Semin Respir Crit Care Med 2017; 38(06): 793-806
DOI: 10.1055/s-0037-1607987
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Ictal-Interictal Continuum: When to Worry About the Continuous Electroencephalography Pattern

Justine Cormier
1   Department of Neurology, Yale University School of Medicine, New Haven, Connecticut
,
Carolina B. Maciel
1   Department of Neurology, Yale University School of Medicine, New Haven, Connecticut
2   Department of Neurology, UF Health Shands Hospital, University of Florida College of Medicine, Gainesville, Florida
,
Emily J. Gilmore
1   Department of Neurology, Yale University School of Medicine, New Haven, Connecticut
3   Division of Neurocritical Care and Emergency Neurology, Department of Neurology, Yale University School of Medicine, New Haven, Connecticut
› Author Affiliations
Further Information

Publication History

Publication Date:
20 December 2017 (online)

Abstract

Continuous electroencephalography (cEEG) monitoring is an invaluable tool in the evaluation of encephalopathy and coma in critically ill patients. Marked increases in cEEG monitoring, coinciding with several societal guideline statements in the last decade, have allowed earlier detection and treatment of clearly harmful patterns, including nonconvulsive seizures (NCSz) and nonconvulsive status epilepticus (NCSE). However, it has also unmasked a range of EEG patterns of less clear clinical significance, with some more “malignant” than others given their potential association with increased neuronal stress and secondary brain injury. These patterns lay on a spectrum often referred to as the ictal-interictal continuum (IIC). To date, no definitive guidelines exist for the management of these potentially harmful EEG patterns, thus presenting a clinical dilemma for critical care physicians. Here, we review the various IIC patterns, their associated features, seizure risk, and outcomes and also propose a clinical approach to management based on the available data and expert opinion.

 
  • References

  • 1 Abend NS, Dlugos DJ, Hahn CD, Hirsch LJ, Herman ST. Use of EEG monitoring and management of non-convulsive seizures in critically ill patients: a survey of neurologists. Neurocrit Care 2010; 12 (03) 382-389
  • 2 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
  • 3 Claassen J, Taccone FS, Horn P, Holtkamp M, Stocchetti N, Oddo M. ; Neurointensive Care Section of the European Society of Intensive Care Medicine. Recommendations on the use of EEG monitoring in critically ill patients: consensus statement from the neurointensive care section of the ESICM. Intensive Care Med 2013; 39 (08) 1337-1351
  • 4 Brophy GM, Bell R, Claassen J. , et al; Neurocritical Care Society Status Epilepticus Guideline Writing Committee. Guidelines for the evaluation and management of status epilepticus. Neurocrit Care 2012; 17 (01) 3-23
  • 5 Pandian JD, Cascino GD, So EL, Manno E, Fulgham JR. Digital video-electroencephalographic monitoring in the neurological-neurosurgical intensive care unit: clinical features and outcome. Arch Neurol 2004; 61 (07) 1090-1094
  • 6 De Marchis GM, Pugin D, Meyers E. , et al. Seizure burden in subarachnoid hemorrhage associated with functional and cognitive outcome. Neurology 2016; 86 (03) 253-260
  • 7 Payne ET, Zhao XY, Frndova H. , et al. Seizure burden is independently associated with short term outcome in critically ill children. Brain 2014; 137 (Pt 5): 1429-1438
  • 8 Wagenman KL, Blake TP, Sanchez SM. , et al. Electrographic status epilepticus and long-term outcome in critically ill children. Neurology 2014; 82 (05) 396-404
  • 9 Rush B, Wiskar K, Fruhstorfer C, Hertz P. Association between seizures and mortality in patients with aneurysmal subarachnoid hemorrhage: A nationwide retrospective cohort analysis. Seizure 2016; 41: 66-69
  • 10 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: 250-254
  • 11 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) 1743-1748
  • 12 Claassen J, Perotte A, Albers D. , et al. Nonconvulsive seizures after subarachnoid hemorrhage: Multimodal detection and outcomes. Ann Neurol 2013; 74 (01) 53-64
  • 13 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
  • 14 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 (02) 79-91
  • 15 Gaspard N, Hirsch LJ, LaRoche SM, Hahn CD, Westover MB. ; Critical Care EEG Monitoring Research Consortium. Interrater agreement for critical care EEG terminology. Epilepsia 2014; 55 (09) 1366-1373
  • 16 Foreman B, Mahulikar A, Tadi P. , et al; Critical Care EEG Monitoring Research Consortium (CCEMRC). Generalized periodic discharges and ‘triphasic waves’: A blinded evaluation of inter-rater agreement and clinical significance. Clin Neurophysiol 2016; 127 (02) 1073-1080
  • 17 Beniczky S, Hirsch LJ, Kaplan PW. , et al. Unified EEG terminology and criteria for nonconvulsive status epilepticus. Epilepsia 2013; 54 (Suppl. 06) 28-29
  • 18 Leitinger M, Beniczky S, Rohracher A. , et al. Salzburg consensus criteria for non-convulsive status epilepticus--approach to clinical application. Epilepsy Behav 2015; 49: 158-163
  • 19 Hirsch LJ. Classification of EEG patterns in patients with impaired consciousness. Epilepsia 2011; 52 (Suppl. 08) 21-24
  • 20 Newey CR, Sahota P, Hantus S. Electrographic features of lateralized periodic discharges stratify risk in the interictal-ictal continuum. J Clin Neurophysiol 2017; 34 (04) 365-369
  • 21 Pohlmann-Eden B, Hoch DB, Cochius JI, Chiappa KH. Periodic lateralized epileptiform discharges--a critical review. J Clin Neurophysiol 1996; 13 (06) 519-530
  • 22 Fitzpatrick W, Lowry N. PLEDs: clinical correlates. Can J Neurol Sci 2007; 34 (04) 443-450
  • 23 Lee JW, LaRoche S, Choi H. , et al; Critical Care EEG Monitoring Research Consortium (CCEMRC). Development and feasibility testing of a critical care EEG monitoring database for standardized clinical reporting and multicenter collaborative research. J Clin Neurophysiol 2016; 33 (02) 133-140
  • 24 Sen-Gupta I, Schuele SU, Macken MP, Kwasny MJ, Gerard EE. “Ictal” lateralized periodic discharges. Epilepsy Behav 2014; 36: 165-170
  • 25 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 (02) 147-151
  • 26 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) 1288-1295
  • 27 Orta DS, Chiappa KH, Quiroz AZ, Costello DJ, Cole AJ. Prognostic implications of periodic epileptiform discharges. Arch Neurol 2009; 66 (08) 985-991
  • 28 Gurer G, Yemisci M, Saygi S, Ciger A. Structural lesions in periodic lateralized epileptiform discharges (PLEDs). Clin EEG Neurosci 2004; 35 (02) 88-93
  • 29 San-Juan OD, Chiappa KH, Costello DJ, Cole AJ. Periodic epileptiform discharges in hypoxic encephalopathy: BiPLEDs and GPEDs as a poor prognosis for survival. Seizure 2009; 18 (05) 365-368
  • 30 Walsh JM, Brenner RP. Periodic lateralized epileptiform discharges--long-term outcome in adults. Epilepsia 1987; 28 (05) 533-536
  • 31 Li HT, Wu T, Lin WR. , et al. Clinical correlation and prognostic implication of periodic EEG patterns: A cohort study. Epilepsy Res 2017; 131: 44-50
  • 32 Claassen J, Jetté N, Chum F. , et al. Electrographic seizures and periodic discharges after intracerebral hemorrhage. Neurology 2007; 69 (13) 1356-1365
  • 33 García-Morales I, García MT, Galán-Dávila L. , et al. Periodic lateralized epileptiform discharges: etiology, clinical aspects, seizures, and evolution in 130 patients. J Clin Neurophysiol 2002; 19 (02) 172-177
  • 34 Hartings JA, Williams AJ, Tortella FC. Occurrence of nonconvulsive seizures, periodic epileptiform discharges, and intermittent rhythmic delta activity in rat focal ischemia. Exp Neurol 2003; 179 (02) 139-149
  • 35 Gross DW, Quesney LF, Sadikot AF. Chronic periodic lateralized epileptiform discharges during sleep in a patient with caudate nucleus atrophy: insights into the anatomical circuitry of PLEDs. Electroencephalogr Clin Neurophysiol 1998; 107 (06) 434-438
  • 36 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: 177-193
  • 37 Téllez-Zenteno JF, Pillai SN, Hill MD, Pillay N. Chronic PLEDs with transitional rhythmic discharges (PLEDs-plus) in remote stroke. Epileptic Disord 2007; 9 (02) 164-169
  • 38 de la Paz D, Brenner RP. Bilateral independent periodic lateralized epileptiform discharges. Clinical significance. Arch Neurol 1981; 38 (11) 713-715
  • 39 Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ. Continuous electroencephalography in the medical intensive care unit. Crit Care Med 2009; 37 (06) 2051-2056
  • 40 Gilmore EJ, Gaspard N, Choi HA. , et al. Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring. Intensive Care Med 2015; 41 (04) 686-694
  • 41 Kurtz P, Gaspard N, Wahl AS. , et al. Continuous electroencephalography in a surgical intensive care unit. Intensive Care Med 2014; 40 (02) 228-234
  • 42 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 (01) 12-17
  • 43 Rodriguez Ruiz A, 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
  • 44 Kim JA, Rosenthal ES, Biswal S. , et al. Epileptiform abnormalities predict delayed cerebral ischemia in subarachnoid hemorrhage. Clin Neurophysiol 2017; 128 (06) 1091-1099
  • 45 Terzano MG, Parrino L, Mazzucchi A, Moretti G. Confusional states with periodic lateralized epileptiform discharges (PLEDs): a peculiar epileptic syndrome in the elderly. Epilepsia 1986; 27 (04) 446-457
  • 46 Beaumanoir A, André-Obadia N, Nahory A, Zerbi D. Special types of periodic lateralized epileptiform discharges associated with confusional state in cerebral circulation insufficiency. Electroencephalogr Clin Neurophysiol 1996; 99 (03) 287-292
  • 47 Drury I, Klass DW, Westmoreland BF, Sharbrough FW. An acute syndrome with psychiatric symptoms and EEG abnormalities. Neurology 1985; 35 (06) 911-914
  • 48 Sivaraju A, Gilmore EJ. Understanding and managing the ictal-interictal continuum in neurocritical care. Curr Treat Options Neurol 2016; 18 (02) 8
  • 49 Sainju RK, Manganas LN, Gilmore EJ. , et al. Clinical correlates and prognostic significance of lateralized periodic discharges in patients without acute or progressive brain injury: a case-control study. J Clin Neurophysiol 2015; 32 (06) 495-500
  • 50 Claassen J. How I treat patients with EEG patterns on the ictal-interictal continuum in the neuro ICU. Neurocrit Care 2009; 11 (03) 437-444
  • 51 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) 1612-1618
  • 52 Pedersen GL, Rasmussen SB, Gyllenborg J, Benedek K, Lauritzen M. Prognostic value of periodic electroencephalographic discharges for neurological patients with profound disturbances of consciousness. Clin Neurophysiol 2013; 124 (01) 44-51
  • 53 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 (19) 1951-1960
  • 54 Yemisci M, Gurer G, Saygi S, Ciger A. Generalised periodic epileptiform discharges: clinical features, neuroradiological evaluation and prognosis in 37 adult patients. Seizure 2003; 12 (07) 465-472
  • 55 Brenner RP, Schaul N. Periodic EEG patterns: classification, clinical correlation, and pathophysiology. J Clin Neurophysiol 1990; 7 (02) 249-267
  • 56 Husain AM, Mebust KA, Radtke RA. Generalized periodic epileptiform discharges: etiologies, relationship to status epilepticus, and prognosis. J Clin Neurophysiol 1999; 16 (01) 51-58
  • 57 Sutter R, Stevens RD, Kaplan PW. Significance of triphasic waves in patients with acute encephalopathy: a nine-year cohort study. Clin Neurophysiol 2013; 124 (10) 1952-1958
  • 58 Faigle R, Sutter R, Kaplan PW. Electroencephalography of encephalopathy in patients with endocrine and metabolic disorders. J Clin Neurophysiol 2013; 30 (05) 505-516
  • 59 Kaplan PW, Sutter R. Affair with triphasic waves-their striking presence, mysterious significance, and cryptic origins: what are they?. J Clin Neurophysiol 2015; 32 (05) 401-405
  • 60 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 (02) 109-123
  • 61 Braksick SA, Burkholder DB, Tsetsou S. , et al. Associated factors and prognostic implications of stimulus-induced rhythmic, periodic, or ictal discharges. JAMA Neurol 2016; 73 (05) 585-590
  • 62 Ong C, Gilmore E, Claassen J, Foreman B, Mayer SA. Impact of prolonged periodic epileptiform discharges on coma prognosis. Neurocrit Care 2012; 17 (01) 39-44
  • 63 Skjei KL, Kessler SK, Abend NS. Stimulus-induced rhythmic, periodic, or ictal discharges in a 13-year-old girl after an overdose and respiratory arrest. Pediatr Neurol 2011; 45 (05) 350-351
  • 64 Van Straten AF, Fesler JR, Hakimi R, Sheng T, Thompson DM, Hakimi AS. SIRPIDs: prevalence and outcome in critically ill patients. J Clin Neurophysiol 2014; 31 (05) 418-421
  • 65 Rossetti AO, Dunand M. Creutzfeldt-Jakob disease: evolution from nonconvulsive status epilepticus, through SIRPIDs, to generalized periodic discharges. Clin Neurophysiol 2007; 118 (11) 2533-2536
  • 66 Kaplan PW, Duckworth J. Confusion and SIRPIDs regress with parenteral lorazepam. Epileptic Disord 2011; 13 (03) 291-294
  • 67 Smith CC, Tatum WO, Gupta V, Pooley RA, Freeman WD. SPECT-negative SIRPIDs: less aggressive neurointensive care?. J Clin Neurophysiol 2014; 31 (03) e6-e10
  • 68 Zeiler SR, Turtzo LC, Kaplan PW. SPECT-negative SIRPIDs argues against treatment as seizures. J Clin Neurophysiol 2011; 28 (05) 493-496
  • 69 Alvarez V, Oddo M, Rossetti AO. Stimulus-induced rhythmic, periodic or ictal discharges (SIRPIDs) in comatose survivors of cardiac arrest: characteristics and prognostic value. Clin Neurophysiol 2013; 124 (01) 204-208
  • 70 DeGiorgio CM, Heck CN, Rabinowicz AL, Gott PS, Smith T, Correale J. Serum neuron-specific enolase in the major subtypes of status epilepticus. Neurology 1999; 52 (04) 746-749
  • 71 Lee JW. EEG in the ICU: what should one treat, what not?. Epileptologie 2012; 29: 210-217
  • 72 Rodríguez V, Rodden MF, LaRoche SM. Ictal-interictal continuum: A proposed treatment algorithm. Clin Neurophysiol 2016; 127 (04) 2056-2064
  • 73 Lansberg MG, O'Brien MW, Norbash AM, Moseley ME, Morrell M, Albers GW. MRI abnormalities associated with partial status epilepticus. Neurology 1999; 52 (05) 1021-1027
  • 74 Chu K, Kang DW, Kim JY, Chang KH, Lee SK. Diffusion-weighted magnetic resonance imaging in nonconvulsive status epilepticus. Arch Neurol 2001; 58 (06) 993-998
  • 75 Kavuk I, Koeppen S, Agelink M, Dörfler A, Limmroth V, Diener HC. Transient MRI abnormalities associated with partial status epilepticus. J Neurol 2004; 251 (09) 1156-1157
  • 76 Szabo K, Poepel A, Pohlmann-Eden B. , et al. Diffusion-weighted and perfusion MRI demonstrates parenchymal changes in complex partial status epilepticus. Brain 2005; 128 (Pt 6): 1369-1376
  • 77 Narayanan J. Can diffusion-weighted imaging be used as a tool to predict seizures in patients with PLEDS?. Epileptic Disord 2016; 18 (04) 440-446
  • 78 Handforth A, Cheng JT, Mandelkern MA, Treiman DM. Markedly increased mesiotemporal lobe metabolism in a case with PLEDs: further evidence that PLEDs are a manifestation of partial status epilepticus. Epilepsia 1994; 35 (04) 876-881
  • 79 Ergün EL, Salanci BV, Erbaş B, Saygi S. SPECT in periodic lateralized epileptiform discharges (PLEDs): a case report on PLEDs. Ann Nucl Med 2006; 20 (03) 227-231
  • 80 Bozkurt MF, Saygi S, Erbas B. SPECT in a patient with postictal PLEDs: is hyperperfusion evidence of electrical seizure?. Clin Electroencephalogr 2002; 33 (04) 171-173
  • 81 Struck AF, Westover MB, Hall LT, Deck GM, Cole AJ, Rosenthal ES. Metabolic correlates of the ictal-interictal continuum: FDG-PET during continuous EEG. Neurocrit Care 2016; 24 (03) 324-331
  • 82 DeGiorgio CM, Correale JD, Gott PS. , et al. Serum neuron-specific enolase in human status epilepticus. Neurology 1995; 45 (06) 1134-1137
  • 83 Ramont L, Thoannes H, Volondat A, Chastang F, Millet MC, Maquart FX. Effects of hemolysis and storage condition on neuron-specific enolase (NSE) in cerebrospinal fluid and serum: implications in clinical practice. Clin Chem Lab Med 2005; 43 (11) 1215-1217
  • 84 Marangos PJ, Campbell IC, Schmechel DE, Murphy DL, Goodwin FK. Blood platelets contain a neuron-specific enolase subunit. J Neurochem 1980; 34 (05) 1254-1258
  • 85 Vespa P, Tubi M, Claassen J. , et al. Metabolic crisis occurs with seizures and periodic discharges after brain trauma. Ann Neurol 2016; 79 (04) 579-590
  • 86 Witsch J, Frey HP, Schmidt JM. , et al. Electroencephalographic periodic discharges and frequency-dependent brain tissue hypoxia in acute brain injury. JAMA Neurol 2017; 74 (03) 301-309
  • 87 Jirsch J, Hirsch LJ. Nonconvulsive seizures: developing a rational approach to the diagnosis and management in the critically ill population. Clin Neurophysiol 2007; 118 (08) 1660-1670
  • 88 Fountain NB, Waldman WA. Effects of benzodiazepines on triphasic waves: implications for nonconvulsive status epilepticus. J Clin Neurophysiol 2001; 18 (04) 345-352
  • 89 Litt B, Wityk RJ, Hertz SH. , et al. Nonconvulsive status epilepticus in the critically ill elderly. Epilepsia 1998; 39 (11) 1194-1202
  • 90 O'Rourke D, Chen PM, Gaspard N. , et al. Response rates to anticonvulsant trials in patients with triphasic-wave EEG patterns of uncertain significance. Neurocrit Care 2016; 24 (02) 233-239
  • 91 Rossetti AO, Bromfield EB. Levetiracetam in the treatment of status epilepticus in adults: a study of 13 episodes. Eur Neurol 2005; 54 (01) 34-38
  • 92 Towne AR, Garnett LK, Waterhouse EJ, Morton LD, DeLorenzo RJ. The use of topiramate in refractory status epilepticus. Neurology 2003; 60 (02) 332-334