EEG monitoring duration to identify electroencephalographic seizures in critically ill children

France W Fung, Jiaxin Fan, Lisa Vala, Marin Jacobwitz, Darshana S Parikh, Maureen Donnelly, Alexis A Topjian, Rui Xiao, Nicholas S Abend, France W Fung, Jiaxin Fan, Lisa Vala, Marin Jacobwitz, Darshana S Parikh, Maureen Donnelly, Alexis A Topjian, Rui Xiao, Nicholas S Abend

Abstract

Objectives: To determine the optimal duration of continuous EEG monitoring (CEEG) for electrographic seizure (ES) identification in critically ill children.

Methods: We performed a prospective observational cohort study of 719 consecutive critically ill children with encephalopathy. We evaluated baseline clinical risk factors (age and prior clinically evident seizures) and emergent CEEG risk factors (epileptiform discharges and ictal-interictal continuum patterns) using a multistate survival model. For each subgroup, we determined the CEEG duration for which the risk of ES was <5% and <2%.

Results: ES occurred in 184 children (26%). Patients achieved <5% risk of ES after (1) 6 hours if ≥1 year without prior seizures or EEG risk factors; (2) 1 day if <1 year without prior seizures or EEG risks; (3) 1 day if ≥1 year with either prior seizures or EEG risks; (4) 2 days if ≥1 year with prior seizures and EEG risks; (5) 2 days if <1 year without prior seizures but with EEG risks; and (6) 2.5 days if <1 year with prior seizures regardless of the presence of EEG risks. Patients achieved <2% risk of ES at the same durations except patients without prior seizures or EEG risk factors would require longer CEEG (1.5 days if <1 year of age, 1 day if ≥1 year of age).

Conclusions: A model derived from 2 baseline clinical risk factors and emergent EEG risk factors would allow clinicians to implement personalized strategies that optimally target limited CEEG resources. This would enable more widespread use of CEEG-guided management as a potential neuroprotective strategy.

Clinicaltrialsgov identifier: NCT03419260.

© 2020 American Academy of Neurology.

Figures

Figure 1. Summary of the model states…
Figure 1. Summary of the model states (entry state, EEG risk state, and ES state) and transitions
Each participant could remain in the entry state, transition from the entry state to the electrographic seizures (ES) state, or transition from the entry state to the EEG risk state. Subjects in the EEG risk state could remain in the EEG risk state or transition to the ES state.
Figure 2. Swimmer plots and multistate survival…
Figure 2. Swimmer plots and multistate survival analysis results for the full cohort and each clinical risk state
Top row: swimmer plot showing the duration of continuous EEG monitoring (line length along x-axis) and state (entry = green; EEG risk = yellow; electrographic seizures [ES] = red) for each participant (y-axis). Middle row: proportion of participants in each state (entry, ES risk, ES) over time. Some participants remain in the same state over time (same color); some participants develop EEG risk factors but never experience ES (green to yellow transition); some participants experience ES without having experienced EEG risk factors (green to red transition); and some participants experience EEG risk factors and then ES (green to yellow to red transitions). Bottom row: remaining risk of transitioning to the ES state for patients in the entry (green) and EEG risk (yellow) states. Shaded areas represent the 95% confidence intervals. For the full cohort and each of the 4 clinical risk states, the risk of transitioning to the ES state remains higher over time for participants with EEG risk factors than those in the entry state.

References

    1. Jette N, Claassen J, Emerson RG, Hirsch LJ. Frequency and predictors of nonconvulsive seizures during continuous electroencephalographic monitoring in critically ill children. Arch Neurol 2006;63:1750–1755.
    1. Tay SK, Hirsch LJ, Leary L, Jette N, Wittman J, Akman CI. Nonconvulsive status epilepticus in children: clinical and EEG characteristics. Epilepsia 2006;47:1504–1509.
    1. Shahwan A, Bailey C, Shekerdemian L, Harvey AS. The prevalence of seizures in comatose children in the pediatric intensive care unit: a prospective video-EEG study. Epilepsia 2010;51:1198–1204.
    1. Abend NS, Topjian A, Ichord R, et al. . Electroencephalographic monitoring during hypothermia after pediatric cardiac arrest. Neurology 2009;72:1931–1940.
    1. Williams K, Jarrar R, Buchhalter J. Continuous video-EEG monitoring in pediatric intensive care units. Epilepsia 2011;52:1130–1136.
    1. Greiner HM, Holland K, Leach JL, Horn PS, Hershey AD, Rose DF. Nonconvulsive status epilepticus: the encephalopathic pediatric patient. Pediatrics 2012;129:e748–e755.
    1. Kirkham FJ, Wade AM, McElduff F, et al. . Seizures in 204 comatose children: incidence and outcome. Intensive Care Med 2012;38:853–862.
    1. 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;28:1925–1929.
    1. Piantino JA, Wainwright MS, Grimason M, et al. . Nonconvulsive seizures are common in children treated with extracorporeal cardiac life support. Pediatr Crit Care Med 2013;14:601–609.
    1. Abend NS, Arndt DH, Carpenter JL, et al. . Electrographic seizures in pediatric ICU patients: cohort study of risk factors and mortality. Neurology 2013;81:383–391.
    1. McCoy B, Sharma R, Ochi A, et al. . Predictors of nonconvulsive seizures among critically ill children. Epilepsia 2011;52:1973–1978.
    1. Schreiber JM, Zelleke T, Gaillard WD, Kaulas H, Dean N, Carpenter JL. Continuous video EEG for patients with acute encephalopathy in a pediatric intensive care unit. Neurocrit Care 2012;17:31–38.
    1. Arndt DH, Lerner JT, Matsumoto JH, et al. . Subclinical early posttraumatic seizures detected by continuous EEG monitoring in a consecutive pediatric cohort. Epilepsia 2013;54:1780–1788.
    1. Payne ET, Zhao XY, Frndova H, et al. . Seizure burden is independently associated with short term outcome in critically ill children. Brain 2014;137:1429–1438.
    1. Abend NS, Gutierrez-Colina AM, Topjian AA, et al. . Nonconvulsive seizures are common in critically ill children. Neurology 2011;76:1071–1077.
    1. Gold JJ, Crawford JR, Glaser C, Sheriff H, Wang S, Nespeca M. The role of continuous electroencephalography in childhood encephalitis. Pediatr Neurol 2014;50:318–323.
    1. Vlachy J, Jo M, Li Q, et al. . Risk factors for seizures among young children monitored with continuous electroencephalography in intensive care unit: a retrospective study. Front Pediatr 2018;6:303.
    1. Sansevere AJ, Duncan ED, Libenson MH, Loddenkemper T, Pearl PL, Tasker RC. Continuous EEG in pediatric critical care: yield and efficiency of seizure detection. J Clin Neurophysiol 2017;34:421–426.
    1. Sanchez Fernandez I, Sansevere AJ, Gainza-Lein M, Buraniqi E, Tasker RC, Loddenkemper T. Time to continuous electroencephalogram in repeated admissions to the pediatric intensive care unit. Seizure 2018;54:19–26.
    1. Sanchez SM, Arndt DH, Carpenter JL, et al. . Electroencephalography monitoring in critically ill children: current practice and implications for future study design. Epilepsia 2013;54:1419–1427.
    1. Topjian AA, Gutierrez-Colina AM, Sanchez SM, et al. . Electrographic status epilepticus is associated with mortality and worse short-term outcome in critically ill children. Crit Care Med 2013;41:215–223.
    1. Wagenman KL, Blake TP, Sanchez SM, et al. . Electrographic status epilepticus and long-term outcome in critically ill children. Neurology 2014;82:396–404.
    1. Hasbani DM, Topjian AA, Friess SH, et al. . Nonconvulsive electrographic seizures are common in children with abusive head trauma. Pediatr Crit Care Med 2013;14:709–715.
    1. 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;16:167–176.
    1. Vaewpanich J, Reuter-Rice K. Continuous electroencephalography in pediatric traumatic brain injury: seizure characteristics and outcomes. Epilepsy Behav 2016;62:225–230.
    1. Gwer S, Idro R, Fegan G, et al. . Continuous EEG monitoring in Kenyan children with non-traumatic coma. Arch Dis Child 2012;97:343–349.
    1. Ostendorf AP, Hartman ME, Friess SH. Early electroencephalographic findings correlate with neurologic outcome in children following cardiac arrest. Pediatr Crit Care Med 2016;17:667–676.
    1. Sanchez Fernandez I, Sansevere AJ, Guerriero RM, et al. . Time to electroencephalography is independently associated with outcome in critically ill neonates and children. Epilepsia 2017;58:420–428.
    1. Brophy GM, Bell R, Claassen J, et al. . Guidelines for the evaluation and management of status epilepticus. Neurocrit Care 2012;17:3–23.
    1. Herman ST, Abend NS, Bleck TP, et al. . Consensus statement on continuous EEG in critically ill adults and children, part I: indications. J Clin Neurophysiol 2015;32:87–95.
    1. Herman ST, Abend NS, Bleck TP, et al. . Consensus statement on continuous EEG in critically ill adults and children, part II: personnel, technical specifications, and clinical practice. J Clin Neurophysiol 2015;32:96–108.
    1. Sanchez SM, Carpenter J, Chapman KE, et al. . Pediatric ICU EEG monitoring: current resources and practice in the United States and Canada. J Clin Neurophysiol 2013;30:156–160.
    1. Gutierrez-Colina AM, Topjian AA, Dlugos DJ, Abend NS. EEG monitoring in critically ill children: indications and strategies. Pediatr Neurol 2012;46:158–161.
    1. Abend NS, Topjian AA, Williams S. How much does it cost to identify a critically ill child experiencing electrographic seizures? J Clin Neurophysiol 2015;32:257–264.
    1. Yang A, Arndt DH, Berg RA, et al. . Development and validation of a seizure prediction model in critically ill children. Seizure 2015;25:104–111.
    1. Fung FW, Jacobwitz M, Parikh DS, et al. . Development of a model to predict electroencephalographic seizures in critically ill children. Epilepsia 2020;61:498–508.
    1. Struck AF, Osman G, Rampal N, et al. . Time-dependent risk of seizures in critically ill patients on continuous electroencephalogram. Ann Neurol 2017;82:177–185.
    1. Claassen J, Mayer SA, Kowalski RG, Emerson RG, Hirsch LJ. Detection of electrographic seizures with continuous EEG monitoring in critically ill patients. Neurology 2004;62:1743–1748.
    1. von Elm E, Altman DG, Egger M, et al. . The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 2008;61:344–349.
    1. Children's Hospital of Philadelphia. Critical Care Pathway for EEG Monitoring [online]. Available at: . Accessed July 20, 2019.
    1. Hirsch LJ, LaRoche SM, Gaspard N, et al. . American Clinical Neurophysiology Society's standardized critical care EEG terminology: 2012 version. J Clin Neurophysiol 2013;30:1–27.
    1. Abend NS, Gutierrez-Colina A, Zhao H, et al. . Interobserver reproducibility of electroencephalogram interpretation in critically ill children. J Clin Neurophysiol 2011;28:15–19.
    1. Abend NS, Wiebe DJ, Xiao R, et al. . EEG factors after pediatric cardiac arrest. J Clin Neurophysiol 2018;35:251–255.
    1. Abend NS, Xiao R, Kessler SK, Topjian AA. Stability of early EEG background patterns after pediatric cardiac arrest. J Clin Neurophysiol 2018;35:246–250.
    1. Beniczky S, Hirsch LJ, Kaplan PW, et al. . Unified EEG terminology and criteria for nonconvulsive status epilepticus. Epilepsia 2013;54(suppl 6):28–29.
    1. de Wreede LC, Fiocco M, Putter H. The mstate package for estimation and prediction in non- and semi-parametric multi-state and competing risks models. Comput Methods Programs Biomed 2010;99:261–274.
    1. Struck AF, Ustun B, Ruiz AR, et al. . Association of an electroencephalography-based risk score with seizure probability in hospitalized patients. JAMA Neurol 2017;74:1419–1424.
    1. Fung FW, Jacobwitz M, Vala L, et al. . Electroencephalographic seizures in critically ill children: management and adverse events. Epilepsia 2019;60:2095–2104.
    1. Abend NS, Sanchez SM, Berg RA, Dlugos DJ, Topjian AA. Treatment of electrographic seizures and status epilepticus in critically ill children: a single center experience. Seizure 2013;22:467–471.
    1. Westover MB, Shafi MM, Bianchi MT, et al. . The probability of seizures during EEG monitoring in critically ill adults. Clin Neurophysiol 2015;126:463–471.

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