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Electrographic Seizures in Patients with Acute Encephalitis

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Abstract

Introduction

Clinical seizures and status epilepticus are frequent complications of encephalitis, can lead to depressed level of consciousness, and are associated with poor outcome. We sought to determine the frequency, risk factors, and clinical impact of electrographic seizures detected with continuing electroencephalography (cEEG) in patients with encephalitis and altered level of consciousness.

Methods

We retrospectively identified all patients with presumed or definite viral or autoimmune encephalitis who underwent cEEG monitoring at Henry Ford Hospital from January 2012 to October 2017. Clinical data and cEEG monitoring reports were abstracted and recorded. The primary outcome was electrographic seizures detected by cEEG.

Results

Of 1,735 patients who underwent a minimum of 12 h of cEEG monitoring, we identified 54 with a verified discharge diagnosis of encephalitis. Twenty-two of these patients (41%) had electrographic seizures on cEEG. Compared with encephalitis patients without seizures, electrographic seizures were associated with lower serum sodium levels (137 ± 5 vs 141 ± 7, P = 0.027) and more often were on antiepileptic therapy (100% vs 78%, P = 0.033) on the first day of monitoring. Seizures were also associated with a higher frequency of cortical imaging abnormalities (68% vs 28%, P = 0.005), lateralized periodic discharges (LPDs; 50% vs 16%, P = 0.014), delta background frequency (81% vs 45%, P = 0.010), low or suppressed voltage (96% vs 62%, P = 0.005), and focal slowing (86% vs 47%, P = 0.004). There was no association between electrographic seizures and clinical outcome at discharge.

Conclusion

Electrographic seizures occur in approximately 40% of patients with acute encephalitis. Low serum sodium, cortical imaging abnormalities, and on cEEG LPDs and background abnormalities are associated factors. The lack of association with short-term outcome suggests that with aggressive treatment, the clinical impact of electrographic seizures in encephalitis can be minimized.

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References

  1. Tunkel AR, Glaser CA, Bloch KC, Sejvar JJ, Marra CM, Roos KL, et al. The management of encephalitis: clinical practice guidelines by the infectious diseases society of America. Clin Infect Dis. 2008;47(3):303–27.

    Article  CAS  Google Scholar 

  2. Vora NM, Holman RC, Mehal JM, Steiner CA, Blanton J, Sejvar J. Burden of encephalitis-associated hospitalizations in the United States, 1998–2010. Neurology. 2014;82(5):443–51.

    Article  Google Scholar 

  3. Granerod J, Ambrose HE, Davies NW, Clewley JP, Walsh AL, Morgan D, et al. Causes of encephalitis and differences in their clinical presentations in England: a multicentre, population-based prospective study. Lancet Infect Dis. 2010;10(12):835–44.

    Article  Google Scholar 

  4. Thakur KT, Motta M, Asemota AO, Kirsch HL, Benavides DR, Schneider EB, et al. Predictors of outcome in acute encephalitis. Neurology. 2013;81(9):793–800.

    Article  Google Scholar 

  5. Singh TD, Fugate JE, Rabinstein AA. The spectrum of acute encephalitis: causes, management, and predictors of outcome. Neurology. 2015;84(4):359–66.

    Article  CAS  Google Scholar 

  6. Granerod J, Tam CC, Crowcroft NS, Davies NW, Borchert M, Thomas SL. Challenge of the unknown. A systematic review of acute encephalitis in non-outbreak situations. Neurology. 2010;75(10):924–32.

    Article  CAS  Google Scholar 

  7. Venkatesan A, Tunkel AR, Bloch KC, Lauring AS, Sejvar J, Bitnun A, et al. Case definitions, diagnostic algorithms, and priorities in encephalitis: consensus statement of the international encephalitis consortium. Clin Infect Dis. 2013;57(8):1114–28.

    Article  CAS  Google Scholar 

  8. Ney JP, van der Goes DN, Nuwer MR, Nelson L, Eccher MA. Continuous and routine EEG in intensive care: utilization and outcomes, United States 2005–2009. Neurology. 2013;81(23):2002–8.

    Article  Google Scholar 

  9. Billakota S, Sinha SR. Utility of continuous EEG monitoring in noncritically lll hospitalized patients. J Clin Neurophysiol. 2016;33(5):421–5.

    Article  Google Scholar 

  10. Carrera E, Claassen J, Oddo M, Emerson RG, Mayer SA, Hirsch LJ. Continuous electroencephalographic monitoring in critically ill patients with central nervous system infections. Arch Neurol. 2008;65(12):1612–8.

    Article  Google Scholar 

  11. Mittal MK, Rabinstein AA, Hocker SE, Pittock SJ, Wijdicks EF, McKeon A. Autoimmune encephalitis in the ICU: analysis of phenotypes, serologic findings, and outcomes. Neurocrit Care. 2016;24(2):240–50.

    Article  CAS  Google Scholar 

  12. Harris Paul A, Taylor Robert, Thielke Robert, Payne Jonathon, Gonzalez Nathaniel, Conde Jose G. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–81.

    Article  Google Scholar 

  13. Graus F, Titulaer MJ, Balu R, Benseler S, Bien CG, Cellucci T, et al. A clinical approach to diagnosis of autoimmune encephalitis. Lancet Neurol. 2016;15(4):391–404.

    Article  Google Scholar 

  14. Hirsch LJ, LaRoche SM, Gaspard N, Gerard E, Svoronos A, Herman ST, et al. American clinical neurophysiology society’s standardized critical care EEG terminology: 2012 version. J Clin Neurophysiol. 2013;30(1):1–27.

    Article  CAS  Google Scholar 

  15. Leitinger M, Beniczky S, Rohracher A, Gardella E, Kalss G, Qerama E, et al. Salzburg consensus criteria for non-convulsive status epilepticus—approach to clinical application. Epilepsy Behav. 2015;49:158–63.

    Article  CAS  Google Scholar 

  16. Hirsch LJ, Claassen J, Mayer SA, Emerson RG. Stimulus-induced rhythmic, periodic, or ictal discharges (SIRPIDs): a common EEG phenomenon in the critically ill. Epilepsia. 2004;45(2):109–23.

    Article  Google Scholar 

  17. Yoo JY, Rampal N, Petroff OA, Hirsch LJ, Gaspard N. Brief potentially ictal rhythmic discharges in critically ill adults. JAMA Neurol. 2014;71(4):454–62.

    Article  Google Scholar 

  18. Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet. 1975;1(7905):480–4.

    Article  CAS  Google Scholar 

  19. Sutter R, Kaplan PW, Cervenka MC, Thakur KT, Asemota AO, Venkatesan A, et al. Electroencephalography for diagnosis and prognosis of acute encephalitis. Clin Neurophysiol. 2015;126(8):1524–31.

    Article  Google Scholar 

  20. 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(10):1743–8.

    Article  CAS  Google Scholar 

  21. 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(12):1750–5.

    Article  Google Scholar 

  22. Sutter R, Fuhr P, Grize L, Marsch S, Ruegg S. Continuous video-EEG monitoring increases detection rate of nonconvulsive status epilepticus in the ICU. Epilepsia. 2011;52(3):453–7.

    Article  Google Scholar 

  23. Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ. Continuous electroencephalography in the medical intensive care unit. Crit Care Med. 2009;37(6):2051–6.

    Article  Google Scholar 

  24. Friedman D, Claassen J, Hirsch LJ. Continuous electroencephalogram monitoring in the intensive care unit. Anesth Analg. 2009;109(2):506–23.

    Article  Google Scholar 

  25. Sutter R, Stevens RD, Kaplan PW. Continuous electroencephalographic monitoring in critically ill patients: indications, limitations, and strategies. Crit Care Med. 2013;41(4):1124–32.

    Article  Google Scholar 

  26. Misra UK, Kalita J. Seizures in encephalitis: predictors and outcome. Seizure. 2009;18(8):583–7.

    Article  CAS  Google Scholar 

  27. Halawa I, Andersson T, Tomson T. Hyponatremia and risk of seizures: a retrospective cross-sectional study. Epilepsia. 2011;52(2):410–3.

    PubMed  Google Scholar 

  28. Adrogue HJ, Madias NE. The challenge of hyponatremia. J Am Soc Nephrol. 2012;23(7):1140–8.

    Article  CAS  Google Scholar 

  29. Overgaard-Steensen C, Ring T. Clinical review: practical approach to hyponatraemia and hypernatraemia in critically ill patients. Crit Care. 2013;17(1):206.

    Article  Google Scholar 

  30. Rodriguez Ruiz A, Vlachy J, Lee JW, Gilmore EJ, Ayer T, Haider HA, et al. Association of periodic and rhythmic electroencephalographic patterns with seizures in critically ill patients. JAMA Neurol. 2017;74(2):181–8.

    Article  Google Scholar 

  31. 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(10):1288–95.

    PubMed  Google Scholar 

  32. Punia V, Garcia CG, Hantus S. Incidence of recurrent seizures following hospital discharge in patients with LPDs (PLEDs) and nonconvulsive seizures recorded on continuous EEG in the critical care setting. Epilepsy Behav. 2015;49:250–4.

    Article  Google Scholar 

  33. Garcia-Morales I, Garcia MT, Galan-Davila L, Gomez-Escalonilla C, Saiz-Diaz R, Martinez-Salio A, et al. Periodic lateralized epileptiform discharges: etiology, clinical aspects, seizures, and evolution in 130 patients. J Clin Neurophysiol. 2002;19(2):172–7.

    Article  Google Scholar 

  34. Snodgrass SM, Tsuburaya K, Ajmone-Marsan C. Clinical significance of periodic lateralized epileptiform discharges: relationship with status epilepticus. J Clin Neurophysiol. 1989;6(2):159–72.

    Article  CAS  Google Scholar 

  35. Chatrian GE, Shaw CM, Leffman H. The significance of periodic lateralized epileptiform discharges in EEG: an electrographic, clinical, and pathological study. Electroencephalogr Clin Neurophysiol. 1964;17:177–93.

    Article  CAS  Google Scholar 

  36. Brigo F. Intermittent rhythmic delta activity patterns. Epilepsy Behav. 2011;20(2):254–6.

    Article  Google Scholar 

  37. Foreman B, Claassen J, Abou Khaled K, Jirsch J, Alschuler DM, Wittman J, et al. Generalized periodic discharges in the critically ill: a case-control study of 200 patients. Neurology. 2012;79(19):1951–60.

    Article  Google Scholar 

  38. Gaspard N, Gilmore EJ. Electroencephalography and evoked potentials. In: Louis ED, Mayer SA, Rowland LP, editors. Merritt’s neurology. 13th ed. Philadelphia: Wolters Kluwer; 2016. p. 206–15.

    Google Scholar 

  39. Swisher CB, Shah D, Sinha SR, Husain AM. Baseline EEG pattern on continuous ICU EEG monitoring and incidence of seizures. J Clin Neurophysiol. 2015;32(2):147–51.

    Article  Google Scholar 

  40. Abend NS, Arndt DH, Carpenter JL, Chapman KE, Cornett KM, Gallentine WB, et al. Electrographic seizures in pediatric ICU patients: cohort study of risk factors and mortality. Neurology. 2013;81(4):383–91.

    Article  Google Scholar 

  41. Chen JW, Wasterlain CG. Status epilepticus: pathophysiology and management in adults. Lancet Neurol. 2006;5(3):246–56.

    Article  Google Scholar 

  42. DeLorenzo RJ, Pellock JM, Towne AR, Boggs JG. Epidemiology of status epilepticus. J Clin Neurophysiol. 1995;12(4):316–25.

    Article  CAS  Google Scholar 

  43. Logroscino G, Hesdorffer DC, Cascino G, Annegers JF, Hauser WA. Short-term mortality after a first episode of status epilepticus. Epilepsia. 1997;38(12):1344–9.

    Article  CAS  Google Scholar 

  44. Kang BS, Kim DW, Kim KK, Moon HJ, Kim YS, Kim HK, et al. Prediction of mortality and functional outcome from status epilepticus and independent external validation of STESS and EMSE scores. Crit Care. 2016;20:25.

    Article  Google Scholar 

  45. Vooturi S, Jayalakshmi S, Sahu S, Mohandas S. Prognosis and predictors of outcome of refractory generalized convulsive status epilepticus in adults treated in neurointensive care unit. Clin Neurol Neurosurg. 2014;126:7–10.

    Article  Google Scholar 

  46. Kaplan PW. Assessing the outcomes in patients with nonconvulsive status epilepticus: nonconvulsive status epilepticus is underdiagnosed, potentially overtreated, and confounded by comorbidity. J Clin Neurophysiol. 1999;16(4):341–52 (discussion 53).

    Article  CAS  Google Scholar 

  47. Gaspard N, Hirsch LJ, LaRoche SM, Hahn CD, Westover MB. Interrater agreement for critical care EEG terminology. Epilepsia. 2014;55(9):1366–73.

    Article  Google Scholar 

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Funding

This study was funded by Educational and Research Fund from Department of Neurology of Henry Ford Hospital. Tanuwong Viarasilpa has received funding from Siriraj Hospital, Mahidol University, Bangkok, Thailand. The funding sources had no role in the collection, analysis, or interpretation of the data.

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Authors and Affiliations

  1. Department of Neurology, Henry Ford Hospital, 2799 W Grand Blvd, Detroit, MI, 48202, USA

    Tanuwong Viarasilpa, Nicha Panyavachiraporn, Gamaleldin Osman, Christopher Parres, Panayiotis Varelas & Stephan A. Mayer

  2. Division of Critical Care, Department of Medicine, Siriraj Hospital, Mahidol University, Bangkok, Thailand

    Tanuwong Viarasilpa & Nicha Panyavachiraporn

  3. Department of Public Health Sciences of Henry Ford Health System, Detroit, USA

    Meredith Van Harn

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  1. Tanuwong Viarasilpa
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Contributions

TV 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, performed data collection, analysis and interpretation, drafted and revised the manuscript. NP performed data collection, analysis and interpretation, assisted in drafting and revised the manuscript. GO performed data collection, data review and interpretation, and revised the manuscript. CP designed the study, performed data review and interpretation, and revised the manuscript. PV performed data collection and revised the manuscript. MVH performed the statistical analysis. SAM designed the study and data analysis, performed data review and interpretation, drafted and revised the manuscript. All authors have read and approved the final manuscript and agree to be accountable for all aspects of the work.

Corresponding author

Correspondence to Stephan A. Mayer.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

This study was approved by the Henry Ford Hospital Institutional Review Board.

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Viarasilpa, T., Panyavachiraporn, N., Osman, G. et al. Electrographic Seizures in Patients with Acute Encephalitis. Neurocrit Care 30, 207–215 (2019). https://doi.org/10.1007/s12028-018-0599-4

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