Abstract
Background
The objective of this study was to validate the value of the Status Epilepticus Severity Score (STESS) in the prediction of the risk of in-hospital mortality in patients with nonhypoxic status epilepticus (SE) using a machine learning analysis.
Methods
We included consecutive patients with nonhypoxic SE (aged ≥ 16 years) admitted from 2013 to 2021 at the Modena Academic Hospital. A decision tree analysis was performed using in-hospital mortality as a dependent variable and the STESS predictors as input variables. We evaluated the accuracy of STESS in predicting in-hospital mortality using the area under the receiver operating characteristic curve (AUROC) with 95% confidence interval (CI).
Results
Among 629 patients with SE, the in-hospital mortality rate was 23.4% (147 of 629). The median STESS in the entire cohort was 2.9 (SD 1.6); it was lower in surviving compared with deceased patients (2.7, SD 1.5 versus 3.9, SD 1.6; p < 0.001). Of deceased patients, 82.3% (121 of 147) had scores of 3–6, whereas 17.7% (26 of 147) had scores of 0–2 (p < 0.001). STESS was accurate in predicting mortality, with an AUROC of 0.688 (95% CI 0.641–0.734) only slightly reduced after bootstrap resampling. The most significant predictor was the seizure type, followed by age and level of consciousness at SE onset. Nonconvulsive SE in coma and age ≥ 65 years predicted a higher risk of mortality, whereas generalized convulsive SE and age < 65 years were associated with a lower risk of death. The decision tree analysis using STESS variables correctly classified 90% of survivors and 34% of nonsurvivors after the SE, with an overall risk of error of 23.1%.
Conclusions
This validation study using a machine learning system showed that STESS is a valuable prognostic tool. The score appears particularly accurate and effective in identifying patients who are alive at discharge (high negative predictive value), whereas it has a lower predictive value for in-hospital mortality.
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Data Availability
On request from qualified investigators, we will share anonymized data.
References
Trinka E, Cock H, Hesdorffer D, et al. A definition and classification of status epilepticus–report of the ILAE task force on classification of status epilepticus. Epilepsia. 2015;56(10):1515–23. https://doi.org/10.1111/epi.13121.
Leitinger M, Trinka E, Zimmermann G, Granbichler CA, Kobulashvili T, Siebert U. Epidemiology of status epilepticus in adults: apples, pears, and oranges - a critical review. Epilepsy Behav. 2020;103(Pt A): 106720. https://doi.org/10.1016/j.yebeh.2019.106720.
Neligan A, Shorvon SD. Frequency and prognosis of convulsive status epilepticus of different causes: a systematic review. Arch Neurol. 2010;67(8):931–40. https://doi.org/10.1001/archneurol.2010.169.
Giovannini G, Monti G, Tondelli M, et al. Mortality, morbidity and refractoriness prediction in status epilepticus: comparison of STESS and EMSE scores. Seizure. 2017;46:31–7. https://doi.org/10.1016/j.seizure.2017.01.004.
Yuan F, Gao Q, Jiang W. Prognostic scores in status epilepticus-a critical appraisal. Epilepsia. 2018;59(Suppl 2):170–5. https://doi.org/10.1111/epi.14483.
Rossetti AO, Logroscino G, Bromfield EB. A clinical score for prognosis of status epilepticus in adults. Neurology. 2006;66(11):1736–8. https://doi.org/10.1212/01.wnl.0000223352.71621.97.
Rossetti AO, Logroscino G, Milligan TA, Michaelides C, Ruffieux C, Bromfield EB. Status epilepticus severity score (STESS): a tool to orient early treatment strategy. J Neurol. 2008;255(10):1561–6. https://doi.org/10.1007/s00415-008-0989-1.
Goyal MK, Chakravarthi S, Modi M, Bhalla A, Lal V. Status epilepticus severity score (STESS): a useful tool to predict outcome of status epilepticus. Clin Neurol Neurosurg. 2015;139:96–9. https://doi.org/10.1016/j.clineuro.2015.09.010.
Pacha MS, Orellana L, Silva E, et al. Role of EMSE and STESS scores in the outcome evaluation of status epilepticus. Epilepsy Behav. 2016;64(Pt A):140–2. https://doi.org/10.1016/j.yebeh.2016.09.036.
Aukland P, Lando M, Vilholm O, Christiansen EB, Beier CP. Predictive value of the status epilepticus severity score (STESS) and its components for long-term survival. BMC Neurol. 2016;16(1):213. https://doi.org/10.1186/s12883-016-0730-0.
González-Cuevas M, Santamarina E, Toledo M, et al. A new clinical score for the prognosis of status epilepticus in adults. Eur J Neurol. 2016;23(10):1534–40. https://doi.org/10.1111/ene.13073.
Sutter R, Kaplan PW, Rüegg S. Independent external validation of the status epilepticus severity score. Crit Care Med. 2013;41(12):e475–9. https://doi.org/10.1097/CCM.0b013e31829eca06.
Leitinger M, Höller Y, Kalss G, et al. Epidemiology-based mortality score in status epilepticus (EMSE). Neurocrit Care. 2015;22(2):273–82. https://doi.org/10.1007/s12028-014-0080-y.
Kang BS, Kim DW, Kim KK, et al. Prediction of mortality and functional outcome from status epilepticus and independent external validation of STESS and EMSE scores. Crit Care. 2016;20:25. https://doi.org/10.1186/s13054-016-1190-z.
Wang P, Guan Y, Lin X, et al. Diagnostic value of status epilepticus severity score for survival conditions of patients with status epilepticus: a PRISMA-compliant systematic review and meta-analysis. Epilepsy Behav. 2018;82:104–10. https://doi.org/10.1016/j.yebeh.2018.02.033.
Leitinger M, Kalss G, Rohracher A, et al. Predicting outcome of status epilepticus. Epilepsy Behav. 2015;49:126–30. https://doi.org/10.1016/j.yebeh.2015.04.066.
Song YY, Lu Y. Decision tree methods: applications for classification and prediction. Shanghai Arch Psychiatry. 2015;27:130–5.
Shirali GA, Noroozi MV, Malehi AS. Predicting the outcome of occupational accidents by CART and CHAID methods at a steel factory in Iran. J Public Health Res. 2018;7:1361.
Brigo F, Turcato G, Lattanzi S, et al. Machine-learning validation through decision-tree analysis of the epidemiology-based mortality score in status epilepticus. Epilepsia. 2022. https://doi.org/10.1111/epi.17372.
Leitinger M, Beniczky S, Rohracher A, et al. Salzburg consensus criteria for non-convulsive status epilepticus–approach to clinical application. Epilepsy Behav. 2015;49:158–63. https://doi.org/10.1016/j.yebeh.2015.05.007.
Leitinger M, Trinka E, Gardella E, et al. Diagnostic accuracy of the Salzburg EEG criteria for non-convulsive status epilepticus: a retrospective study. Lancet Neurol. 2016;15(10):1054–62. https://doi.org/10.1016/S1474-4422(16)30137-5.
Brophy GM, Bell R, Claassen J, et al. Guidelines for the evaluation and management of status epilepticus. Neurocrit Care. 2012;17(1):3–23. https://doi.org/10.1007/s12028-012-9695-z.
Glauser T, Shinnar S, Gloss D, et al. Evidence-based guideline: treatment of convulsive status epilepticus in children and adults: report of the guideline committee of the American epilepsy society. Epilepsy Curr. 2016;16(1):48–61. https://doi.org/10.5698/1535-7597-16.1.48.
Minicucci F, Ferlisi M, Brigo F, et al. Management of status epilepticus in adults position paper of the Italian League against epilepsy. Epilepsy Behav. 2020;102:106675. https://doi.org/10.1016/j.yebeh.2019.106675.
Hajian-Tilaki K. Receiver operating characteristic (ROC) curve analysis for medical diagnostic test evaluation. Caspian J Intern Med. 2013;4(2):627–35.
Park SH, Goo JM, Jo CH. Receiver operating characteristic (ROC) curve: practical review for radiologists. Korean J Radiol. 2004;5(1):11–8.
Turcato G, Zaboli A, Pfeifer N, et al. Decision tree analysis to predict the risk of intracranial haemorrhage after mild traumatic brain injury in patients taking DOACs. Am J Emerg Med. 2021;50:388–93.
Song YY, Lu Y. Decision tree methods: applications for classification and prediction. Shanghai Arch Psychiatry. 2015;27(2):130–5. https://doi.org/10.11919/j.issn.1002-0829.215044.
Shirali GA, Noroozi MV, Malehi AS. Predicting the outcome of occupational accidents by CART and CHAID methods at a steel factory in Iran. J Public Health Res. 2018;7(2):1361. https://doi.org/10.4081/jphr.2018.1361.
Towne AR, Pellock JM, Ko D, DeLorenzo RJ. Determinants of mortality in status epilepticus. Epilepsia. 1994;35(1):27–34. https://doi.org/10.1111/j.1528-1157.1994.tb02908.x.
Logroscino G, Hesdorffer DC, Cascino G, Annegers JF, Hauser WA. Short-term mortality after a first episode of status epilepticus. Epilepsia. 1997;38(12):1344–9. https://doi.org/10.1111/j.1528-1157.1997.tb00073.x.
Koubeissi M, Alshekhlee A. In-hospital mortality of generalized convulsive status epilepticus: a large US sample. Neurology. 2007;69(9):886–93. https://doi.org/10.1212/01.wnl.0000269791.96189.70.
Leitinger M, Trinka E, Giovannini G, et al. Epidemiology of status epilepticus in adults: a population-based study on incidence, causes, and outcomes. Epilepsia. 2019;60(1):53–62. https://doi.org/10.1111/epi.14607.
Logroscino G, Hesdorffer DC, Cascino G, Annegers JF, Hauser WA. Time trends in incidence, mortality, and case-fatality after first episode of status epilepticus. Epilepsia. 2001;42(8):1031–5. https://doi.org/10.1046/j.1528-1157.2001.0420081031.x.
Lattanzi S, Giovannini G, Brigo F, Orlandi N, Trinka E, Meletti S. Status epilepticus with prominent motor symptoms clusters into distinct electroclinical phenotypes. Eur J Neurol. 2021;28(8):2694–9. https://doi.org/10.1111/ene.14891.
Sutter R, Kaplan PW. The neurophysiologic types of nonconvulsive status epilepticus: EEG patterns of different phenotypes. Epilepsia. 2013;54(Suppl 6):23–7.
Sutter R, Semmlack S, Kaplan PW. Nonconvulsive status epilepticus in adults - insights into the invisible. Nat Rev Neurol. 2016;12(5):281–93.
Sutter R. Are we prepared to detect subtle and nonconvulsive status epilepticus in critically Ill patients? J Clin Neurophysiol. 2016;33(1):25–31.
Kinney MO, Craig JJ, Kaplan PW. Hidden in plain sight: Non-convulsive status epilepticus—recognition and management. Acta Neurol Scand. 2017;136:280–92.
Teasdale G, Jennett B. Assessment of coma and impaired consciousness A practical scale. Lancet. 1974;2(7872):81–4. https://doi.org/10.1016/s0140-6736(74)91639-0.
Lattanzi S, Giovannini G, Brigo F, Orlandi N, Trinka E, Meletti S. Clinical phenotypes within nonconvulsive status epilepticus. Epilepsia. 2021;62(9):e129–34. https://doi.org/10.1111/epi.16999.
Semmlack S, Kaplan PW, Spiegel R, et al. Illness severity scoring in status epilepticus-when STESS meets APACHE II, SAPS II, and SOFA. Epilepsia. 2019;60(2):189–200.
Sutter R, Semmlack S, Opić P, et al. Untangling operational failures of the Status Epilepticus Severity Score (STESS). Neurology. 2019;92(17):e1948–56.
Yechoor N, Adeli A, Hafeez S. External validation of the epidemiology-based mortality score in status epilepticus in an American intensive care population. Epilepsy Res. 2018;148:32–6. https://doi.org/10.1016/j.eplepsyres.2018.10.001.
Huang TH, Lai MC, Chen YS, Huang CW. Status epilepticus mortality risk factors and a correlation survey with the newly modified STESS. Healthcare (Basel). 2021;9(11):1570.
Funding
This research received funding from the Italian MOH (“Status epilepticus: improving therapeutic and quality of care intervention in the Emilia-Romagna region”; project code: RF-2016–02,361,365) and by the MIUR (grant “Dipartimenti di eccellenza 2018–2022” to the Department of Biomedical, Metabolic, and Neural Sciences, University of Modena and Reggio-Emilia).
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FB: conceptualization, methodology, original draft preparation. GT: conceptualization, formal analysis, methodology, original draft preparation. SL: methodology, review and editing. NO: data curation, investigation, review and editing. GT: data curation, investigation, review and editing. AZ: methodology, visualization, review and editing. GG: data curation, investigation, review and editing. SM: review and editing, supervision, validation.
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The study was approved by the local ethical committee (ethics committee approval number 556/2018/OSS/AOUMO–RF‐2016‐02,361,365) and was conducted according to the ethical principles for medical research involving human subjects in the Declaration of Helsinki.
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Brigo, F., Turcato, G., Lattanzi, S. et al. Retrospective External Validation of the Status Epilepticus Severity Score (STESS) to Predict In-hospital Mortality in Adults with Nonhypoxic Status Epilepticus: A Machine Learning Analysis. Neurocrit Care 38, 254–262 (2023). https://doi.org/10.1007/s12028-022-01610-3
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DOI: https://doi.org/10.1007/s12028-022-01610-3