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December 03, 2019; 93 (23) Article

A tool to identify patients with embolic stroke of undetermined source at high recurrence risk

View ORCID ProfileGeorge Ntaios, Georgios Georgiopoulos, Kalliopi Perlepe, Gaia Sirimarco, Davide Strambo, Ashraf Eskandari, View ORCID ProfileStefania Nannoni, Anastasia Vemmou, Eleni Koroboki, Efstathios Manios, Ana Rodríguez-Campello, Elisa Cuadrado-Godia, View ORCID ProfileJaume Roquer, Valentina Arnao, Valeria Caso, Maurizio Paciaroni, Exuperio Diez-Tejedor, Blanca Fuentes, Jorge Rodríguez Pardo, Sara Sánchez-Velasco, Antonio Arauz, Sebastian F. Ameriso, Lucía Pertierra, Maia Gómez-Schneider, Maximiliano A. Hawkes, Miguel A. Barboza, Beatriz Chavarria Cano, Ana Maria Iglesias Mohedano, Andrés García Pastor, Antonio Gil-Núñez, Jukka Putaala, Turgut Tatlisumak, Efstathia Karagkiozi, Vasileios Papavasileiou, Konstantinos Makaritsis, Fabio Bandini, Konstantinos Vemmos, Patrik Michel
First published October 29, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008571
George Ntaios
From the Department of Internal Medicine (G.N., K.P., E. Karagkiozi, V.P., K.M.), Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa, Greece; Department of Clinical Therapeutics (G.G., A.V., E. Koroboki, E.M., K.V.), Medical School of Athens, Alexandra Hospital, Greece; Stroke Center and Neurology Service (G.S., D.S., A.E., S.N., P.M.), Department of Clinical Neurosciences, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Switzerland; Department of Neurology (E.K.), National and Kapodistrian University of Athens, Greece; Division of Brain Sciences (E.K.), Department of Stroke Medicine, Imperial College, London, UK; Stroke Unit (A.R.-C., E.C.-G., J.R.), Department of Neurology, Hospital del Mar, Neurovascular Research Group, IMIM-Hospital del Mar (Institut Hospital del Mar d'Investigacions Mèdiques), Universitat Autònoma de Barcelona, Spain; Stroke Unit (V.A., V.C., M.P.), University of Perugia, Italy; Department of Neurology and Stroke Center (E.D.-T., B.F., J.R.P., S.S.-V.), La Paz University Hospital–Autónoma University of Madrid, IdiPAZ Health Research Institute, Spain; Stroke Clinic (A.A.), Instituto Nacional de Neurología y Neurocirugía Manuel Velasco Suárez, Mexico City, Mexico; Department of Neurology (S.F.A., L.P., M.G.-S., M.A.H.), Institute for Neurological Research, FLENI, Buenos Aires, Argentina; Neurosciences Department (M.A.B.), Hospital Dr. Rafael A. Calderón Guardia, CCSS, University of Costa Rica; Vascular Neurology Section (B.C.C., A.M.I.M., A.G.P., A.G.-N.), Stroke Center, Hospital General Universitario Gregorio Marañón, IiSGM Health Research Institute, Universidad Complutense de Madrid, Spain; Department of Neurology (J.P., T.T.), Helsinki University Central Hospital and University of Helsinki, Finland; Department of Clinical Neurosciences (T.T.), Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg; Department of Neurology (T.T.), Sahlgrenska University Hospital, Gothenburg, Sweden; Stroke Service (V.P.), Department of Neurosciences, Leeds Teaching Hospitals NHS Trust and Medical School, University of Leeds, UK; and Department of Neurology (F.B.), S. Paolo Hospital, Savona, Italy.
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Georgios Georgiopoulos
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Kalliopi Perlepe
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Gaia Sirimarco
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Davide Strambo
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Ashraf Eskandari
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Stefania Nannoni
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Anastasia Vemmou
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Eleni Koroboki
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Efstathios Manios
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Ana Rodríguez-Campello
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Elisa Cuadrado-Godia
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Jaume Roquer
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Valentina Arnao
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Valeria Caso
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Maurizio Paciaroni
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Exuperio Diez-Tejedor
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Blanca Fuentes
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Jorge Rodríguez Pardo
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Sara Sánchez-Velasco
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Antonio Arauz
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Sebastian F. Ameriso
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Lucía Pertierra
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Maia Gómez-Schneider
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Maximiliano A. Hawkes
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Miguel A. Barboza
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Beatriz Chavarria Cano
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Ana Maria Iglesias Mohedano
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Andrés García Pastor
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Antonio Gil-Núñez
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Jukka Putaala
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Turgut Tatlisumak
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Efstathia Karagkiozi
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Vasileios Papavasileiou
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Konstantinos Makaritsis
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Fabio Bandini
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Konstantinos Vemmos
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Patrik Michel
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A tool to identify patients with embolic stroke of undetermined source at high recurrence risk
George Ntaios, Georgios Georgiopoulos, Kalliopi Perlepe, Gaia Sirimarco, Davide Strambo, Ashraf Eskandari, Stefania Nannoni, Anastasia Vemmou, Eleni Koroboki, Efstathios Manios, Ana Rodríguez-Campello, Elisa Cuadrado-Godia, Jaume Roquer, Valentina Arnao, Valeria Caso, Maurizio Paciaroni, Exuperio Diez-Tejedor, Blanca Fuentes, Jorge Rodríguez Pardo, Sara Sánchez-Velasco, Antonio Arauz, Sebastian F. Ameriso, Lucía Pertierra, Maia Gómez-Schneider, Maximiliano A. Hawkes, Miguel A. Barboza, Beatriz Chavarria Cano, Ana Maria Iglesias Mohedano, Andrés García Pastor, Antonio Gil-Núñez, Jukka Putaala, Turgut Tatlisumak, Efstathia Karagkiozi, Vasileios Papavasileiou, Konstantinos Makaritsis, Fabio Bandini, Konstantinos Vemmos, Patrik Michel
Neurology Dec 2019, 93 (23) e2094-e2104; DOI: 10.1212/WNL.0000000000008571

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Abstract

Objective A tool to stratify the risk of stroke recurrence in patients with embolic stroke of undetermined source (ESUS) could be useful in research and clinical practice. We aimed to determine whether a score can be developed and externally validated for the identification of patients with ESUS at high risk for stroke recurrence.

Methods We pooled the data of all consecutive patients with ESUS from 11 prospective stroke registries. We performed multivariable Cox regression analysis to identify predictors of stroke recurrence. Based on the coefficient of each covariate of the fitted multivariable model, we generated an integer-based point scoring system. We validated the score externally assessing its discrimination and calibration.

Results In 3 registries (884 patients) that were used as the derivation cohort, age, leukoaraiosis, and multiterritorial infarct were identified as independent predictors of stroke recurrence and were included in the final score, which assigns 1 point per every decade after 35 years of age, 2 points for leukoaraiosis, and 3 points for multiterritorial infarcts (acute or old nonlacunar). The rate of stroke recurrence was 2.1 per 100 patient-years (95% confidence interval [CI] 1.44–3.06) in patients with a score of 0–4 (low risk), 3.74 (95% CI 2.77–5.04) in patients with a score of 5–6 (intermediate risk), and 8.23 (95% CI 5.99–11.3) in patients with a score of 7–12 (high risk). Compared to low-risk patients, the risk of stroke recurrence was significantly higher in intermediate-risk (hazard ratio [HR] 1.78, 95% CI 1.1–2.88) and high-risk patients (HR 4.67, 95% CI 2.83–7.7). The score was well-calibrated in both derivation and external validation cohorts (8 registries, 820 patients) (Hosmer-Lemeshow test χ2: 12.1 [p = 0.357] and χ2: 21.7 [p = 0.753], respectively). The area under the curve of the score was 0.63 (95% CI 0.58–0.68) and 0.60 (95% CI 0.54–0.66), respectively.

Conclusions The proposed score can assist in the identification of patients with ESUS at high risk for stroke recurrence.

Glossary

AF=
atrial fibrillation;
AUC=
area under the receiver operating characteristic curve;
CI=
confidence interval;
ESUS=
embolic stroke of undetermined source;
HR=
hazard ratio;
IQR=
interquartile range;
VIF=
variance inflation factor

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.

  • Received February 6, 2019.
  • Accepted in final form June 11, 2019.
  • © 2019 American Academy of Neurology
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