Abstract
Cerebrovascular disease is the leading cause of epilepsy in adults, although post-stroke seizures reported frequency is variable and few studies used EEG in their identification. To describe and compare EEG and clinical epileptic manifestations frequency in patients with an anterior circulation ischaemic stroke. Prospective study of acute anterior circulation ischaemic stroke patients, consecutively admitted to a Stroke Unit over 24 months and followed-up for 1 year. All patients underwent standardized clinical and diagnostic assessment. Seizure occurrence was clinically evaluated during hospitalization and by a telephone interview at 6 months and a clinical appointment at 12 months after stroke. Video-EEG was performed in the first 72 h (1st EEG), daily after the 1st EEG for the first 7 days after the stroke, or later if neurological worsening, at discharge, and at 12 months. 151 patients were included (112 men) with a mean age of 67.4 (11.9) years. In the 1st year after stroke, 38 patients (25.2%) had an epileptic seizure. During hospitalization, 27 patients (17.9%) had epileptiform activity (interictal or ictal) in the EEG, 7 (25.9%) of them electrographic seizures. During the first week after stroke, 22 (14.6%) patients had a seizure and 4 (2.6%) non-convulsive status epilepticus criteria. Five (22.7%) acute symptomatic seizures were exclusively electrographic. At least one remote symptomatic seizure occurred in 23 (16%) patients. In the first 7 days after stroke, more than one-fifth of patients with seizures had exclusively electrographic seizures. Without a systematic neurophysiological evaluation the frequency of post-stroke seizures are clinically underestimated.
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References
Fisher RS, Acevedo C, Arzimanoglou A et al (2014) ILAE Official Report: a practical clinical definition of epilepsy. Epilepsia 55:475–482
Hesdorffer DC, Benn EKT, Cascino GD, Hauser WA (2009) Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia 50:1102–1108
Holtkamp M, Beghi E, Benninger F et al (2017) European Stroke Organisation guidelines for the management of post-stroke seizures and epilepsy. Eur Stroke J 2:103–115
Chung JM (2014) Seizures in the acute stroke setting. Neurol Res 36:403–406
Camilo O, Goldstein LB (2004) Seizures and epilepsy after ischemic stroke. Stroke 35:1769–1775
Pitkänen A, Roivainen R, Lukasiuk K (2015) Development of epilepsy after ischaemic stroke. Lancet Neurol 15:185–197
Claassen J, Mayer S, Kowalski RG et al (2004) Detection of electrographic seizures with continuous EEG monitoring in critically ill patients. Neurology 62:1743–1748
Huang CW, Saposnik G, Fang J et al (2014) Influence of seizures on stroke outcomes: a large multicenter study. Neurology 82:768–776
Young GB, Jordan KG, Doig GS (1996) An assessment of nonconvulsive seizures in the intensive care unit using continuous EEG monitoring: an investigation of variables associated with mortality. Neurology 47:83–89
Oddo M, Carrera E, Claassen J et al (2009) Continuous electroencephalography in the medical intensive care unit. Crit Care Med 37:2051–2056
Kamel H, Betjemann JP, Navi BB et al (2013) Diagnostic yield of electroencephalography in the medical and surgical intensive care unit. Neurocrit Care 19:336–341
Goldstein L, Bertels C, Davis J (1989) Interrater reliability of the NIH stroke scale. Arch Neurol 46:660–662
Banks JL, Marotta CA (2007) Outcomes validity and reliability of the modified rankin scale: implications for stroke clinical trials—a literature review and synthesis. Stroke 38:1091–1096
Rankin J (1957) Cerebral vascular accidents in patients over the age of 60: II. Prognosis. Scottish Med J 2:200–215
van Swieten JC, Koudstaal PJ, Visser MC et al (1988) Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19:604–607
Adams H, Bendixen B, Kappelle L et al (1993) Classification of subtype of acute ischemic stroke. Stroke 23:35–41
Ottman R, Barker-Cummings C, Leibson CL et al (2010) Validation of a brief screening instrument for the ascertainment of epilepsy. Epilepsia 51:191–197
Nuwer M, Comi G, Emerson R et al (1998) IFCN standards for digital recording of clinical EEG. International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol 106:259–261
Flink R, Pedersen B, Guekht B et al (2002) Guidelines for the use of EEG methodology in the diagnosis of epilepsy. International League Against Epilepsy: commission report. Commission on European Affairs: subcommission on European Guidelines. Acta Neurol Scand 106:1–7
American Clinical Neurophysiology Society (2006) Guideline 4: standards of Practice in Electroencephalography. http://www.acns.org/pdf/guidelines/Guideline-4.pdf. Accessed 05 Aug 2017
American Clinical Neurophysiology Society (2006) Guideline 5: guidelines for standard electrode position nomenclature. Clin Neurophysiol 6:1–3
Martins da Silva A, Bentes C, Atalaia A, Mendes-Ribeiro JA (2011) Recomendações para utilização do electroencefalograma (EEG) em Epilepsia: Relatório à Liga Portuguesa Contra a Epilepsia. http://static.lvengine.net/epilepsia/Imgs/pages/page_105/comisso-de-eeg_lpce_v1.pdf. Accessed 05 Aug 2017
Alberta Health Services (2016) University of calgary medicine faculty training for aspects. http://www.aspectsinstroke.com/training-for-aspect. Accessed 10 Apr 2016
Barber P, Demchuk A, Zhang J, Buchan A (2000) Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS Study Group. Alberta Stroke Programme Early CT Score. Lancet 355:1670–1674
Anon (2002) The SITS Monitoring Study (SITS-MOST) Final protocol. http://www.acutestroke.org/SM_Protocol/SITS-MOST_final_protocol.pdf. Accessed 05 Aug 2017
Ryglewicz D, Baranska-Gieruszczak M, Niedzielska K, Kryst-Widzgowska T (2013) EEG and CT findings in poststroke epilepsy. Acta Neurol Scand 81:488–490
Awada A, Omojola MF, Obeid T (1999) Late epileptic seizures after cerebral infarction. Acta Neurol Scand 99:265–268
Pohlmann-Eden B, Fatar M, Hennerici M (2001) The preserved cortical island sign is highly predictive of postischemic seizures. Cerebrovasc Dis 12:282
Hirsch LJ, LaRoche SM, Gaspard N et al (2013) American Clinical Neurophysiology Society’s Standardized Critical Care EEG Terminology: 2012 version. J Clin Neurophysiol 30:1–27
Beniczky S, Hirsch LJ, Kaplan PW et al (2013) Unified EEG terminology and criteria for nonconvulsive status epilepticus. Epilepsia 54:28–29
Beghi E, Carpio A, Forsgren L et al (2010) Recommendation for a definition of acute symptomatic seizure. Epilepsia 51:671–675
Hauser WA, Beghi E (2008) First seizure definitions and worldwide incidence and mortality. Epilepsia 49:8–12
Trinka E, Cock H, Hesdorffer D et al (2015) A definition and classification of status epilepticus—Report of the ILAE Task Force on Classification of Status Epilepticus. Epilepsia 56:1515–1523
Leitinger M, Beniczky S, Rohracher A et al (2015) Salzburg consensus criteria for non-convulsive status epilepticus—approach to clinical application. Epilepsy Behav 49:158–163
Noachtar S, Binnie C, Ebersole J et al (1999) A glossary of terms most commonly used by clinical electroencephalographers and proposal for the report form for the EEG findings. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 52:21–41
Bentes C, Martins H, Peralta AR et al (2017) Epileptic manifestations in stroke patients treated with intravenous alteplase. Eur J Neurol 24(6):755–761
Gaspard N, Hirsch LJ, LaRoche SM et al (2014) Interrater agreement for critical care EEG terminology. Epilepsia 55:1366–1373
Leitinger M, Trinka E, Gardella E et al (2016) Diagnostic accuracy of the Salzburg EEG criteria for non-convulsive status epilepticus: a retrospective study. Lancet Neurol 15:1054–1062
Carrera E, Michel P, Despland P et al (2006) Continuous assessment of electrical epileptic activity in acute stroke. Neurology 67:99–104
Chong D, Hirsch L (2005) Which EEG patterns warrant treatment in the critically ill? Reviewing the evidence for treatment of periodic epileptiform discharges and related patterns. J Clin Neurophysiol 22:79–91
Hartings JA, Williams AJ, Tortella FC (2003) Occurrence of nonconvulsive seizures, periodic epileptiform discharges, and intermittent rhythmic delta activity in rat focal ischemia. Exp Neurol 179:139–149
Vespa PM, O’Phelan K, Shah M et al (2003) Acute seizures after intracerebral hemorrhage: a factor in progressive midline shift and outcome. Neurology 60:1441–1446
Kurtz P, Gaspard N, Wahl AS et al (2014) Continuous electroencephalography in a surgical intensive care unit. Intensive Care Med 40:228–234
Pandian JD, Cascino GD, So EL et al (2004) Digital video-electroencephalographic monitoring in the neurological-neurosurgical intensive care unit. Arch Neurol 61:1090–1094
Swisher CB, Shah D, Sinha SR, Husain AM (2015) Baseline EEG pattern on continuous ICU EEG monitoring and incidence of seizures. J Clin Neurophysiol 32:147–151
Westover MB, Shafi MM, Bianchi MT et al (2015) The probability of seizures during EEG monitoring in critically ill adults. Clin Neurophysiol 126:463–471
Claassen J, Vespa P (2014) Electrophysiologic monitoring in acute brain injury. Neurocrit Care 21:129–147
Grillo E (2015) Concerns about utility and cost-effectiveness of continuous critical-care EEG. J Clin Neurophysiol 32:442–443
Meierkord H, Holtkamp M (2007) Non-convulsive status epilepticus in adults: clinical forms and treatment. Lancet Neurol 6:329–339
Velioglu SK, Ozmenoglu M, Boz C, Alioglu Z (2001) Status epilepticus after stroke. Stroke 32:1169–1172
Rumbach L, Sablot D, Berger E et al (2000) Status epilepticus in stroke: report on a hospital-based stroke cohort. Neurology 54:350–354
Knake S, Rochon J, Fleischer S et al (2006) Status epilepticus after stroke is associated with increased long-term case fatality. Epilepsia 47:2020–2026
Acknowledgements
We are obliged to EEG technicians Joana Pires, Lígia Ferreira e Rosa Santos. We are also grateful to all nurses and medical residents working in the Stroke Unit between 2011 and 2013 for their support to this Project.
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The 2012 Research Grant in Cerebrovascular Diseases (scientific promoter: Stroke Portuguese Society (SPAVC)/Sponsor: Tecnifar), supported this work.
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Dr. Bentes received the 2012 Research Grant in Cerebrovascular Diseases (Scientific Promoter: Sociedade Portuguesa do AVC/Sponsor: Tecnifar). Dr. Ferro reports personal fees from Boehringer Ingelheim, outside the submitted work. Other authors have nothing to disclose.
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This study has been approved by the Ethics Committee “Comissão de Ética para a Saúde” of the HSM-CHLN and has, therefore, been preformed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
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Bentes, C., Martins, H., Peralta, A.R. et al. Post-stroke seizures are clinically underestimated. J Neurol 264, 1978–1985 (2017). https://doi.org/10.1007/s00415-017-8586-9
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DOI: https://doi.org/10.1007/s00415-017-8586-9