Abstract
Background
Stroke had been accounted to cause almost 50% of epilepsy in the elderly and may lead to poor functional outcomes. Many studies examining the risk factors have been conducted despite showing inconsistent results and currently still difficult to predict the occurrence of post-stroke epilepsy. The study aimed to determine risk factors related to post-stroke epilepsy that influence clinical seizure, electroencephalography (EEG), and functional outcome of patients. Analytic retrospective case–control study was conducted with a total sampling of 62 samples of post-stroke epilepsy and 62 samples of control from all stroke patients in the Neurology Clinic from January 2019 to December 2021. Epilepsy was classified according to the criteria of the International League Against Epilepsy (ILAE) in 2017. The relevant demographic and clinical data were collected.
Result
The study involved 62 patients in the case group (average age of onset = 57.69; 42 men, 20 women; 51 ischemic stroke, 11 hemorrhagic stroke) and 62 patients in the control group (average age of onset = 56.90; 24 men, 38 women; 52 ischemic stroke, 10 hemorrhagic stroke). We found that 31 patients had focal-to-bilateral seizures, 26 patients had generalized seizures and 5 patients had focal seizures. Men (p = 0.001; OR 3.325) and NIHSS Score (p = 0.027; OR 5.094) had significant correlations with post-stroke epilepsy. Ischemic stroke had a significant correlation (p = 0.008) with seizure onset. Women also had a significant correlation (p = 0.012) with EEG abnormalities. The study found that 59 of 62 post-stroke epilepsy patients had poor functional outcomes (mRS > 2).
Conclusion
Our study confirmed that most patients had focal-to-bilateral seizure patterns that occurred in 1–2 years after stroke, and had poor functional outcomes. Men had 3.325 times more likely to develop post-stroke epilepsy than women. Also, NIHSS score ≥ 15 correlated and 5.094 times more likely to develop post-stroke epilepsy. Ischemic stroke had a peak of epilepsy onset at 1–2 years after stroke and women had significant showing abnormalities on EEG recording than men.
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Background
Stroke is still the second leading cause of death with annual mortality rate of about 5.5 million, and is also the first cause of disability (50%) worldwide. Generally, ischemic strokes account for about 80% of stroke cases while hemorrhagic stroke accounts for 20% of cases [1, 2]. Stroke had accounted to be the cause of epilepsy in the elderly while 30–50% of patients diagnosed with epilepsy after stroke [3, 38].
Our study has a few limitations. We reviewed the medical history of patients retrospectively. This small sample may have limited the derivation of adjusted Odd Ratios with multiple predictor variables. We did not include patients with acute symptomatic seizure during acute onset of stroke that may be a risk of further epilepsy, also did not evaluate functional outcome of epilepsy because of some limitation data. Further studies are needed with a prospective, larger sample, and multicentred study to determine more comprehensive epidemiological data, risk factors, EEG patterns, clinical epilepsy concerning seizure pattern, seizure control, anti-seizure medications, and also functional outcomes of post-stroke epilepsy patients. We also recommend further studies with distinguished samples between ischemic and hemorrhagic stroke to determine the characteristics in own type of stroke.
Conclusion
Our study confirmed that most patients had focal-to-bilateral seizure patterns that occurred 1–2 years after stroke, and had poor functional outcomes. Men had 3.325 times more likely to develop post-stroke epilepsy than women. Also, NIHSS score ≥ 15 correlated and 5.094 times more likely to develop post-stroke epilepsy. Ischemic stroke had a peak of epilepsy onset at 1–2 years after stroke and women had significant abnormalities showing on EEG recording than men.
Availability of data and materials
The dataset generated and/or analyzed during this current study is available in the figshare repository (https://doi.org/10.6084/m9.figshare.21342048.v2).
Abbreviations
- EEG:
-
Electroencephalography
- ILAE:
-
International League Against Epilepsy
- mRS:
-
Modified Rankin Scale
- NIHSS:
-
National Institute of Health Stroke Scale
- WHO:
-
World Health Organization
References
Donkor ES. Stroke in the 21st century: a snapshot of the burden, epidemiology, and quality of life. Stroke Res Treat. 2018. https://doi.org/10.1155/2018/3238165.
Krishnamurthi RV, Feigin VL, Forouzanfar MH, Mensah GA, Connor M, Bennett DA, et al. Global and regional burden of first-ever ischaemic and haemorrhagic stroke during 1990–2010: findings from the Global Burden of Disease Study 2010. Lancet Glob Health. 2013;1(5):e259–81.
Zhao Y, Li X, Zhang K, Tong T, Cui R. The progress of epilepsy after stroke. Curr Neuropharmacol. 2018;16(1):71–8.
Wang G, Jia H, Chen C, Lang S, Liu X, **a C, et al. Analysis of risk factors for first seizure after stroke in Chinese patients. Biomed Res Int. 2013. https://doi.org/10.1155/2013/702871.
Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55(4):475–82.
Hesdorffer DC, Benn EKT, Cascino GD, Hauser WA. Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia. 2009;50(5):1102–8.
Zelano J, Holtkamp M, Agarwal N, Lattanzi S, Trinka E, Brigo F. How to diagnose and treat post-stroke seizures and epilepsy. Epileptic Disord. 2020;22(3):252–63.
Tanaka T, Ihara M. Post-stroke epilepsy. Neurochem Int. 2017;107:219–28. https://doi.org/10.1016/j.neuint.2017.02.002.
Zelano J. Poststroke epilepsy: update and future directions. Ther Adv Neurol Disord. 2016;9(5):424–35.
Fisher RS, Cross JH, French JA, Higurashi N, Hirsch E, Jansen FE, et al. Operational classification of seizure types by the international league against epilepsy: position paper of the ILAE commission for classification and terminology. Epilepsia. 2017;58(4):522–30.
Luders HO, Noacthar S. Atlas and classification of electroencephalography. London: W.B. Saunders Company; 2000.
Organization WS. World Stroke Organization (WSO): global stroke fact sheet 2022. 2022;1–14. https://www.world-stroke.org/assets/downloads/WSO_Global_Stroke_Fact_Sheet.pdf.
Abbafati C, Abbas KM, Abbasi-Kangevari M, Abd-Allah F, Abdelalim A, Abdollahi M, et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020;396(10258):1204–22.
Zelano J. Prognosis of poststroke epilepsy. Epilepsy Behav. 2020;104:1–4. https://doi.org/10.1016/j.yebeh.2019.04.026.
Zou S, Chen Y. Research progress on the prediction of post-stroke epilepsy. Acta Epileptol. 2020;2(1):1–8.
Graham NSN, Crichton S, Koutroumanidis M, Wolfe CDA, Rudd AG. Incidence and associations of poststroke epilepsy the prospective South London stroke register. Stroke. 2013;44(3):605–11.
Misirli H, Özge A, Somay G, Erdoǧan N, Erkal H, Erenoǧlu NY. Seizure development after stroke. Int J Clin Pract. 2006;60(12):1536–41.
Szaflarski JP, Rackley AY, Kleindorfer DO, Khoury J, Woo D, Miller R, et al. Incidence of seizures in the acute phase of stroke: a population-based study. Epilepsia. 2008;49(6):974–81.
Conrad J, Pawlowski M, Dogan M, Kovac S, Ritter MA, Evers S. Seizures after cerebrovascular events: risk factors and clinical features. Seizure. 2013;22(4):275–82.
Dziadkowiak E, Guziński M, Chojdak-Łukasiewicz J, Wieczorek M, Paradowski B. Predictive factors in post-stroke epilepsy: retrospective analysis. Adv Clin Exp Med. 2021;30(1):29–34.
Bladin C, Alexandrov AV, Bellavance A, Bornstein N, Chambers B, Cote R, et al. Seizures after stroke. Arch Neurol. 2000;57:1617–22.
Lamy C, Domigo V, Semah F, Arquizan C, Trystram D, Coste J, et al. Early and late seizures after cryptogenic ischemic stroke in young adults. Neurology. 2003;60(3):400–4.
Beghi E. The epidemiology of epilepsy. Neuroepidemiology. 2020;54(2):185–91.
Reddy DS. The neuroendocrine basis of sex differences in epilepsy. Pharmacol Biochem Behav. 2017;152:97–104.
Kim DW, Lee SY, Chung SE, Cheong HK, Jung KY. Clinical characteristics of patients with treated epilepsy in Korea: a nationwide epidemiologic study. Epilepsia. 2014;55(1):67–75.
Benamer HTS, Grosset DG. A systematic review of the epidemiology of epilepsy in Arab countries. Epilepsia. 2009;50(10):2301–4.
Burneo JG, Tellez-Zenteno J, Wiebe S. Understanding the burden of epilepsy in Latin America: a systematic review of its prevalence and incidence. Epilepsy Res. 2005;66(1–3):63–74.
Casetta I, Pugliatti M, Faggioli R, Cesnik E, Simioni V, Bencivelli D, et al. Incidence of childhood and adolescence epilepsy: a community-based prospective study in the province of Ferrara and in Copparo, Italy, 1996–2005. Eur J Neurol. 2012;19(2):312–6.
Winkler AS, Kerschbaumsteiner K, Stelzhammer B, Meindl M, Kaaya J, Schmutzhard E. Prevalence, incidence, and clinical characteristics of epilepsy—a community-based door-to-door study in northern Tanzania. Epilepsia. 2009;50(10):2310–3.
Beghi E, D’Alessandro R, Beretta S, Consoli D, Crespi V, Delaj L, et al. Incidence and predictors of acute symptomatic seizures after stroke. Neurology. 2011;77(20):1785–93.
Badawy RA, Lai A, Vogrin SJ, Cook MJ. Subcortical epilepsy? Neurology. 2013;80:1901–7.
Norden AD, Blumenfeld H. The role of subcortical structures in human epilepsy. Epilepsy Behav. 2002;3(3):219–31.
Roivainen R, Haapaniemi E, Putaala J, Kaste M, Tatlisumak T. Young adult ischaemic stroke related acute symptomatic and late seizures: risk factors. Eur J Neurol. 2013;20(9):1247–55.
Bryndziar T, Sedova P, Kramer NM, Mandrekar J, Mikulik R, Brown RD, et al. Seizures following ischemic stroke: frequency of occurrence and impact on outcome in a long-term population-based study. J Stroke Cerebrovasc Dis. 2016;25(1):150–6.
De RJ, Claeys I, Martens S, Vanwalleghem P, Van Maele G, Phlypo R, et al. Computed tomographic changes of the brain and clinical outcome of patients with seizures and epilepsy after an ischaemic hemispheric stroke. Eur J Neurol. 2006;13(4):402–7.
Winter Y, Daneshkhah N, Galland N, Kotulla I, Krüger A, Groppa S. Health-related quality of life in patients with poststroke epilepsy. Epilepsy Behav. 2018;80:303–6.
Ingalhalikar M, Smith A, Parker D, Satterthwaite TD, Elliott MA, Ruparel K, et al. Sex differences in the structural connectome of the human brain. Proc Natl Acad Sci USA. 2014;111(2):823–8.
Pradeep HBAC, Meegama RGN. Age and gender related variations in human EEG signals. Int J Digit Signals Smart Syst. 2020;4(1/2/3):87.
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AKW designed the study, collected and analyzed the patient data, and arranged the manuscript. MH designed the study, analyzed the patient data, evaluated and substantively revised the manuscript. RD and NS analyzed the patient data, evaluated and substantively revised the manuscript. All authors read and approved the final manuscript.
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This study protocol has been reviewed and got ethical approval from the Health Research Ethic Commission of Dr. Saiful Anwar General Hospital Malang Indonesia with No. 400/128/K.3/102.7/2022. Informed consent was obtained from all individual participants included in the study.
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Waafi, A.K., Husna, M., Damayanti, R. et al. Clinical risk factors related to post-stroke epilepsy patients in Indonesia: a hospital-based study. Egypt J Neurol Psychiatry Neurosurg 59, 39 (2023). https://doi.org/10.1186/s41983-023-00637-3
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DOI: https://doi.org/10.1186/s41983-023-00637-3