau
    • Luis Prats-Sánchez, Neurologist, Hospital de la Santa Creu i Sant Pau
    Submitted July 01, 2019
  • Reader response: MRI predicts intracranial hemorrhage in patients who receive long-term oral anticoagulation
    • George K. Vilanilam, Research Fellow, Mayo Clinic, Florida
    • Mohammed K. Badi, Research Fellow, Mayo Clinic, Florida
    • Neethu Gopal, Research Fellow, Mayo Clinic, Florida
    • Kaneez Zahra, Research Trainee, Mayo Clinic, Florida
    Submitted May 28, 2019
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