Predicting posttraumatic epilepsy using admission electroencephalography after severe traumatic brain injury.


Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
07 2023
Historique:
revised: 17 04 2023
received: 12 09 2022
accepted: 18 04 2023
medline: 13 7 2023
pubmed: 19 4 2023
entrez: 19 04 2023
Statut: ppublish

Résumé

Posttraumatic epilepsy (PTE) develops in as many as one third of severe traumatic brain injury (TBI) patients, often years after injury. Analysis of early electroencephalographic (EEG) features, by both standardized visual interpretation (viEEG) and quantitative EEG (qEEG) analysis, may aid early identification of patients at high risk for PTE. We performed a case-control study using a prospective database of severe TBI patients treated at a single center from 2011 to 2018. We identified patients who survived 2 years postinjury and matched patients with PTE to those without using age and admission Glasgow Coma Scale score. A neuropsychologist recorded outcomes at 1 year using the Expanded Glasgow Outcomes Scale (GOSE). All patients underwent continuous EEG for 3-5 days. A board-certified epileptologist, blinded to outcomes, described viEEG features using standardized descriptions. We extracted 14 qEEG features from an early 5-min epoch, described them using qualitative statistics, then developed two multivariable models to predict long-term risk of PTE (random forest and logistic regression). We identified 27 patients with and 35 without PTE. GOSE scores were similar at 1 year (p = .93). The median time to onset of PTE was 7.2 months posttrauma (interquartile range = 2.2-22.2 months). None of the viEEG features was different between the groups. On qEEG, the PTE cohort had higher spectral power in the delta frequencies, more power variance in the delta and theta frequencies, and higher peak envelope (all p < .01). Using random forest, combining qEEG and clinical features produced an area under the curve of .76. Using logistic regression, increases in the delta:theta power ratio (odds ratio [OR] = 1.3, p < .01) and peak envelope (OR = 1.1, p < .01) predicted risk for PTE. In a cohort of severe TBI patients, acute phase EEG features may predict PTE. Predictive models, as applied to this study, may help identify patients at high risk for PTE, assist early clinical management, and guide patient selection for clinical trials.

Identifiants

pubmed: 37073101
doi: 10.1111/epi.17622
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1842-1852

Informations de copyright

© 2023 International League Against Epilepsy.

Références

Pease M, Gonzalez-Martinez J, Puccio A, Nwachuku E, Castellano JF, Okonkwo DO, et al. Risk factors and incidence of epilepsy after severe traumatic brain injury. Ann Neurol. 2022;92:663-9. https://doi.org/10.1002/ana.26443
Annegers JF, Hauser WA, Coan SP, Rocca WA. A population-based study of seizures after traumatic brain injuries. N Engl J Med. 1998;338(1):20-4. https://doi.org/10.1056/NEJM199801013380104
Englander J, Bushnik T, Duong TT, Cifu DX, Zafonte R, Wright J, et al. Analyzing risk factors for late posttraumatic seizures: a prospective, multicenter investigation. Arch Phys Med Rehabil. 2003;84(3 Suppl. 1):365-73. https://doi.org/10.1053/apmr.2003.50022
Tubi MA, Lutkenhoff E, Blanco MB, McArthur D, Villablanca P, Ellingson B, et al. Early seizures and temporal lobe trauma predict post-traumatic epilepsy: a longitudinal study. Neurobiol Dis. 2019;123:115-21. https://doi.org/10.1016/j.nbd.2018.05.014
Gupta PK, Sayed N, Ding K, Agostini MA, van Ness PC, Yablon S, et al. Subtypes of post-traumatic epilepsy: clinical, electrophysiological, and imaging features. J Neurotrauma. 2014;31(16):1439-43. https://doi.org/10.1089/neu.2013.3221
Thijs RD, Surges R, O'Brien TJ, Sander JW. Epilepsy in adults. Lancet. 2019;393(10172):689-701. https://doi.org/10.1016/S0140-6736(18)32596-0
Fordington S, Manford M. A review of seizures and epilepsy following traumatic brain injury. J Neurol. 2020;267(10):3105-11. https://doi.org/10.1007/s00415-020-09926-w
Farrell JS, Wolff MD, Teskey GC. Neurodegeneration and pathology in epilepsy: clinical and basic perspectives. Adv Neurobiol. 2017;15:317-34. https://doi.org/10.1007/978-3-319-57193-5_12
Mukhtar I. Inflammatory and immune mechanisms underlying epileptogenesis and epilepsy: from pathogenesis to treatment target. Seizure. 2020;82:65-79. https://doi.org/10.1016/j.seizure.2020.09.015
Burke J, Gugger J, Ding K, Kim JA, Foreman B, Yue JK, et al. Association of Posttraumatic Epilepsy with 1-year outcomes after traumatic brain injury. JAMA Netw Open. 2021;4(12):1-14. https://doi.org/10.1001/jamanetworkopen.2021.40191
Pease M, Mallela AN, Elmer J, Okonkwo DO, Shutter L, Barot N, et al. Association of posttraumatic epilepsy with long-term functional outcomes in individuals with severe traumatic brain injury. Neurology. 2023. [Online ahead of print]. https://doi.org/10.1212/WNL.0000000000207183
Pingue V, Mele C, Nardone A. Post-traumatic seizures and antiepileptic therapy as predictors of the functional outcome in patients with traumatic brain injury. Sci Rep. 2021;11(1):1-12. https://doi.org/10.1038/s41598-021-84203-y
Titano JJ, Badgeley M, Schefflein J, Pain M, Su A, Cai M, et al. Automated deep-neural-network surveillance of cranial images for acute neurologic events. Nat Med. 2018;24(9):1337-41. https://doi.org/10.1038/s41591-018-0147-y
Pease M, Arefan D, Barber J, Yuh E, Puccio A, Hochberger K, et al. Outcome prediction in patients with severe traumatic brain injury using deep learning from head CT scans. Radiology. 2022;304:385-94. https://doi.org/10.1148/radiol.212181
Farzaneh N, Williamson CA, Gryak J, Najarian K. A hierarchical expert-guided machine learning framework for clinical decision support systems: an application to traumatic brain injury prognostication. Npj Digit Med. 2021;4(1):1-9. https://doi.org/10.1038/s41746-021-00445-0
Raj R, Luostarinen T, Pursiainen E, Posti JP, Takala RSK, Bendel S, et al. Machine learning-based dynamic mortality prediction after traumatic brain injury. Sci Rep. 2019;9(1):1-13. https://doi.org/10.1038/s41598-019-53889-6
Yang I, Chang EF, Han SJ, Barry JJ, Fang S, Tihan T, et al. Early surgical intervention in adult patients with ganglioglioma is associated with improved clinical seizure outcomes. J Clin Neurosci off J Neurosurg Soc Australas. 2011;18(1):29-33. https://doi.org/10.1016/j.jocn.2010.05.002
Freitag H, Tuxhorn I. Cognitive function in preschool children after epilepsy surgery: rationale for early intervention. Epilepsia. 2005;46(4):561-7. https://doi.org/10.1111/j.0013-9580.2005.03504.x
Engel JJ, McDermott MP, Wiebe S, Langfitt JT, Stern JM, Dewar S, et al. Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA. 2012;307(9):922-30. https://doi.org/10.1001/jama.2012.220
Etc MCS, Das C, Lucia MS, H K, T J. 乳鼠心肌提取 HHS public access. Physiol Behav. 2019;176(3):139-48. https://doi.org/10.1097/CCM.0000000000003639.Continuous
Chen DF, Kumari P, Haider HA, Ruiz AR, Lega J, Dhakar MB. Association of Epileptiform Abnormality on electroencephalography with development of epilepsy after acute brain injury. Neurocrit Care. 2021;35(2):428-33. https://doi.org/10.1007/s12028-020-01182-0
Haveman ME, van Putten MJAM, Beishuizen A, Hom HW, Eertman-Meyer CJ, Tjepkema-Cloostermans MC. P39-T predicting outcome in patients with moderate to severe traumatic brain injury using electroencephalography. Clin Neurophysiol. 2019;130(7):e50. https://doi.org/10.1016/j.clinph.2019.04.402
Müller M, Rossetti AO, Zimmermann R, Alvarez V, Rüegg S, Haenggi M, et al. Standardized visual EEG features predict outcome in patients with acute consciousness impairment of various etiologies. Crit Care. 2020;24(1):1-13. https://doi.org/10.1186/s13054-020-03407-2
Westhall E, Rossetti AO, Van Rootselaar A, Wesenberg Kjaer T, Horn J, Ullén S, et al. Standardized EEG interpretation accurately predicts prognosis after cardiac arrest. Neurology. 2016;86(16):1482-90. https://doi.org/10.1212/WNL.0000000000002462
Noor NSEM, Ibrahim H. Machine learning algorithms and quantitative electroencephalography predictors for outcome prediction in traumatic brain injury: A systematic review. IEEE Access. 2020;8:102075-92. https://doi.org/10.1109/ACCESS.2020.2998934
Vespa PM, Boscardin WJ, Hovda DA, McArthur DL, Nuwer MR, Martin NA, et al. Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. J Neurosurg. 2002;97(1):84-92. https://doi.org/10.3171/jns.2002.97.1.0084
Smith PH, Bessette AJ, Weinberger AH, Sheffer CE, Mckee SA. 乳鼠心肌提取 HHS public access. Physiol Behav. 2016;92(3):135-40. https://doi.org/10.1016/j.nbd.2018.06.002.Electrophysiological
Jennett B, van de Sande J. EEG prediction of post-traumatic epilepsy. Epilepsia. 1975;16(2):251-6. https://doi.org/10.1111/j.1528-1157.1975.tb06055.x
Foster JB. Traumatic epilepsy. Med Leg J. 1962;30(4):20-4. https://doi.org/10.1177/002581726203000103
Angeleri F, Majkowski J, Cacchiò G, Sobieszek A, D'Acunto S, Gesuita R, et al. Posttraumatic epilepsy risk factors: one-year prospective study after head injury. Epilepsia. 1999;40(9):1222-30. https://doi.org/10.1111/j.1528-1157.1999.tb00850.x
Pease M, Nwachuku E, Goldschmidt E, Elmer J, Okonkwo DO. Complications from multimodal monitoring do not affect long-term outcomes in severe traumatic brain injury. World Neurosurg. 2022;161:e109-17. https://doi.org/10.1016/j.wneu.2022.01.059
Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig L, et al. STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. Radiology. 2015;277(3):826-32. https://doi.org/10.1148/radiol.2015151516
Ritter AC, Wagner AK, Fabio A, Pugh MJ, Walker WC, Szaflarski JP, et al. Incidence and risk factors of posttraumatic seizures following traumatic brain injury: A traumatic brain injury model systems study. Epilepsia. 2016;57(12):1968-77. https://doi.org/10.1111/epi.13582
Haltiner AM, Temkin NR, Dikmen SS. Risk of seizure recurrence after the first late posttraumatic seizure. Arch Phys Med Rehabil. 1997;78(8):835-40. https://doi.org/10.1016/S0003-9993(97)90196-9
Hirsch LJ, Fong MWK, Leitinger M, LaRoche SM, Beniczky S, Abend NS, et al. American clinical neurophysiology Society's standardized critical care EEG terminology: 2021 version. J Clin Neurophysiol. 2021;38(1):1-29. https://doi.org/10.1097/WNP.0000000000000806
Cooper DJ, Rosenfeld JV, Murray L, Arabi YM, Davies AR, D'Urso P, et al. Decompressive craniectomy in diffuse traumatic brain injury. N Engl J Med. 2011;364(16):1493-502. https://doi.org/10.1056/NEJMoa1102077
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57(1):289-300.
Biau G, Scornet E. A random forest guided tour. TEST. 2016;25(2):197-227. https://doi.org/10.1007/s11749-016-0481-7
Marcoulides KM, Raykov T. Evaluation of variance inflation factors in regression models using latent variable modeling methods. Educ Psychol Meas. 2019;79(5):874-82. https://doi.org/10.1177/0013164418817803
Özbek Y, Fide E, Yener GG. Resting-state EEG alpha/theta power ratio discriminates early-onset Alzheimer's disease from healthy controls. Clin Neurophysiol off J Int Fed Clin Neurophysiol. 2021;132(9):2019-31. https://doi.org/10.1016/j.clinph.2021.05.012
Moretti DV, Paternicò D, Binetti G, Zanetti O, Frisoni GB. Electroencephalographic upper/low alpha frequency power ratio relates to cortex thinning in mild cognitive impairment. Neurodegener Dis. 2014;14(1):18-30. https://doi.org/10.1159/000354863
Yu Z, Wen D, Zheng J, Guo R, Li H, You C, et al. Predictive accuracy of Alpha-Delta ratio on quantitative electroencephalography for delayed cerebral ischemia in patients with aneurysmal subarachnoid hemorrhage: meta-analysis. World Neurosurg. 2019;126:e510-6. https://doi.org/10.1016/j.wneu.2019.02.082
Murphy K. Machine learning: a probabilistic perspective. Cambridge, MA: MIT Press; 2013.
Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JMM. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics. 2011;12:77.
Lundberg S, Lee S-I. A unified approach to interpreting model predictions. arXiv 2017. https://arxiv.org/abs/1705.07874
Lin M-Y, Li C-C, Lin P-H, Wang JL, Chan MC, Wu CL, et al. Explainable machine learning to predict successful weaning among patients requiring prolonged mechanical ventilation: A retrospective cohort study in Central Taiwan. Front Med. 2021;8:663739. https://doi.org/10.3389/fmed.2021.663739
Richter S, Stevenson S, Newman T, Wilson L, Menon DK, Maas AIR, et al. Handling of missing outcome data in traumatic brain injury research: a systematic review. J Neurotrauma. 2019;36(19):2743-52. https://doi.org/10.1089/neu.2018.6216
Miranda P, Cox CD, Alexander M, Lakey JRT, Danev S. Electroencephalography (EEG)-based detection, management, recovery and brain retraining tracking of Traumatic Brain Injury (TBI) when “Only Time Can Tell”. J Syst Integr Neurosci. 2020;6(3):1-15. https://doi.org/10.15761/jsin.1000230
Baranowski CJ. The quality of life of older adults with epilepsy: a systematic review. Seizure. 2018;60:190-7. https://doi.org/10.1016/j.seizure.2018.06.002
Begley CE, Durgin TL. The direct cost of epilepsy in the United States: a systematic review of estimates. Epilepsia. 2015;56(9):1376-87. https://doi.org/10.1111/epi.13084
Nudo R. Recovery after brain injury: mechanisms and principles. Front Hum Neurosci. 2013;7:887. https://doi.org/10.3389/fnhum.2013.00887
Carney N, Totten AM, O'Reilly C, Ullman JS, Hawryluk GWJ, Bell MJ, et al. Guidelines for the management of severe traumatic brain injury, fourth edition. Neurosurgery. 2017;80(1):6-15. https://doi.org/10.1227/NEU.0000000000001432
Hutchinson PJ, Kolias AG, Timofeev IS, Corteen EA, Czosnyka M, Timothy J, et al. Trial of decompressive craniectomy for traumatic intracranial hypertension. N Engl J Med. 2016;375(12):1119-30. https://doi.org/10.1056/nejmoa1605215
Brigo F, Cicero R, Fiaschi A, Bongiovanni LG. The breach rhythm. Clin Neurophysiol off J Int Fed Clin Neurophysiol. 2011;122(11):2116-20. https://doi.org/10.1016/j.clinph.2011.07.024
Quist J, Taylor L, Staaf J, Grigoriadis A. Random Forest modelling of high-dimensional mixed-type data for breast cancer classification. Cancers (Basel). 2021;13(5):991. https://doi.org/10.3390/cancers13050991
Luo G, Zhu Y, Wang R, Tong Y, Lu W, Wang H. Random forest-based classsification and analysis of hemiplegia gait using low-cost depth cameras. Med Biol Eng Comput. 2020;58(2):373-82. https://doi.org/10.1007/s11517-019-02079-7

Auteurs

Matthew Pease (M)

Department of Neurological Surgery, University of Pittsburgh Medical Center Healthcare System, Pittsburgh, Pennsylvania, USA.

Jonathan Elmer (J)

Department of Neurology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.
Department of Critical Care, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.
Department of Emergency Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

Ameneh Zare Shahabadi (AZ)

Department of Neurology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

Arka N Mallela (AN)

Department of Neurological Surgery, University of Pittsburgh Medical Center Healthcare System, Pittsburgh, Pennsylvania, USA.

Juan F Ruiz-Rodriguez (JF)

Department of Neurological Surgery, University of Washington, Seattle, Washington, USA.

Daniel Sexton (D)

Department of Neurosurgery, Duke University, Durham, North Carolina, USA.

Niravkumar Barot (N)

Department of Neurology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

Jorge A Gonzalez-Martinez (JA)

Department of Neurological Surgery, University of Pittsburgh Medical Center Healthcare System, Pittsburgh, Pennsylvania, USA.

Lori Shutter (L)

Department of Neurological Surgery, University of Pittsburgh Medical Center Healthcare System, Pittsburgh, Pennsylvania, USA.
Department of Neurology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.
Department of Critical Care, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

David O Okonkwo (DO)

Department of Neurological Surgery, University of Pittsburgh Medical Center Healthcare System, Pittsburgh, Pennsylvania, USA.

James F Castellano (JF)

Department of Neurology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

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