
Electroencephalogram Monitoring in Critical Care
Clio Rubinos,MD
Ayham Alkhachroum,MD
Caroline Der-Nigoghossian,PharmD, BCCCP
Corresponding author: Jan Claassen, MD, PhD, Associate Professor of Neurology, Neurological Institute, Columbia University, 177 Fort Washington Avenue, MHB 8 Center, Room 300, New York, NY 10032, Phone: 212-305-7236; Fax: 212-305-2792,jc1439@columbia.edu
Roles
Issue date 2020 Dec.
Abstract
Seizures are common in critically ill patients. Electroencephalogram (EEG) is a tool that enables clinicians to provide continuous brain monitoring and to guide treatment decisions – brain telemetry. EEG monitoring has particular utility in the intensive care unit (ICU) as most seizures in this setting are nonconvulsive. Despite the increased use of EEG monitoring in the critical care unit, it remains underutilized. In this review, we summarize the utility of EEG and different EEG modalities to monitor patients in the critical care setting.
Keywords: electroencephalogram, intensive care unit, seizures, status epilepticus
Introduction
EEG is relatively inexpensive, non-invasive, portable, and provides real-time continuous monitoring.1 Indications for EEG use include: seizure detection and management, ischemia and sedation monitoring, and neuro-prognostication.2 Seizures are a frequent complication in patients in the intensive care unit (ICU), but they are often under-recognized as they are mostly electrographic without clinical correlates.2,3 Nonconvulsive seizures occur in 10–48% of patients in the ICU. They are associated with high mortality.4–12 Despite studies reporting a tenfold increase in the use of EEG between 2004 and 2013, it is still an underutilized tool.13 The focus of this article is to review the utility of EEG for the detection and management of seizures in the ICU. In addition, we will discuss different EEG modalities available for monitoring, and the challenges faced by clinicians when recording critically ill patients.
Monitoring seizures in the ICU
Risk factors for seizures in critically ill patients include: acute structural lesions, traumatic brain injury (TBI), infections, intoxications, substance abuse and withdrawal, epilepsy and metabolic derangements.5 The incidence of seizures varies depending on the etiology.14 Seizures are most commonly nonconvulsive, particularly in patients with brain tumors and central nervous system infections.4 Nonconvulsive seizures also commonly occur in patients following the control of the convulsive phase.15,16 Many clinical signs can help prompt early recognition of nonconvulsive seizures including impaired consciousness, fluctuating mental status, episodic behavioral arrest, focal neurological manifestations, and subtle motor symptoms such as nystagmus, clonus, or opsoclonus.7
Seizures are not exclusively seen in the neurological ICU. In a medical ICU, up to 22% of the patients without brain injury had periodic discharges (PDs) or seizures – most commonly seen with sepsis and acute renal failure.17 Similarly, in a surgical ICU, up to 16% of patients who underwent EEG monitoring had electrographic seizures and up to 29% had PDs.18
EEG monitoring is recommended for the diagnosis of seizures and for monitoring the response to therapy by the American Clinical Neurophysiology Society (ACNS) critical care EEG task force, the European Society of Intensive Care Medicine (ESICM) and the Neurocritical Care Society.10,19,20
Monitoring Techniques
Surface EEG monitoring can be performed over a short duration as a spot EEG (30 – 60 minutes), or over a prolonged duration as a continuous EEG (cEEG).21 Monitoring for seizures can also be obtained using intracortical EEG (ICE).22 Monitoring can be performed via a portable EEG, a mobile desktop EEG, or an EEG workstation, ideally associated with a video camera system in order to minimize artifacts and to recognize clinical correlates of the EEG signal.21 The EEG signal reflects the recording of electrophysiological activity which are generated primarily by cortical layers 3 and 5.23 The EEG potentials are displayed in channels. In a bipolar montage, each displayed waveform represents the difference in potential between two electrodes. An upward deflection represents a negative difference, and a downward deflection represents a positive difference.24
Surface raw-data EEG (spot and continuous monitoring)
The arrangement of electrodes results in a variety of montages. Most commonly, a standard 21-electrode montage is used for monitoring, using what is known as the International 10–20 system.24 Alternative montages with less than 21 electrodes have been described, also known as limited montages. An example is a sub-hairline recording, which uses four bipolar derivations: left and right temporal placements and left and right frontal placements.25 The sub-hairline recording has excellent specificity (100%) but has limited sensitivity (54%) for detecting seizures.25 Another example is the use of a 10 electrode, 14 – channel montage to monitor patients with traumatic brain injury.26 The use of a full set of 21 electrodes is ideal for detection of subtle findings and for differentiating artifacts from brain activity.
The two main types of electrodes that are currently used include scalp disk electrodes (by far the most commonly used electrode type), and subdermal needle or wire electrodes.27 Subdermal needle electrodes are not usually placed on awake patients, but they are relatively easy to place and are useful for brief recordings in comatose patients.21,27 Wire electrodes are thin wires with a silver chloride tip that are usually placed using a needle applicator; they may reduce skin breakdown when compared to disc electrodes. One significant inconvenience in the ICU context is the need to remove and replace electrodes for magnetic resonance (MRI) and computed tomography (CT) imaging. MRI and CT compatible electrodes are available, but they are costly and not commonly applied.28
Surface EEG remains the most common method to detect seizures in the ICU using page-by-page visual inspection of the recording.21 This is usually done on-site or remotely by a neurophysiologist with EEG reading expertise.21 Spot EEG identifies only 45 – 58% of patients who eventually developed seizures.29 Patients should be ideally recorded for at least 24 hours, and for 48 hours if comatose.4 In a series of adult ICU patients with nonconvulsive seizures, 87% of patients experienced their first recorded seizure in the first 24 hours of EEG monitoring.4 When comatose patients were evaluated separately, 20% had their first seizure after more than 24 hours of monitoring.4 In children, 50% of seizures were detected within the first hour of monitoring, and 80% in the first 24 hours.30
Early EEG findings may help identify which patients require prolonged monitoring. In a study of 625 critically ill patients, the absence of epileptiform abnormalities during the first 15 minutes and 2 hours of recording was associated with a seizure probability of less than 10% and less than 5%, respectively.31 In cardiac arrest patients, brief 30-minute serial EEGs have been demonstrated to have a similar yield of seizure detection when compared to cEEG.32 Specific EEG patterns are associated with a higher risk of seizures such as generalized periodic discharges (GPDs), lateralized periodic discharges (LPDs), or lateralized rhythmic delta activity (LRDA), and longer recordings should be considered in these patients.33
Quantitative EEG (qEEG)
qEEG is a computational analysis of the EEG signal that enables the provider to quickly review large amounts of recorded EEG and unmask subtle changes that occur over many hours.21 This method allows quantification of power within different frequency spectra.21 Quantitative EEG can also visualize changes over time in amplitudes, various frequencies, and/or rhythmicity, and can be generated for individual channels or a combination of channels.34 An example of a qEEG measure used for seizure detection is color density spectral array (DSA). Color DSA displays power measurements for specific frequencies over time. The measurements are potentially helpful to screen for seizures which often have a characteristic appearance (i.e., flame shape) on DSA. Additionally, the technique allows identification of gradual changes that are difficult to detect when reading the raw data alone at a speed of 10 – 15 seconds per page.21 Other qEEG measurements that may be used for seizure detection include envelope trends, amplitude-integrated EEG, spectral edge display, rhythmicity spectrograms and commercially available seizure detection algorithms such as Persyst-Reveal, IdentEvent, BESA, and EpiScan.35–38 (Figure 1)
Figure 1.
qEEG monitoring demonstrating cyclic seizures arising from the right hemisphere in a 72-year-old woman with viral encephalitis. Her neurological examination was significant for altered mental status and left gaze deviation. Transient increases of power, especially in the higher frequencies (arrows), indicate brief right hemisphere nonconvulsive seizures.
In a critical care setting, the sensitivity and specificity of qEEG to detect nonconvulsive seizures ranges from 65% to 83% and 65% to 92%, respectively.39 However, critically ill patients frequently present with cyclic electrographic seizure patterns that are – once diagnosed - easily quantified using compressed spectral array (CSA).40 For example, CSA detected 89% of 1190 seizures in one study.41 (Figure 2)
Figure 2.
A 76-year-old man was admitted to the neurological ICU after a hemicraniectomy for the evacuation of traumatic right subdural hematoma with 6 mm midline shift. The neurological exam was significant for encephalopathy. A limited electrode montage was placed over the left hemisphere due to the presence of wound and surgical wrap. Continuous EEG showed left sided cyclic seizures (arrows on CSA and rectangle on raw EEG).
qEEG is becoming more widely available and there is an increasing interest in its interpretation by non-neurophysiologists. In a 2010 survey, qEEG use was reported by 66% of responders, and the most common techniques used were CSA (18%) and amplitude integrated EEG (13%).42 In a more recent survey, the authors found that qEEG was predominantly used for seizure detection (92%); the most commonly used trends were rhythmicity spectrogram (61%) followed by automated seizure detectors (55%), and color DSA (47%).43 Neurocritical care nurses detected seizures with 56% accuracy after a brief training session with a false positive rate of 1 per 3.2 hours.44
Intracortical EEG
Invasive EEG monitoring are available using subdural strips or intracortical depth electrodes. Intracortical electrodes consist of eight-contact ring electrodes with 2.2 mm intercontact spacing and contact width of 1.32 mm. One to two contacts are placed in the gray matter, some in the white matter, and one or two may be outside of the brain. Depth electrodes are commonly placed through a burr hole and affixed in a bolt with other multimodality monitoring devices such as an intracranial pressure probe.22 In a study of 14 patients with acute brain injury, 6 patients had seizures on depth recording while only 2 patients had changes on the surface EEG.22 In a multicenter study that combined surface and depth EEG recordings in severe TBI patients, 42.9% of seizures were only detected by the depth EEG and were associated with metabolic crisis.45 In a larger study of almost 50 SAH patients, 38% had seizures only using the depth electrode, while only 8% had seizures detected on scalp EEG. Depth EEG seizures were associated with increased heart rate, blood pressure, brain metabolism and respiratory rate.46 More recently, hyperemia was associated with increased risk of seizures using depth EEG recordings in patients with SAH.47 Despite the higher likelihood of seizure detection with intracortical EEG, its use is not widespread, because it is invasive and current guidelines do not provide recommendations as to when to use it.
Seizures and periodic discharges on EEG
Electrographic seizures are defined as rhythmic patterns >2.5 Hz in frequency or <2.5 Hz with one of the following: typical ictal spatiotemporal evolution, subtle ictal clinical phenomenon, and EEG and clinical improvement after IV antiseizure drugs (ASD).48
Periodic discharges (PDs) can be lateralized, generalized, bilateral independent (BIPDs), stimulus-induced rhythmic, periodic, or ictal discharges, or lateralized or generalized rhythmic delta activity (RDA).49 Up to 29% of patients undergoing cEEG in the ICU were found to have PDs with a variety of underlying pathologies.4,18,50 PDs are associated with seizures, worse functional outcome and higher mortality.51–53 PDs may also have similar metabolic consequences as seizures - such as increased regional glucose metabolism, elevated lactate/pyruvate ratio, and tissue hypoxia.45,54 Based on these pathophysiologic observations, many experts recommend that certain PDs such as high frequency discharges (>2.5 Hz) warrant management similar to seizures.49
Seizure mimics on EEG
Artifacts are common in the ICU and can be misinterpreted as seizures. Up to 10% of presumed motor seizures in the neurological ICU and up to 73% in non-neurological intensive care units are not ictal.5 These abnormal movements include tremors, purposeful movements, myoclonus and shivering.5 Sources of artifacts are related to medical staff, patients, electrical currents and life-supporting devices. Artifacts are generally divided into two groups: physiological and non-physiological. Physiological artifacts are the result of eye movements, muscle, sweat, tongue and pulse. Non-physiological artifacts are commonly generated by the environment- such as 50 or 60 Hz artifact, mechanical ventilation, and intravenous drips.5
Many rhythmic patterns can mimic seizures in the ICU, such as chest percussion during respiratory therapy, electrocardiogram or pacemaker artifact, glossokinetic artifact (tongue movement), vibrating bed artifact and respiratory artifact. Tongue movements can result in prominent bursts of slow waves and can resemble frontally predominant generalized rhythmic delta activity. Digital video recording is extremely helpful to identify these artifacts.5
Management of Status Epilepticus (SE), refractory SE, super refractory SE
Treatment guidelines recommend cEEG monitoring in patients who do not regain consciousness within 30 minutes of starting seizure treatment.10,20,55 If a patient is being treated in a facility that does not have cEEG monitoring, it is recommended to transfer the patient to an ICU that can offer the monitoring.10 Delay in diagnosis of seizures and duration of SE have been associated with increased mortality and neuronal damage.11,56,57 Despite successful treatment of generalized convulsive SE, most patients remain comatose or obtunded.15,16 Therefore, timely initiation of cEEG monitoring is essential to guide treatment and rapidly escalate therapy.
The treatment goal for SE is controversial and there is no consensus on the superiority of seizure suppression, burst suppression or complete background suppression or the duration of treatment. A meta-analysis evaluating continuous anesthetics for the treatment of refractory SE showed that background suppression was associated with significantly less withdrawal seizures but more hypotension.58 In contrast, a recent retrospective study showed that patients that were under deeper therapeutic coma, receiving higher doses of anesthetics, were 68% less likely to experience complications including urinary tract infections, hospital-acquired/ventilator-associated pneumonia, deep vein thrombosis/pulmonary embolism, stroke, myocardial infarction, sepsis from any source, critical illness myopathy/neuropathy, and hypotension requiring vasopressor therapy.59
The optimal duration of maintaining therapeutic coma is also unknown. Current guidelines suggest 24 – 48 hours of therapeutic coma, followed by gradual withdrawal of the continuous ASD infusion.20 However, Muhlhofer et al. recently suggested that shorter duration (<35 hours) yet deeper therapeutic coma may be more effective for the treatment for refractory SE.59 Prospective and randomized trials should be conducted to validate these assertions.
Weaning of Anesthetics and Antiseizure Drugs
Current treatment guidelines recommend monitoring for recurrent seizures by cEEG when weaning off continuous anesthetics.19,20 Subclinical withdrawal seizures that can only be detected with cEEG are common in patients with nonconvulsive SE (68%).60 Continuous EEG monitoring is essential to guide titration of anesthetics and ASDs. There is insufficient evidence to support an optimal duration of cEEG monitoring after the treatment goal is achieved but guidelines recommend a duration of 24 to 48 hours.42 The half-life of anesthetics and ASDs should also be considered, as this can guide the duration of cEEG monitoring. Longer recording may be warranted when discontinuing medications with longer half-lives and in patients with organ dysfunction.
Challenges in Monitoring Critically Ill Patients
There are many technical challenges to overcome in order to generate high quality cEEG recordings in the ICU environment. EEG technologist coverage to provide maintenance of electrodes is one of the most common ones.27,61 Another major challenge is data storage- several days of cEEG in the ICU generate gigabytes worth of data. The choice of server architecture, processor speed, and memory should be considered.61 Additionally, in current practice, cEEG monitoring is not reviewed in real-time and it requires evaluation by trained personnel. Records are ideally reviewed by neurophysiologists two to three times a day. Trends and automated alarms – using qEEG – can be used to facilitate detection of events by electroencephalographers, intensivists and nursing staff.34,35
Conclusion
Continuous EEG is a tool for dynamic assessment of brain physiology, most commonly used for seizure detection and to guide management decisions. In this review, we present this tool for the purpose of seizure detection –brain telemetry. We present different modalities of recording, and the EEG-driven treatment of most commonly seen epileptic patterns. Finally, we reviewed some of the most common challenges in using EEG in the ICU, including artifacts.
Footnotes
Conflicts of interest: JC is a minority shareholder at iCE Neurosystems. None of the authors have significant conflicts of interest to report.
Contributor Information
Clio Rubinos, Division of Critical Care Neurology, University of North Carolina School of Medicine, 170 Manning Drive , Physician Office, CB 7025, Chapel Hill, NC 27599 – 7025.
Ayham Alkhachroum, Department of Neurology, University of Miami, Miller School of Medicine, Jackson Memorial Health System, 1120 NW 14 Street, Suite 1353, Miami, FL 33136.
Caroline Der-Nigoghossian, Neurosciences Intensive Care Unit, Department of Pharmacy, NewYork-Presbyterian Hospital/Columbia University Irving Medical Center, 622 West 168th street, New York, NY 10032.
References
- 1.Nuwer MR. Electroencephalograms and evoked potentials. Monitoring cerebral function in the neurosurgical intensive care unit. Neurosurg Clin N Am. 1994;5(4):647–659 [PubMed] [Google Scholar]
- 2.Jordan KG. Neurophysiologic monitoring in the neuroscience intensive care unit. Neurologic clinics. 1995;13(3):579–626 [PubMed] [Google Scholar]
- 3.Limotai C, Ingsathit A, Thadanipon K, McEvoy M, Attia J, Thakkinstian A. How and Whom to Monitor for Seizures in an ICU: A Systematic Review and Meta-Analysis. Critical care medicine. 2019;47(4):e366–e373 [DOI] [PubMed] [Google Scholar]
- 4.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 [DOI] [PubMed] [Google Scholar]
- 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(7):1090–1094 [DOI] [PubMed] [Google Scholar]
- 6.Towne AR, Waterhouse EJ, Boggs JG, et al. Prevalence of nonconvulsive status epilepticus in comatose patients. Neurology. 2000;54(2):340–345 [DOI] [PubMed] [Google Scholar]
- 7.Jordan KG. Nonconvulsive status epilepticus in acute brain injury. J Clin Neurophysiol. 1999;16(4):332–340; discussion 353 [DOI] [PubMed] [Google Scholar]
- 8.Privitera M, Hoffman M, Moore JL, Jester D. EEG detection of nontonic-clonic status epilepticus in patients with altered consciousness. Epilepsy research. 1994;18(2):155–166 [DOI] [PubMed] [Google Scholar]
- 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. Journal of neurosurgery. 1999;91(5):750–760 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Claassen J, Taccone FS, Horn P, et al. Recommendations on the use of EEG monitoring in critically ill patients: consensus statement from the neurointensive care section of the ESICM. Intensive care medicine. 2013;39(8):1337–1351 [DOI] [PubMed] [Google Scholar]
- 11.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(1):83–89 [DOI] [PubMed] [Google Scholar]
- 12.Shneker BF, Fountain NB. Assessment of acute morbidity and mortality in nonconvulsive status epilepticus. Neurology. 2003;61(8):1066–1073 [DOI] [PubMed] [Google Scholar]
- 13.Hill CE, Blank LJ, Thibault D, et al. Continuous EEG is associated with favorable hospitalization outcomes for critically ill patients. Neurology. 2019;92(1):e9–e18 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Abou Khaled KJ, Hirsch LJ. Advances in the management of seizures and status epilepticus in critically ill patients. Crit Care Clin. 2006;22(4):637–659; abstract viii [DOI] [PubMed] [Google Scholar]
- 15.Treiman DM, Meyers PD, Walton NY, et al. A comparison of four treatments for generalized convulsive status epilepticus. Veterans Affairs Status Epilepticus Cooperative Study Group. The New England journal of medicine. 1998;339(12):792–798 [DOI] [PubMed] [Google Scholar]
- 16.DeLorenzo RJ, Waterhouse EJ, Towne AR, et al. Persistent nonconvulsive status epilepticus after the control of convulsive status epilepticus. Epilepsia. 1998;39(8):833–840 [DOI] [PubMed] [Google Scholar]
- 17.Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ. Continuous electroencephalography in the medical intensive care unit. Critical care medicine. 2009;37(6):2051–2056 [DOI] [PubMed] [Google Scholar]
- 18.Kurtz P, Gaspard N, Wahl AS, et al. Continuous electroencephalography in a surgical intensive care unit. Intensive care medicine. 2014;40(2):228–234 [DOI] [PubMed] [Google Scholar]
- 19.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(2):87–95 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Brophy GM, Bell R, Claassen J, et al. Guidelines for the evaluation and management of status epilepticus. Neurocritical care. 2012;17(1):3–23 [DOI] [PubMed] [Google Scholar]
- 21.Caricato A, Melchionda I, Antonelli M. Continuous Electroencephalography Monitoring in Adults in the Intensive Care Unit. Critical care. 2018;22(1):75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Waziri A, Claassen J, Stuart RM, et al. Intracortical electroencephalography in acute brain injury. Annals of neurology. 2009;66(3):366–377 [DOI] [PubMed] [Google Scholar]
- 23.Jordan KG. Emergency EEG and continuous EEG monitoring in acute ischemic stroke. J Clin Neurophysiol. 2004;21(5):341–352 [PubMed] [Google Scholar]
- 24.Society ACN. Guideline 1: minimum technical requirements for performing clinical electroencephalography. Am J Electroneurodiagnostic Technol. 2006;46(3):198–204 [PubMed] [Google Scholar]
- 25.Tanner AE, Särkelä MO, Virtanen J, et al. Application of subhairline EEG montage in intensive care unit: comparison with full montage. J Clin Neurophysiol. 2014;31(3):181–186 [DOI] [PubMed] [Google Scholar]
- 26.Vespa PM, Boscardin WJ, Hovda DA, et al. Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. Journal of neurosurgery. 2002;97(1):84–92 [DOI] [PubMed] [Google Scholar]
- 27.Young GB, Campbell VC. EEG monitoring in the intensive care unit: pitfalls and caveats. J Clin Neurophysiol. 1999;16(1):40–45 [DOI] [PubMed] [Google Scholar]
- 28.Mirsattari SM, Lee DH, Jones D, Bihari F, Ives JR. MRI compatible EEG electrode system for routine use in the epilepsy monitoring unit and intensive care unit. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2004;115(9):2175–2180 [DOI] [PubMed] [Google Scholar]
- 29.Fogang Y, Legros B, Depondt C, Mavroudakis N, Gaspard N. Yield of repeated intermittent EEG for seizure detection in critically ill adults. Neurophysiol Clin. 2017;47(1):5–12 [DOI] [PubMed] [Google Scholar]
- 30.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):1750–1755 [DOI] [PubMed] [Google Scholar]
- 31.Gaspard N, Foreman BP, Alvarez V, et al. New-onset refractory status epilepticus: Etiology, clinical features, and outcome. Neurology. 2015;85(18):1604–1613 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Alvarez V, Sierra-Marcos A, Oddo M, Rossetti AO. Yield of intermittent versus continuous EEG in comatose survivors of cardiac arrest treated with hypothermia. Critical care. 2013;17(5):R190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Rodriguez Ruiz A, Vlachy J, Lee JW, et al. Association of Periodic and Rhythmic Electroencephalographic Patterns With Seizures in Critically Ill Patients. JAMA neurology. 2017;74(2):181–188 [DOI] [PubMed] [Google Scholar]
- 34.Scheuer ML, Wilson SB. Data analysis for continuous EEG monitoring in the ICU: seeing the forest and the trees. J Clin Neurophysiol. 2004;21(5):353–378 [PubMed] [Google Scholar]
- 35.Wilson SB, Scheuer ML, Emerson RG, Gabor AJ. Seizure detection: evaluation of the Reveal algorithm. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2004;115(10):2280–2291 [DOI] [PubMed] [Google Scholar]
- 36.Kelly KM, Shiau DS, Kern RT, et al. Assessment of a scalp EEG-based automated seizure detection system. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2010;121(11):1832–1843 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Hopfengärtner R, Kasper BS, Graf W, et al. Automatic seizure detection in long-term scalp EEG using an adaptive thresholding technique: a validation study for clinical routine. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2014;125(7):1346–1352 [DOI] [PubMed] [Google Scholar]
- 38.Hartmann MM, Fürbass F, Perko H, et al. EpiScan: online seizure detection for epilepsy monitoring units. Conf Proc IEEE Eng Med Biol Soc2011;2011:6096–6099 [DOI] [PubMed] [Google Scholar]
- 39.Sansevere AJ, Hahn CD, Abend NS. Conventional and quantitative EEG in status epilepticus. Seizure. 2019;68:38–45 [DOI] [PubMed] [Google Scholar]
- 40.Friedman DE, Schevon C, Emerson RG, Hirsch LJ. Cyclic electrographic seizures in critically ill patients. Epilepsia. 2008;49(2):281–287 [DOI] [PubMed] [Google Scholar]
- 41.Williamson CA, Wahlster S, Shafi MM, Westover MB. Sensitivity of compressed spectral arrays for detecting seizures in acutely ill adults. Neurocritical care. 2014;20(1):32–39 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.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. Neurocritical care. 2010;12(3):382–389 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Swisher CB, Sinha SR. Utilization of Quantitative EEG Trends for Critical Care Continuous EEG Monitoring: A Survey of Neurophysiologists. J Clin Neurophysiol. 2016;33(6):538–544 [DOI] [PubMed] [Google Scholar]
- 44.Amorim E, Williamson CA, Moura LMVR, et al. Performance of Spectrogram-Based Seizure Identification of Adult EEGs by Critical Care Nurses and Neurophysiologists. J Clin Neurophysiol. 2017;34(4):359–364 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Vespa P, Tubi M, Claassen J, et al. Metabolic crisis occurs with seizures and periodic discharges after brain trauma. Annals of neurology. 2016;79(4):579–590 [DOI] [PubMed] [Google Scholar]
- 46.Claassen J, Perotte A, Albers D, et al. Nonconvulsive seizures after subarachnoid hemorrhage: Multimodal detection and outcomes. Annals of neurology. 2013;74(1):53–64 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Alkhachroum A, Megjhani M, Terilli K, et al. Hyperemia in subarachnoid hemorrhage patients is associated with an increased risk of seizures. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 2019:271678X19863028 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Beniczky S, Hirsch LJ, Kaplan PW, et al. Unified EEG terminology and criteria for nonconvulsive status epilepticus. Epilepsia. 2013;54Suppl 6:28–29 [DOI] [PubMed] [Google Scholar]
- 49.Bauerschmidt A, Rubinos C, Claassen J. Approach to Managing Periodic Discharges. J Clin Neurophysiol. 2018;35(4):309–313 [DOI] [PubMed] [Google Scholar]
- 50.Rubinos C, Reynolds AS, Claassen J. The Ictal-Interictal Continuum: To Treat or Not to Treat (and How)?Neurocritical care. 2018;29(1):3–8 [DOI] [PubMed] [Google Scholar]
- 51.Claassen J, Hirsch LJ, Frontera JA, et al. Prognostic significance of continuous EEG monitoring in patients with poor-grade subarachnoid hemorrhage. Neurocritical care. 2006;4(2):103–112 [DOI] [PubMed] [Google Scholar]
- 52.Claassen J, Jetté N, Chum F, et al. Electrographic seizures and periodic discharges after intracerebral hemorrhage. Neurology. 2007;69(13):1356–1365 [DOI] [PubMed] [Google Scholar]
- 53.Sainju RK, Moeller JJ, Hirsch LJ. Teaching neuroImages: a broadly distributed ictal rhythm easily missed on bipolar montage: “now you see it…”. Neurology. 2015;84(15):e115–116 [DOI] [PubMed] [Google Scholar]
- 54.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(4):876–881 [DOI] [PubMed] [Google Scholar]
- 55.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(2):87–95 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Wasterlain CG, Fujikawa DG, Penix L, Sankar R. Pathophysiological mechanisms of brain damage from status epilepticus. Epilepsia. 1993;34Suppl 1:S37–53 [DOI] [PubMed] [Google Scholar]
- 57.Chen JW, Wasterlain CG. Status epilepticus: pathophysiology and management in adults. Lancet Neurol. 2006;5(3):246–256 [DOI] [PubMed] [Google Scholar]
- 58.Claassen J, Hirsch LJ, Emerson RG, Mayer SA. Treatment of refractory status epilepticus with pentobarbital, propofol, or midazolam: a systematic review. Epilepsia. 2002;43(2):146–153 [DOI] [PubMed] [Google Scholar]
- 59.Muhlhofer WG, Layfield S, Lowenstein D, et al. Duration of therapeutic coma and outcome of refractory status epilepticus. Epilepsia. 2019;60(5):921–934 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60.Claassen J, Hirsch LJ, Emerson RG, Bates JE, Thompson TB, Mayer SA. Continuous EEG monitoring and midazolam infusion for refractory nonconvulsive status epilepticus. Neurology. 2001;57(6):1036–1042 [DOI] [PubMed] [Google Scholar]
- 61.Kull LL, Emerson RG. Continuous EEG monitoring in the intensive care unit: technical and staffing considerations. J Clin Neurophysiol. 2005;22(2):107–118 [DOI] [PubMed] [Google Scholar]