J Pediatr Intensive Care 2024; 13(04): 364-371
DOI: 10.1055/s-0042-1743500
Original Article

Associations between Electroencephalographic Variables, Early Post-Traumatic Seizure Risk, and Outcomes following Pediatric Severe Traumatic Brain Injury

1   Division of Critical Care Medicine, Department of Pediatrics, Cohen Children's Medical Center, Zucker School of Medicine at Hofstra/Northwell, New Hyde Park, New York, United States
,
Lauren Villo
2   Division of Critical Care Medicine, Department of Pediatrics, Atrium Health Navicent, Mercer University, Macon, Georgia, United States
,
Mariah Eisner
3   Department of Biomedical Informatics, Center for Biostatistics, The Ohio State University, Columbus, Ohio, United States
,
Marlina E. Lovett
4   Division of Critical Care Medicine, Department of Pediatrics, The Ohio State University, Nationwide Children's Hospital, Columbus, Ohio, United States
,
Melissa G. Chung
4   Division of Critical Care Medicine, Department of Pediatrics, The Ohio State University, Nationwide Children's Hospital, Columbus, Ohio, United States
5   Division of Neurology, Department of Pediatrics, The Ohio State University, Nationwide Children's Hospital, Columbus, Ohio, United States
,
Nicole F. O'Brien
4   Division of Critical Care Medicine, Department of Pediatrics, The Ohio State University, Nationwide Children's Hospital, Columbus, Ohio, United States
,
Eric A. Sribnick
6   Division of Neurological Surgery, The Ohio State University, Nationwide Children's Hospital, Columbus, Ohio, United States
,
Adam P. Ostendorf
5   Division of Neurology, Department of Pediatrics, The Ohio State University, Nationwide Children's Hospital, Columbus, Ohio, United States
› Author Affiliations
Funding None.

Abstract

Early post-traumatic seizures (PTS) are associated with worse outcomes in children with traumatic brain injury (TBI). Our aim was to identify the association between continuous electroencephalogram (cEEG) characteristics and early PTS risk following pediatric severe TBI. We also evaluated the relationship between cEEG background features and outcomes. A single-center retrospective cohort study was performed on children between 0 and 18 years of age admitted to the pediatric intensive care unit from 2016 to 2019 with severe TBI and cEEG monitoring within 7 days of injury. Raw cEEG tracings were reviewed by an epileptologist in accordance with American Clinical Neurophysiology Society (ACNS) Critical Care EEG terminology. Univariate comparisons were made between children with and without early PTS, as well as between those with and without varying cEEG background features. Eighteen children (31%) of the 59 included had early PTS. Interictal abnormalities, inclusive of sporadic spikes and sharp waves, rhythmic delta activity, or lateralized periodic discharges (LPDs) were more common among children with seizures (100 vs. 22%; p < 0.01). LPDs were also more common in the seizure group (44 vs. 2%; p < 0.01). Background discontinuity was associated with worse Glasgow Outcome Scale—Extended Pediatric Version (GOS-E Peds) scores at discharge and 3-, 6-, and 12-month post-discharge (p < 0.01). Lack of reactivity was also associated with worse GOS-E Peds scores at 3-, 6-, and 12-month post-discharge (p < 0.01). Interictal abnormalities and LPDs were each associated with early PTS following pediatric severe TBI. Larger studies should evaluate if high-risk patients would benefit from prolonged cEEG monitoring and/or more aggressive anti-seizure prophylaxis. Discontinuity and lack of variability were associated with worse outcomes. Future studies should attempt to clarify their role as potential early markers of prognosis.



Publication History

Received: 17 September 2021

Accepted: 26 January 2022

Article published online:
28 February 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
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  • References

  • 1 Vaewpanich J, Reuter-Rice K. Continuous electroencephalography in pediatric traumatic brain injury: seizure characteristics and outcomes. Epilepsy Behav 2016; 62: 225-230
  • 2 Bennett KS, DeWitt PE, Harlaar N, Bennett TD. Seizures in children with severe traumatic brain injury. Pediatr Crit Care Med 2017; 18 (01) 54-63
  • 3 Arndt DH, Goodkin HP, Giza CC. Early Posttraumatic seizures in the pediatric population. J Child Neurol 2016; 31 (01) 46-56
  • 4 Chung MG, O'Brien NF. Prevalence of early posttraumatic seizures in children with moderate to severe traumatic brain injury despite levetiracetam prophylaxis. Pediatr Crit Care Med 2016; 17 (02) 150-156
  • 5 Johnson AR, DeMatt E, Salorio CF. Predictors of outcome following acquired brain injury in children. Dev Disabil Res Rev 2009; 15 (02) 124-132
  • 6 Kurz JE, Poloyac SM, Abend NS, Fabio A, Bell MJ, Wainwright MS. Investigators for the Approaches and Decisions in Acute Pediatric TBI Trial. Variation in anticonvulsant selection and electroencephalographic monitoring following severe traumatic brain injury in children-understanding resource availability in sites participating in a comparative effectiveness study. Pediatr Crit Care Med 2016; 17 (07) 649-657
  • 7 Chiaretti A, Piastra M, Pulitanò S. et al. Prognostic factors and outcome of children with severe head injury: an 8-year experience. Childs Nerv Syst 2002; 18 (3-4): 129-136
  • 8 Arango JI, Deibert CP, Brown D, Bell M, Dvorchik I, Adelson PD. Posttraumatic seizures in children with severe traumatic brain injury. Childs Nerv Syst 2012; 28 (11) 1925-1929
  • 9 Vespa PM, Nuwer MR, Nenov V. et al. Increased incidence and impact of nonconvulsive and convulsive seizures after traumatic brain injury as detected by continuous electroencephalographic monitoring. J Neurosurg 1999; 91 (05) 750-760
  • 10 Arndt DH, Lerner JT, Matsumoto JH. et al. Subclinical early posttraumatic seizures detected by continuous EEG monitoring in a consecutive pediatric cohort. Epilepsia 2013; 54 (10) 1780-1788
  • 11 O'Neill BR, Handler MH, Tong S, Chapman KE. Incidence of seizures on continuous EEG monitoring following traumatic brain injury in children. J Neurosurg Pediatr 2015; 16 (02) 167-176
  • 12 Herman ST, Abend NS, Bleck TP. et al; Critical Care Continuous EEG Task Force of the American Clinical Neurophysiology Society. Consensus statement on continuous EEG in critically ill adults and children, part I: indications. J Clin Neurophysiol 2015; 32 (02) 87-95
  • 13 Kochanek PM, Tasker RC, Bell MJ. et al. Management of pediatric severe traumatic brain injury: 2019 consensus and guidelines-based algorithm for first and second tier therapies. Pediatr Crit Care Med 2019; 20 (03) 269-279
  • 14 Ruzas CM, DeWitt PE, Bennett KS, Chapman KE, Harlaar N, Bennett TD. EEG monitoring and antiepileptic drugs in children with severe TBI. Neurocrit Care 2017; 26 (02) 256-266
  • 15 Lee H, Mizrahi MA, Hartings JA. et al. Continuous electroencephalography after moderate to severe traumatic brain injury. Crit Care Med 2019; 47 (04) 574-582
  • 16 Beers SR, Wisniewski SR, Garcia-Filion P. et al. Validity of a pediatric version of the Glasgow Outcome Scale-Extended. J Neurotrauma 2012; 29 (06) 1126-1139
  • 17 Hirsch LJ, LaRoche SM, Gaspard N. et al. American Clinical Neurophysiology Society's Standardized Critical Care EEG Terminology: 2012 version. J Clin Neurophysiol 2013; 30 (01) 1-27
  • 18 Lewis RJ, Yee L, Inkelis SH, Gilmore D. Clinical predictors of post-traumatic seizures in children with head trauma. Ann Emerg Med 1993; 22 (07) 1114-1118
  • 19 Ruiz AR, Vlachy J, Lee JW. et al; Critical Care EEG Monitoring Research Consortium. Association of periodic and rhythmic electroencephalographic patterns with seizures in critically ill patients. JAMA Neurol 2017; 74 (02) 181-188
  • 20 Newey CR, Kinzy TG, Punia V, Hantus S. Continuous electroencephalography in the critically ill: clinical and continuous electroencephalography markers for targeted monitoring. J Clin Neurophysiol 2018; 35 (04) 325-331
  • 21 Struck AF, Ustun B, Ruiz AR. et al. Association of an electroencephalography-based risk score with seizure probability in hospitalized patients. JAMA Neurol 2017; 74 (12) 1419-1424
  • 22 Jing J, Sun H, Kim JA. et al. Development of expert-level automated detection of epileptiform discharges during electroencephalogram interpretation. JAMA Neurol 2020; 77 (01) 103-108
  • 23 Topjian AA, Sánchez SM, Shults J, Berg RA, Dlugos DJ, Abend NS. Early electroencephalographic background features predict outcomes in children resuscitated from cardiac arrest. Pediatr Crit Care Med 2016; 17 (06) 547-557
  • 24 Yoon SY, Choi YJ, Park SH, Hwang JH, Hwang SK. Traumatic brain injury in children under age 24 months: analysis of demographic data, risk factors, and outcomes of post-traumatic seizure. J Korean Neurosurg Soc 2017; 60 (05) 584-590
  • 25 Rumalla K, Smith KA, Letchuman V, Gandham M, Kombathula R, Arnold PM. Nationwide incidence and risk factors for posttraumatic seizures in children with traumatic brain injury. J Neurosurg Pediatr 2018; 22 (06) 684-693
  • 26 Huth SF, Slater A, Waak M, Barlow K, Raman S. Predicting neurological recovery after traumatic brain injury in children: a systematic review of prognostic models. J Neurotrauma 2020; 37 (20) 2141-2149
  • 27 Maas AI, Marmarou A, Murray GD, Teasdale SG, Steyerberg EW. Prognosis and clinical trial design in traumatic brain injury: the IMPACT study. J Neurotrauma 2007; 24 (02) 232-238