Clinico-biological markers for the prognosis of status epilepticus in adults.
Clinico-biological scores
Prognosis
Recovery
Status epilepticus
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
received:
06
04
2022
accepted:
16
05
2022
revised:
15
05
2022
pubmed:
30
6
2022
medline:
14
10
2022
entrez:
29
6
2022
Statut:
ppublish
Résumé
Prediction of mortality, functional outcome and recovery after status epilepticus (SE) is a challenge. Biological and clinical markers have been proposed to reflect the brain injury or to monitor critical ill patients' severity. The aim of this study was to characterize short-term and long-term prognostic factors for SE patients hospitalized in intensive care unit. Patient's outcome was assessed using the modified Rankin Scale at discharge and after 6-12 months. We first assessed the univariate prognosis significance of 51 clinical, demographic or biochemical markers. Next, we built multivariate clinico-biological models by combining most important factors. Statistical models' performances were compared to those of two previous published scales STESS and mSTESS. Eighty-one patients were enrolled. Thirty-five patients showed a steady state while 46 patients clinically worsened at discharge: 14 died, 14 had persistent disability at 6-12 months and 18 recovered. Logistic regression analysis revealed that clinical markers (SE refractoriness, SE duration, de novo SE) were significant independent predictors of worsening while lipids markers and progranulin better predicted mortality. The association of clinico-biological variables allowed to accurately predict worsening at discharge (AUC > 0.72), mortality at discharge (AUC 0.83) and recovery at long-term (AUC 0.89). Previous scales provided lower prediction for worsening (AUC 0.63, STESS; 0.53, mSTESS) and mortality (AUC 0.56, STESS; 0.62, mSTESS) (p < 0.001). We proposed new clinico-biological models with a strong discrimination power for prediction of short- and long-term outcome of hospitalized status epilepticus patients. Their implementation in electronic devices may enhance their clinical liability.
Identifiants
pubmed: 35768546
doi: 10.1007/s00415-022-11199-4
pii: 10.1007/s00415-022-11199-4
doi:
Substances chimiques
Biomarkers
0
Lipids
0
Progranulins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5868-5882Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-10-IAIHU-06
Organisme : Fondation pour la Recherche Médicale
ID : FDM20170839111
Organisme : Fondation Assitance Publique-Hôpitaux de Paris
ID : EPIRES- Marie Laure PLV Merchandising
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.
Références
Trinka E, Kälviäinen R (2017) 25 years of advances in the definition, classification and treatment of status epilepticus. Seizure 44:65–73. https://doi.org/10.1016/j.seizure.2016.11.001
doi: 10.1016/j.seizure.2016.11.001
pubmed: 27890484
Leitinger M, Trinka E, Giovannini G et al (2019) Epidemiology of status epilepticus in adults: a population-based study on incidence, causes, and outcomes. Epilepsia 60:53–62. https://doi.org/10.1111/epi.14607
doi: 10.1111/epi.14607
pubmed: 30478910
Alkhachroum A, Der-Nigoghossian CA, Rubinos C, Claassen J (2020) Markers in status epilepticus prognosis. J Clin Neurophysiol 37:422–428. https://doi.org/10.1097/WNP.0000000000000761
doi: 10.1097/WNP.0000000000000761
pubmed: 32890064
pmcid: 7864547
Kantanen A-M, Reinikainen M, Parviainen I, Kälviäinen R (2017) Long-term outcome of refractory status epilepticus in adults: a retrospective population-based study. Epilepsy Res 133:13–21. https://doi.org/10.1016/j.eplepsyres.2017.03.009
doi: 10.1016/j.eplepsyres.2017.03.009
pubmed: 28402834
Rossetti AO, Logroscino G, Bromfield EB (2006) A clinical score for prognosis of status epilepticus in adults. Neurology 66:1736–1738. https://doi.org/10.1212/01.wnl.0000223352.71621.97
doi: 10.1212/01.wnl.0000223352.71621.97
pubmed: 16769951
González-Cuevas M, Santamarina E, Toledo M et al (2016) A new clinical score for the prognosis of status epilepticus in adults. Eur J Neurol 23:1534–1540. https://doi.org/10.1111/ene.13073
doi: 10.1111/ene.13073
pubmed: 27415411
Gao Q, Ou-Yang T, Sun X et al (2016) Prediction of functional outcome in patients with convulsive status epilepticus: the END-IT score. Crit Care 20:46. https://doi.org/10.1186/s13054-016-1221-9
doi: 10.1186/s13054-016-1221-9
pubmed: 26916702
pmcid: 4768332
Leitinger M, Höller Y, Kalss G et al (2015) Epidemiology-based mortality score in status epilepticus (EMSE). Neurocrit Care 22:273–282. https://doi.org/10.1007/s12028-014-0080-y
doi: 10.1007/s12028-014-0080-y
pubmed: 25412806
Yuan F, Gao Q, Jiang W (2018) Prognostic scores in status epilepticus-a critical appraisal. Epilepsia 59(Suppl 2):170–175. https://doi.org/10.1111/epi.14483
doi: 10.1111/epi.14483
pubmed: 30159870
Rossetti AO, Logroscino G, Milligan TA et al (2008) Status Epilepticus Severity Score (STESS): a tool to orient early treatment strategy. J Neurol 255:1561–1566. https://doi.org/10.1007/s00415-008-0989-1
doi: 10.1007/s00415-008-0989-1
pubmed: 18769858
Madžar D, Geyer A, Knappe RU et al (2016) Association of seizure duration and outcome in refractory status epilepticus. J Neurol 263:485–491. https://doi.org/10.1007/s00415-015-7992-0
doi: 10.1007/s00415-015-7992-0
pubmed: 26725091
Kang BS, Kim DW, Kim KK et al (2016) Prediction of mortality and functional outcome from status epilepticus and independent external validation of STESS and EMSE scores. Crit Care 20:25. https://doi.org/10.1186/s13054-016-1190-z
doi: 10.1186/s13054-016-1190-z
pubmed: 26812954
pmcid: 4728818
Ciurans J, Grau-López L, Jiménez M et al (2018) Refractory status epilepticus: Impact of baseline comorbidity and usefulness of STESS and EMSE scoring systems in predicting mortality and functional outcome. Seizure 56:98–103. https://doi.org/10.1016/j.seizure.2018.02.007
doi: 10.1016/j.seizure.2018.02.007
pubmed: 29462742
Giovannini G, Monti G, Tondelli M et al (2017) Mortality, morbidity and refractoriness prediction in status epilepticus: comparison of STESS and EMSE scores. Seizure 46:31–37. https://doi.org/10.1016/j.seizure.2017.01.004
doi: 10.1016/j.seizure.2017.01.004
pubmed: 28226274
Chaudhry F, Hunt RJ, Hariharan P et al (2020) Machine learning applications in the neuro ICU: a solution to big data mayhem? Front Neurol 11:554633. https://doi.org/10.3389/fneur.2020.554633
doi: 10.3389/fneur.2020.554633
pubmed: 33162926
pmcid: 7581704
von Elm E, Altman DG, Egger M et al (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med 4:e296. https://doi.org/10.1371/journal.pmed.0040296
doi: 10.1371/journal.pmed.0040296
DeGiorgio CM, Correale JD, Gott PS et al (1995) Serum neuron-specific enolase in human status epilepticus. Neurology 45:1134–1137
doi: 10.1212/WNL.45.6.1134
DeGiorgio CM, Heck CN, Rabinowicz AL et al (1999) Serum neuron-specific enolase in the major subtypes of status epilepticus. Neurology 52:746–749
doi: 10.1212/WNL.52.4.746
Hanin A, Baudin P, Demeret S et al (2021) Disturbances of brain cholesterol metabolism: a new excitotoxic process associated with status epilepticus. Neurobiol Dis 154:105346. https://doi.org/10.1016/j.nbd.2021.105346
doi: 10.1016/j.nbd.2021.105346
pubmed: 33774180
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. https://doi.org/10.1111/epi.13121
doi: 10.1111/epi.13121
pubmed: 26336950
Hirsch LJ, Gaspard N, van Baalen A et al (2018) Proposed consensus definitions for new-onset refractory status epilepticus (NORSE), febrile infection-related epilepsy syndrome (FIRES), and related conditions. Epilepsia 59:739–744. https://doi.org/10.1111/epi.14016
doi: 10.1111/epi.14016
pubmed: 29399791
Wu YW, Shek DW, Garcia PA et al (2002) Incidence and mortality of generalized convulsive status epilepticus in California. Neurology 58:1070–1076. https://doi.org/10.1212/wnl.58.7.1070
doi: 10.1212/wnl.58.7.1070
pubmed: 11940695
Hanin A, Denis JA, Frazzini V et al (2022) Neuron Specific Enolase, S100-beta protein and progranulin as diagnostic biomarkers of status epilepticus. J Neurol. https://doi.org/10.1007/s00415-022-11004-2
doi: 10.1007/s00415-022-11004-2
pubmed: 35768546
Hanin A, Demeret S, Denis JA et al (2021) Serum neuron-specific enolase: a new tool for seizure risk monitoring after status epilepticus. Eur J Neurol. https://doi.org/10.1111/ene.15154
doi: 10.1111/ene.15154
pubmed: 34687105
Hanin A, Lambrecq V, Denis JA et al (2020) Cerebrospinal fluid and blood biomarkers of status epilepticus. Epilepsia 61:6–18. https://doi.org/10.1111/epi.16405
doi: 10.1111/epi.16405
pubmed: 31828792
DeGiorgio CM, Gott PS, Rabinowicz AL et al (1996) Neuron-specific enolase, a marker of acute neuronal injury, is increased in complex partial status epilepticus. Epilepsia 37:606–609
doi: 10.1111/j.1528-1157.1996.tb00623.x
Correale J, Rabinowicz AL, Heck CN et al (1998) Status epilepticus increases CSF levels of neuron-specific enolase and alters the blood-brain barrier. Neurology 50:1388–1391
doi: 10.1212/WNL.50.5.1388
Freund Y, Bloom B, Bokobza J et al (2015) Predictive value of S100-B and copeptin for outcomes following seizure: the BISTRO international cohort study. PLoS ONE 10:e0122405. https://doi.org/10.1371/journal.pone.0122405
doi: 10.1371/journal.pone.0122405
pubmed: 25849778
pmcid: 4388444
Zhu S, Tai C, Petkau TL et al (2013) Progranulin promotes activation of microglia/macrophage after pilocarpine-induced status epilepticus. Brain Res 1530:54–65. https://doi.org/10.1016/j.brainres.2013.07.023
doi: 10.1016/j.brainres.2013.07.023
pubmed: 23887054
Sen J, Belli A (2007) S100B in neuropathologic states: the CRP of the brain? J Neurosci Res 85:1373–1380. https://doi.org/10.1002/jnr.21211
doi: 10.1002/jnr.21211
pubmed: 17348038
Chali F, Djelti F, Eugene E et al (2015) Inhibiting cholesterol degradation induces neuronal sclerosis and epileptic activity in mouse hippocampus. Eur J Neurosci 41:1345–1355. https://doi.org/10.1111/ejn.12911
doi: 10.1111/ejn.12911
pubmed: 25847620
pmcid: 4439180
Chali F, Milior G, Marty S et al (2019) Lipid markers and related transcripts during excitotoxic neurodegeneration in kainate-treated mice. Eur J Neurosci 50:1759–1778. https://doi.org/10.1111/ejn.14375
doi: 10.1111/ejn.14375
pubmed: 30767299
Bateman RM, Sharpe MD, Jagger JE et al (2016) 36th international symposium on intensive care and emergency medicine: Brussels, Belgium, 15–18 March 2016. Crit Care 20:94. https://doi.org/10.1186/s13054-016-1208-6
doi: 10.1186/s13054-016-1208-6
pmcid: 5493079
Hifumi T, Nakamura K, Kuroda Y et al (2021) High early phase hemoglobin level is associated with favorable neurological outcome in patients with severe traumatic brain injury. Am J Emerg Med 44:373–377. https://doi.org/10.1016/j.ajem.2020.04.065
doi: 10.1016/j.ajem.2020.04.065
pubmed: 32507479
Lan P, Wang S-J, Shi Q-C et al (2018) Comparison of the predictive value of scoring systems on the prognosis of cirrhotic patients with suspected infection. Medicine (Baltimore) 97:e11421. https://doi.org/10.1097/MD.0000000000011421
doi: 10.1097/MD.0000000000011421
Lv Z, Wang W, Qiao B et al (2021) The prognostic value of general laboratory testing in patients with COVID-19. J Clin Lab Anal 35:e23668. https://doi.org/10.1002/jcla.23668
doi: 10.1002/jcla.23668
pubmed: 33314316
Sonneville R, Mariotte E, Neuville M et al (2016) Early-onset status epilepticus in patients with acute encephalitis. Medicine (Baltimore) 95:e4092. https://doi.org/10.1097/MD.0000000000004092
doi: 10.1097/MD.0000000000004092
Madžar D, Reindl C, Mrochen A et al (2021) Value of initial C-reactive protein levels in status epilepticus outcome prediction. Epilepsia 62:e48–e52. https://doi.org/10.1111/epi.16842
doi: 10.1111/epi.16842
pubmed: 33609292
Bruno A, Shah N, Lin C et al (2010) Improving modified Rankin Scale assessment with a simplified questionnaire. Stroke 41:1048–1050. https://doi.org/10.1161/STROKEAHA.109.571562
doi: 10.1161/STROKEAHA.109.571562
pubmed: 20224060
Noble WS (2006) What is a support vector machine? Nat Biotechnol 24:1565–1567
doi: 10.1038/nbt1206-1565
Ojala M, Garriga G (2010) Permutation tests for studying classifier performance. J Mach Learn Res 11:1833–1863
Saito T, Rehmsmeier M (2015) The precision-recall plot is more informative than the ROC plot when evaluating binary classifiers on imbalanced datasets. PLoS ONE 10:e0118432. https://doi.org/10.1371/journal.pone.0118432
doi: 10.1371/journal.pone.0118432
pubmed: 25738806
pmcid: 4349800
Marawar R, Basha M, Mahulikar A et al (2018) Updates in refractory status epilepticus. Crit Care Res Pract 2018:9768949. https://doi.org/10.1155/2018/9768949
doi: 10.1155/2018/9768949
pubmed: 29854452
pmcid: 5964484
Adibhatla RM, Hatcher JF (2008) Altered lipid metabolism in brain injury and disorders. Subcell Biochem 49:241–268. https://doi.org/10.1007/978-1-4020-8831-5_9
doi: 10.1007/978-1-4020-8831-5_9
pubmed: 18751914
pmcid: 2293298
Maxfield FR, Tabas I (2005) Role of cholesterol and lipid organization in disease. Nature 438:612–621. https://doi.org/10.1038/nature04399
doi: 10.1038/nature04399
pubmed: 16319881
Gaspard N, Hirsch LJ, Sculier C et al (2018) New-onset refractory status epilepticus (NORSE) and febrile infection-related epilepsy syndrome (FIRES): state of the art and perspectives. Epilepsia 59:745–752. https://doi.org/10.1111/epi.14022
doi: 10.1111/epi.14022
pubmed: 29476535
Gaspard N, Foreman BP, Alvarez V et al (2015) New-onset refractory status epilepticus: etiology, clinical features, and outcome. Neurology 85:1604–1613. https://doi.org/10.1212/WNL.0000000000001940
doi: 10.1212/WNL.0000000000001940
pubmed: 26296517
pmcid: 4642147
Sutter R, Kaplan PW, Rüegg S (2013) Independent external validation of the status epilepticus severity score. Crit Care Med 41:e475-479. https://doi.org/10.1097/CCM.0b013e31829eca06
doi: 10.1097/CCM.0b013e31829eca06
pubmed: 23982031
Pacha MS, Orellana L, Silva E et al (2016) Role of EMSE and STESS scores in the outcome evaluation of status epilepticus. Epilepsy Behav 64:140–142. https://doi.org/10.1016/j.yebeh.2016.09.036
doi: 10.1016/j.yebeh.2016.09.036
pubmed: 27741463
Hutson M (2018) Artificial intelligence faces reproducibility crisis. Science 359:725–726. https://doi.org/10.1126/science.359.6377.725
doi: 10.1126/science.359.6377.725
pubmed: 29449469
The Lancet Respiratory Medicine (2018) Opening the black box of machine learning. Lancet Respir Med 6:801. https://doi.org/10.1016/S2213-2600(18)30425-9
doi: 10.1016/S2213-2600(18)30425-9
pubmed: 30343029
Snodgrass SM, Tsuburaya K, Ajmone-Marsan C (1989) Clinical significance of periodic lateralized epileptiform discharges: relationship with status epilepticus. J Clin Neurophysiol 6:159–172. https://doi.org/10.1097/00004691-198904000-00003
doi: 10.1097/00004691-198904000-00003
pubmed: 2708516
Trinka E, Leitinger M (2022) Management of status epilepticus, refractory status epilepticus, and super-refractory status epilepticus. Continuum (Minneap Minn) 28:559–602. https://doi.org/10.1212/CON.0000000000001103
doi: 10.1212/CON.0000000000001103