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Neurocritical Care

, Volume 29, Issue 3, pp 388–395 | Cite as

Early Epileptiform Discharges and Clinical Signs Predict Nonconvulsive Status Epilepticus on Continuous EEG

  • Johannes Koren
  • Johannes Herta
  • Simone Draschtak
  • Georg Pötzl
  • Franz Fürbass
  • Manfred Hartmann
  • Tilmann Kluge
  • Andreas Gruber
  • Christoph Baumgartner
Original Article

Abstract

Background

Critical care continuous electroencephalography (CCEEG) represents the gold standard for detection of nonconvulsive status epilepticus (NCSE) in neurological critical care patients. It is unclear which findings on short-term routine EEG and which clinical parameters predict NCSE during subsequent CCEEG reliably. The aim of the present study was to assess the prognostic significance of changes within the first 30 min of EEG as well as of clinical parameters for the occurrence of NCSE during subsequent CCEEG.

Methods

Systematic analysis of the first 30 min and the remaining segments of prospective CCEEG recordings according to the ACNS Standardized Critical Care EEG Terminology and according to recently proposed NCSE criteria as well as review of clinical parameters of 85 consecutive neurological critical care patients. Logistic regression and binary classification tests were used to determine the most useful parameters within the first 30 min of EEG predicting subsequent NCSE.

Results

The presence of early sporadic epileptiform discharges (SED) and early rhythmic or periodic EEG patterns of “ictal–interictal uncertainty” (RPPIIIU) (OR 15.51, 95% CI 2.83–84.84, p = 0.002) and clinical signs of NCS (OR 18.43, 95% CI 2.06–164.62, p = 0.009) predicted NCSE on subsequent CCEEG. Various combinations of early SED, early RPPIIIU, and clinical signs of NCS showed sensitivities of 79–100%, specificities of 49–89%, and negative predictive values of 95–100% regarding the incidence of subsequent NCSE (p < 0.001).

Conclusions

Early SED and early RPPIIIU within the first 30 min of EEG as well as clinical signs of NCS predict the occurrence of NCSE during subsequent CCEEG with high sensitivity and high negative predictive value and may be useful to select patients who should undergo CCEEG.

Keywords

Early epileptiform discharges Ictal–interictal continuum Nonconvulsive status epilepticus Standardized Critical Care EEG Terminology EEG in critical care patients 

Abbreviations

ACNS

American Clinical Neurophysiology Society

CCEEG

Critical care continuous electroencephalography

EEG

Electroencephalography

ED

Epileptiform discharges

GCS

Glasgow Coma Scale

ICU

Intensive care unit

NCS

Nonconvulsive seizures

NCSE

Nonconvulsive status epilepticus

NPV

Negative predictive value

OR

Odds ratio

PD

Periodic discharges

RDA

Rhythmic delta activity

RPPIIIU

Rhythmic and periodic EEG patterns of “ictal–interictal uncertainty”

SCCET

Standardized Critical Care EEG Terminology

SE

Status epilepticus

SED

Sporadic epileptiform discharges

Notes

Acknowledgements

We thank the attending physicians and neurology residents of the Neurological Department, General Hospital Hietzing with Neurological Center Rosenhuegel, for their overall support of this project. We like to thank Sofija Kopitovic, Ingeborg Moser, and Sandra Zeckl for their contribution and help during EEG data acquisition and processing.

Author Contributions

JK participated in study idea, clinical and EEG data analysis, statistical analysis, preparing and modifying manuscript. JH participated in study idea, clinical and EEG data analysis, and modifying manuscript. SD, GP participated in clinical data analysis and modifying manuscript. FF, MH, CB participated in study idea, EEG data analysis, and modifying manuscript. TK, AG participated in study idea and modifying manuscript.

Statistical Testing

Johannes Koren had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Source of Support

This study was supported by the FFG—Austrian Research Promotion Agency grant 826816 (EpiMon). Johannes Koren and Johannes Herta were both partially supported by the FFG grant.

Compliance with Ethical Standards

Conflict of interest

All listed authors do not have any conflict of interest in regard to the content of this study. We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

Ethical Approval

The study protocol was approved by the institutional ethics commission. Patients included in the present study were mainly not able to give consent during EEG recordings. Therefore, the ethics commission requested that all patients that were not able to give consent and their relatives receive a written patient information and/or were informed about the study and the possibility to withdraw their personal data in the future.

References

  1. 1.
    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.CrossRefPubMedGoogle Scholar
  2. 2.
    Chong DJ, Hirsch LJ. Which EEG patterns warrant treatment in the critically ill? Reviewing the evidence for treatment of periodic epileptiform discharges and related patterns. J Clin Neurophysiol. 2005;22:79–91.CrossRefPubMedGoogle Scholar
  3. 3.
    Claassen J, Mayer SA, Kowalski RG, Emerson RG, Hirsch LJ. Detection of electrographic seizures with continuous EEG monitoring in critically ill patients. Neurology. 2004;62:1743–8.CrossRefPubMedGoogle Scholar
  4. 4.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Claassen J, Perotte A, Albers D, et al. Nonconvulsive seizures after subarachnoid hemorrhage: multimodal detection and outcomes. Ann Neurol. 2013;74:53–64.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Bauer G, Trinka E. Nonconvulsive status epilepticus and coma. Epilepsia. 2010;51:177–90.CrossRefPubMedGoogle Scholar
  7. 7.
    Sivaraju A, Gilmore EJ. Understanding and managing the ictal-interictal continuum in neurocritical care. Curr Treat Options Neurol. 2016;18:8.CrossRefPubMedGoogle Scholar
  8. 8.
    Sutter R, Semmlack S, Kaplan PW. Nonconvulsive status epilepticus in adults—insights into the invisible. Nat Rev Neurol. 2016;12:281–93.CrossRefPubMedGoogle Scholar
  9. 9.
    Young GB, Jordan KG, Doig GS. An assessment of nonconvulsive seizures in the intensive care unit using continuous EEG monitoring: an investigation of variables associated with mortality. Neurology. 1996;47:83–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Vespa PM, O’Phelan K, Shah M, et al. Acute seizures after intracerebral hemorrhage: a factor in progressive midline shift and outcome. Neurology. 2003;60:1441–6.CrossRefPubMedGoogle Scholar
  11. 11.
    Trinka E, Leitinger M. Which EEG patterns in coma are nonconvulsive status epilepticus? Epilepsy Behav. 2015;49:203–22.CrossRefPubMedGoogle Scholar
  12. 12.
    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.CrossRefPubMedGoogle Scholar
  13. 13.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Shafi MM, Westover MB, Cole AJ, Kilbride RD, Hoch DB, Cash SS. Absence of early epileptiform abnormalities predicts lack of seizures on continuous EEG. Neurology. 2012;79:1796–801.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Koren J, Herta J, Draschtak S, et al. Prediction of rhythmic and periodic EEG patterns and seizures on continuous EEG with early epileptiform discharges. Epilepsy Behav. 2015;49:286–9.CrossRefPubMedGoogle Scholar
  16. 16.
    Westover MB, Shafi MM, Bianchi MT, et al. The probability of seizures during EEG monitoring in critically ill adults. Clin Neurophysiol. 2015;126:463–71.CrossRefPubMedGoogle Scholar
  17. 17.
    Husain AM, Horn GJ, Jacobson MP. Non-convulsive status epilepticus: usefulness of clinical features in selecting patients for urgent EEG. J Neurol Neurosurg Psychiatry. 2003;74:189–91.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Koren JP, Herta J, Pirker S, et al. Rhythmic and periodic EEG patterns of ‘ictal-interictal uncertainty’ in critically ill neurological patients. Clin Neurophysiol. 2016;127:1176–81.CrossRefPubMedGoogle Scholar
  19. 19.
    Herta J, Koren J, Furbass F, et al. Prospective assessment and validation of rhythmic and periodic pattern detection in NeuroTrend: a new approach for screening continuous EEG in the intensive care unit. Epilepsy Behav. 2015;49:273–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Rodriguez Ruiz A, Vlachy J, Lee JW, et al. Association of periodic and rhythmic electroencephalographic patterns with seizures in critically ill patients. JAMA Neurol. 2017;74:181–8.CrossRefPubMedGoogle Scholar
  21. 21.
    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;56:1515–23.CrossRefPubMedGoogle Scholar
  22. 22.
    Bursac Z, Gauss CH, Williams DK, Hosmer DW. Purposeful selection of variables in logistic regression. Source Code Biol Med. 2008;3:17.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Calculation for the Chi square test: an interactive calculation tool for Chi square tests of goodness of fit and independence [Computer software]. Available from http://quantpsy.org. 2017.
  24. 24.
    Snodgrass SM, Tsuburaya K, Ajmone-Marsan C. Clinical significance of periodic lateralized epileptiform discharges: relationship with status epilepticus. J Clin Neurophysiol. 1989;6:159–72.CrossRefPubMedGoogle Scholar
  25. 25.
    Reiher J, Rivest J, Grand’Maison F, Leduc CP. Periodic lateralized epileptiform discharges with transitional rhythmic discharges: association with seizures. Electroencephalogr Clin Neurophysiol. 1991;78:12–7.CrossRefPubMedGoogle Scholar
  26. 26.
    Husain AM, Mebust KA, Radtke RA. Generalized periodic epileptiform discharges: etiologies, relationship to status epilepticus, and prognosis. J Clin Neurophysiol. 1999;16:51–8.CrossRefPubMedGoogle Scholar
  27. 27.
    Foreman B, Claassen J, Abou Khaled K, et al. Generalized periodic discharges in the critically ill: a case-control study of 200 patients. Neurology. 2012;79:1951–60.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Crepeau AZ, Kerrigan JF, Gerber P, et al. Rhythmical and periodic EEG patterns do not predict short-term outcome in critically ill patients with subarachnoid hemorrhage. J Clin Neurophysiol. 2013;30:247–54.CrossRefPubMedGoogle Scholar
  29. 29.
    Gaspard N, Manganas L, Rampal N, Petroff OA, Hirsch LJ. Similarity of lateralized rhythmic delta activity to periodic lateralized epileptiform discharges in critically ill patients. JAMA Neurol. 2013;70:1288–95.PubMedGoogle Scholar
  30. 30.
    Privitera M, Hoffman M, Moore JL, Jester D. EEG detection of nontonic-clonic status epilepticus in patients with altered consciousness. Epilepsy Res. 1994;18:155–66.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society 2018

Authors and Affiliations

  • Johannes Koren
    • 1
    • 2
  • Johannes Herta
    • 3
  • Simone Draschtak
    • 2
  • Georg Pötzl
    • 2
  • Franz Fürbass
    • 4
  • Manfred Hartmann
    • 4
  • Tilmann Kluge
    • 4
  • Andreas Gruber
    • 3
    • 5
  • Christoph Baumgartner
    • 1
    • 2
    • 6
  1. 1.Karl Landsteiner Institute for Clinical Epilepsy Research and Cognitive NeurologyViennaAustria
  2. 2.Department of NeurologyGeneral Hospital Hietzing with Neurological Center RosenhügelViennaAustria
  3. 3.Department of NeurosurgeryMedical University of ViennaViennaAustria
  4. 4.Center for Health and BioresourcesAIT Austrian Institute of Technology GmbHViennaAustria
  5. 5.Department of NeurosurgeryKepler University HospitalLinzAustria
  6. 6.Medical FacultySigmund Freud UniversityViennaAustria

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