INVITED REVIEW
Are We Prepared to Detect Subtle and Nonconvulsive Status
Epilepticus in Critically Ill Patients?
Raoul Sutter*†
Summary: Continuous electroencephalography uncovers a clinically under-
appreciated burden of subtle and nonconvulsive status epilepticus in critically
ill patients. Prolonged recordings over days are labor intensive and patient or
medical equipment related electrographic artifacts are challenging, calling for
a targeted use of electroencephalography in patients with defined seizure risk
profiles. This review compiles current data of the impact of continuous
electroencephalography on the detection of subtle and nonconvulsive status
epilepticus in different clinical scenarios and its contribution to treatment and
monitoring in intensive care units. Current recommendations on the use of
continuous electroencephalography in the critically ill are outlined.
Key Words: Continuous EEG, Subtle status epilepticus, Nonconvulsive
status epilepticus, Critically illness, Neurocritical care.
(J Clin Neurophysiol 2016;33: 25–31)
S ince electroencephalography (EEG) converted from analog to
digital, electronic data storage volumes increased, and computer
networking enabled remote EEG reading, continuous electroenceph-
alography (cEEG) monitoring over hours to days emerged. This
diagnostic tool provides dynamic real-time information of brain
function enabling immediate detection of changes in neurofunctional
status, even if clinical signs and symptoms of pathologic cerebral
processes are subtle or unspecific.
The increasing use of cEEG reveals a clinically underappre-
ciated burden of seizures in a large variety of patients with different
critical illnesses. Studies of the diagnostic yield of cEEG in the
intensive care units (ICUs) are limited, especially regarding the
detection of life-threatening subtle or nonconvulsive status epilepti-
cus (SSE or NCSE). Early diagnosis and treatment monitoring of
status epilepticus (SE) with cEEG is likely to shorten SE duration
and to improve patients’ outcomes (Logroscino et al., 2002; Sagduyu
et al., 1998; Sutter et al., 2013b, 2013c; Towne et al., 1994; Young
et al., 1996). However, the recording over days, the challenges
arising from patient and ICU equipment-related electrographic
artifacts, and the interpretation by trained EEG readers are time
consuming and labor intensive, calling for a targeted use in patients
with defined risk profiles for SE. When compared with short-term
From the *Clinic for Intensive Care Medicine and Department of Neurology,
University Hospital Basel, Basel, Switzerland; and †Division of Clinical
Neurophysiology, Department of Neurology, University Hospital Basel, Basel,
Switzerland.
R. Sutter was supported by the Research Fund of the University of Basel, the
Scientific Society Basel, and the Gottfried Julia Bangerter-Rhyner Foundation.
He holds stocks from Roche and Novartis. He received honoraria from
Centron Medical Education and travel grants from UCB Pharma.
Address correspondence and reprint requests to Raoul Sutter, MD, Department
Neurology and Intensive Care Units, University Hospital Basel, Basel,
Switzerland; e-mail: raoul.sutter@usb.ch.
Copyright Ó 2016 by the American Clinical Neurophysiology Society
ISSN: 0736-0258/16/3301-0025
Journal of Clinical Neurophysiology
Volume 33, Number 1, February 2016
EEG, the diagnostic advantage of cEEG has been questioned,
especially in institutions with limited resources and restricted access
to cEEG (Rai et al., 2013).
This review compiles the current data of the impact of cEEG
in different clinical scenarios on the detection rate of SSE and
NCSE, and its important contribution to rapid treatment initiation
and escalation tailored to the individual patient. The current
recommendations on the use of cEEG in the critically ill are
outlined.
THE DEFINITIONS OF SUBTLE AND NCSE
Nonconvulsive Status Epilepticus
Nonconvulsive SE is a state of continuous seizures without
convulsions or repetitive nonconvulsive seizures without intermedi-
ate complete neurofunctional recovery for at least 30 minutes (Sutter
et al., 2012). Even seizures lasting more than 5 minutes are likely to
persist and may functionally represent SE (Lowenstein et al., 1999).
The clinical features of NCSE and SSE are highly variable. In
a systematic review of the literature regarding NCSE symptoms
(Sutter et al., 2012), detailed descriptions of clinical symptoms were
identified in 105 cases where EEG patterns of NCSE were provided.
The most frequently described symptoms can challenge diagnosis
(Fig. 1), as they may arise from other conditions (Sutter et al., 2012).
Hence, the diagnosis of NCSE has to be confirmed by EEG. The
EEG criteria for NCSE are complex and depend on the presence or
absence of epileptic encephalopathy and on the underlying clinical
syndromes (Kaplan, 2007; Sutter et al., 2012) (Table 1). In
a systematic review, characteristic electrographic patterns and
sequential arrangements were elucidated for 22 NCSE syndromes
as a compendium that allows the definition of the EEG character-
istics and semiologic borderlines among the NCSE subtypes (Sutter
and Kaplan, 2012).
Subtle Status Epilepticus
Subtle SE is a form of NCSE that evolves from a generalized
convulsive SE if the latter has been treated insufficiently or not at all.
Subtle SE was first described as a syndrome of discrete (subtle)
clinical signs, such as nystagmus, eye blinking, and/or mild motor
movements combined with marked impairment of consciousness and
continuous or nearly continuous, usually bilateral, ictal EEG patterns
(Treiman et al., 1984). Some patients continued to have ictal EEG
activity after all movements ceased. The definition was expanded
mentioning that sometimes a single convulsion can introduce SSE
rather than a convulsive SE episode. Furthermore, although most
patients present a focal component at some point during SSE,
periodic discharges usually become bilateral even if first generated
from a unilateral source (Treiman, 1995).
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Volume 33, Number 1, February 2016
FIG. 1. The most frequently reported symptoms of nonconvulsive status epilepticus in the literature [numbers extracted from
a systematic review of the literature identifying 105 cases (Sutter et al., 2012)].
DETECTION OF SUBTLE AND NONCONVULSIVE
STATUS EPILEPTICUS IN CRITICALLY ILL PATIENTS
The increasing use of cEEG uncovers clinically undetected
epileptic activity in 10% to 67% of critically ill patients (Claassen
et al., 2004; DeLorenzo et al., 1998; Friedman et al., 2009; Jette
TABLE 1. EEG Criteria for Nonconvulsive Status Epilepticus in
Adults With and Without Epileptic Encephalopathy (Based on
the Work of Peter Kaplan [Kaplan, 2007])
NCSE Without Epileptic Encephalopathy
Repetitive focal or generalized spikes, polyspike, sharp waves, and spike-and-
wave or sharp-and-slow wave discharges with
Discharges at frequencies of more than 2.5 Hz with ictal symptoms* but
with improvement after intravenous benzodiazepines with increase in EEG
reactivity and appearance of EEG background activity
Or discharges at frequencies of less than 2.5 Hz with ictal symptoms and
clinical improvement after intravenous benzodiazepines with increase in EEG
reactivity and normalization of EEG background activity
Rhythmic waves at a frequency of more than 0.5 Hz (theta–delta range) with
a) Incrementing onset (increase in voltage and increase or decrease in
frequency)
b) Evolution in pattern (increase or decrease in frequency, or location)
c) Decrementing termination (voltage and/or frequency)
d) Postperiodic epileptiform discharges and slowing or attenuation of EEG
background
Therefore, a, b, and c may be abolished after the intravenous administration
of benzodiazepines
NCSE With Epileptic Encephalopathy
Frequent or continuous generalized spike waves, which show an increase in
profusion or frequency when compared with baseline EEG paralleled by
change in clinical neurofunctional state. Improvement of clinical
neurofunctional and/or EEG state after the intravenous administration of
benzodiazepines
*Ictal symptoms ¼ altered mental status, facial twitching, gaze deviation,
nystagmus, and myoclonus of the limbs.
EEG, electroencephalography; i.v., intravenous; NCSE, nonconvulsive status
epilepticus.
26
et al., 2006; Oddo et al., 2009; Sutter et al., 2011; Vespa et al., 1999).
The proportion of patients with seizures and SE depends on the
underlying critical illnesses (Fig. 2) (Sutter et al., 2013a). When
assessing the detection of first seizures over time elapsing after
initiation of cEEG in critically ill patients, the percentage of newly
diagnosed seizures increases markedly in the first 2 days (Fig. 3). In
a study of ICU patients with altered levels of consciousness, only
56% of seizures were detected in the first hour, and 93% in the first
48 hours underscoring the importance of cEEG monitoring (Claassen
et al., 2004). Further evidence for the diagnostic yield of cEEG in
patients with altered consciousness comes from a study revealing an
increased NCSE detection rate after the introduction of cEEG as
compared with historic controls with short-term EEG (Sutter et al.,
2011). Further analyses revealed SSE and NCSE in 81% of all SE in
the ICUs (Rudin et al., 2011), pointing to the need for EEG
monitoring. In a study of critically ill patients with altered
consciousness and clinically suspected NCSE, cEEG provided
independent prognostic information with unfavorable findings
(associated with a modified Rankin Scale 4–6), being nonconvulsive
seizures (NCSz), periodic epileptiform discharges, and abnormal
background activity (Rai et al., 2013). Conversely, short-term EEG
was ineffective in detecting seizures and therefore not recommended
as a cEEG substitute (Rai et al., 2013). The higher SE detection rates
with cEEG are possibly explained by the intermittent nature of occult
seizures that are frequently missed with short-term recording
(Claassen et al., 2004) and by the heightened awareness of SE once
cEEG is introduced (Sutter et al., 2011).
Although these data of unselected ICU populations leave no
doubt that cEEG has a diagnostic impact, they do not clarify if cEEG
has a similar diagnostic impact in subsets of ICU populations with
specific illnessesda question that will be addressed below.
CONTINUOUS EEG MONITORING IN PATIENTS
WITH PRIMARY NONNEUROLOGIC
CRITICAL ILLNESSES
In nonneurologic ICUs, seizures occur in 4% to 15% of patients
(Bleck et al., 1993; Gofton et al., 2014; Marcuse et al., 2014; Oddo
et al., 2009), whereas SE is reported in less than 1% (Bleck et al., 1993)
Copyright Ó 2016 by the American Clinical Neurophysiology Society
Journal of Clinical Neurophysiology
Volume 33, Number 1, February 2016
FIG. 2. The occurrence rates of seizures and SE in critically ill patients. SE, status epilepticus.
(Fig. 2). In patients with septic encephalopathy, seizures are
associated with poor outcome (Oddo et al., 2009). Electroenceph-
alographic evidence of NCSz or NCSE is described in more than
a third of patients admitted to emergency rooms with altered mental
FIG. 3. The detection of first seizures over time after start of
continuous electroencephalography in critically ill patients.
Copyright Ó 2016 by the American Clinical Neurophysiology Society
Detect Subtle and Nonconvulsive SE
statusdthe only clinical sign in a third and subtle motor activity
being present in another third (Privitera et al., 1994). In another
study of comatose patients without previous seizures, epilepsy, or
other neurologic illnesses, 8% had NCSE during EEG (Towne et al.,
2000). Therefore, guidelines recommend cEEG in nonneurocritically
ill ICU patients with unexplained altered consciousness for seizure
detection (Claassen et al., 2013; Sutter et al., 2013a) (Table 2).
However, the cost effectiveness and impact of cEEG on outcome in
this population need to be determined.
CONTINUOUS EEG MONITORING IN
NEUROCRITICALLY ILL PATIENTS
Traumatic Brain Injury
Traumatic brain injury (TBI) is associated with seizures in
more than 20% of patients with blunt trauma and in 35% to 50%
with penetrating cranial injuries (Yablon, 1993) (Fig. 2). With cEEG,
10% of TBI patients show NCSz, and SE is associated with 100%
mortality (Vespa et al., 1999). Continuous electroencephalography
reveals seizures in more than a third of patients within the first 74
hours after head trauma (Ronne-Engstrom and Winkler, 2006).
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TABLE 2. Synthesis of Current Recommendations on the Use of cEEG in Critically Ill Patients to Detect NCSz, SSE, or NCSE
(Based on Current Reviews [Claassen et al., 2013; Sutter et al., 2013a])
Tentative Grading of Importance of
Underlying Etiology Scenario cEEG for Seizure Detection*
Generalized convulsive SE No return to functional baseline after initial antiepileptic therapy 111
Refractory SE Concern for ongoing seizures 111
Cardiac arrest Unexplained altered level of consciousness 111
TBI Unexplained altered level of consciousness 11
SAH Unexplained altered level of consciousness 11
ICH Persistent coma 11
Encephalitis Unexplained altered level of consciousness 11
Comatose patients without primary brain injury Unexplained altered level of consciousness 1(1)
*Tentative grading of importance of continuous electroencephalography: 1 ¼ minor importance; 11 ¼ moderate importance; 111 ¼ strong importance.
cEEG, continuous electroencephalography; ICH, intracerebral hemorrhage; NCSE, nonconvulsive status epilepticus; SAH, subarachnoid hemorrhage; SE, status epilepticus; SSE,
subtle status epilepticus; TBI, traumatic brain injury.

Seizures after TBI are linked to elevated intracranial pressure and
cerebral metabolic distress possibly leading to additional brain
damage (Vespa et al., 2007) and poor neurofunctional outcome
(Thapa et al., 2010; Wiedemayer et al., 2002). Adverse effects are
also shown in a case series of six TBI patients (four with NCSE) with
hippocampal atrophy ipsilateral to the seizures on serial brain MRIs
(Vespa et al., 2010). Further research is needed to clarify if early and
intensive seizure suppression may improve outcome in this pop-
ulation. Meanwhile, guidelines recommend 7 days of prophylactic
administration of antiepileptic drugs (AEDs) after moderate or
severe TBI and cEEG monitoring in TBI patients who have an
unexplained severe or prolonged altered consciousness (Bratton
et al., 2007; Claassen et al., 2013; Sutter et al., 2013a).
Subarachnoid Hemorrhage
Studies of patients with aneurysmal subarachnoid hemorrhage
(SAH) report seizures in up to 16%, with NCSE in more than 10%
and more frequently in severe cerebral insults (Claassen et al., 2006,
2003; Hart et al., 2011; Hirsch, 2004; Martinez-Manas et al., 2002;
Olafsson et al., 2000) (Fig. 2). The role of routine seizure
prophylaxis, however, remains controversial. In a prospective study
mortality with SE persisting beyond the fifth day after SAH is
reported to be 100% (Dennis et al., 2002) supporting cEEG and
rigorous treatment of SAH-related SE. However, data from four
randomized trials of SAH patients relate the prophylactic AED
administration with worse outcome (Rosengart et al., 2007). Hence,
cEEG in SAH patients with altered consciousness remains indispens-
able to uncover SSE or NCSE calling for immediate antiepileptic
therapy (Claassen et al., 2013).
Intracerebral Hemorrhage
Intracerebral hemorrhage (ICH)-related seizures can be de-
tected in up to a third of patients (Bladin et al., 2000; Faught et al.,
1989; Kilpatrick et al., 1990; Passero et al., 2002; Sung and Chu,
1989) and SE in up to 20% (Bateman et al., 2007; De Reuck et al.,
2007; Sung and Chu, 1989) (Fig. 2). Although ICH progression,
lobar and cortical bleeds (Claassen et al., 2007; De Herdt et al., 2011;
Vespa et al., 2003), hydrocephalus, and midline-shift are associated
with post-ICH seizures (Balami and Buchan, 2012; Bladin et al.,
2000), studies fail to identify seizures or SE as independent
predictors for poor outcome (Bladin et al., 2000; De Herdt et al.,
2011; Passero et al., 2002; Reith et al., 1997). Furthermore, the
prophylactic AED administration is associated with adverse outcome
(Naidech et al., 2009). Hence, guidelines from the American Heart
Association advise against the prophylactic AED administration in
all patients with ICH (Morgenstern et al., 2010) and underscore the
importance of cEEG for the identification of selected patients with
seizures or SE that urgently need antiepileptic treatment.
Hypoxic–Ischemic Brain Injury
In cardiorespiratory arrest survivors with persistent coma,
seizures occur in up to 40% and SE in 30% (Fig. 2); however, they
are not believed to be the principal cause of coma nor the driver of
outcome (Crepeau et al., 2014; Krumholz et al., 1988; Levy et al.,
1985; Snyder et al., 1980; Zandbergen et al., 2006). The
hypothesis that cardiorespiratory arrest patients with SE but other
markers indicating favorable outcome including professional
resuscitation, a short time to return of spontaneous circulation,
normal somatosensory evoked potentials, and normal neuroimag-
ing studies might benefit from rapid antiseizure therapy calls for
an increasing use of cEEG (Claassen et al., 2013; Sutter et al.,
2013a). However, in one study, cEEG after cardiorespiratory
arrest and during therapeutic hypothermia improved seizure
detection, but not outcomes, and the mean estimated EEG charges
for the cEEG cohort were significantly higher ($4214.93/patient),
as compared with the pre-cEEG controls ($1571.59/patient; P ,
0.0001)dresults questioning the use of cEEG in this context
(Crepeau et al., 2014).
Aside from brainstem reflexes, cortical N20 responses on
somatosensory evoked potentials and neuroimaging correlates of
hypoxic–ischemic injury, EEG background reactivity to stimuli and
burst-suppression pattern, nonreactive, or flat-line EEG provide
important prognostic information (Stevens and Sutter, 2013).
Acute Encephalitis
In patients with infectious encephalitides, seizures occur in up
to 13% and SE in 23% (Carrera et al., 2008; Claassen et al., 2004;
Kramer et al., 2012) (Fig. 2). In a large cohort undergoing cEEG,
central nervous system infections and metabolic encephalopathy
account for 13% of all patients with NCSE in 23% being mostly
detected by cEEG with the first 24 hours recording time (Claassen
et al., 2004). In a study, cEEG reveals mostly NCSz in one third of
ICU patients with primary central nervous system infections (Carrera

28 Copyright Ó 2016 by the American Clinical Neurophysiology Society

Journal of Clinical Neurophysiology
Volume 33, Number 1, February 2016
et al., 2008) (Fig. 2). In another study of patients with altered
consciousness at admission and short-term EEG or cEEG, the
prevalence of NCSz is reported 13% and seems to be highest among
those with infectious encephalitides (Kramer et al., 2012). However,
it remains to be determined if the use of cEEG in this context
improves outcome.
In noninfectious encephalitides, NCSz are more frequent with
almost 80% (Schmitt et al., 2012). Therefore, currently cEEG is
recommended in patients with encephalitis and an altered conscious-
ness (Claassen et al., 2013).
Acute Ischemic Stroke
Seizures are observed in more than 5% of patients with acute
ischemic strokes (Carrera et al., 2006; Giroud et al., 1994), and SE is
reported in 9% during a mean follow-up period of 3.7 years
(Labovitz et al., 2001; Velioglu et al., 2001) (Fig. 2). Nonconvulsive
status epilepticus accounts for up to 85% of early postischemic
seizures and 50% of late-onset seizures (Afsar et al., 2003). In two
thirds, early seizures emerge within 24 hours after acute ischemic
stroke (Lamy et al., 2003; Reith et al., 1997), and patients with early
poststroke seizures have an 8-fold greater risk of late seizures, as
compared with patients without early seizures (Lamy et al., 2003; So
et al., 1996). Besides the severity of acute ischemic stroke, the
synergistic adverse effect of the cytotoxic injuries from increasing
interstitial neurotransmitter levels during SE and neuronal ischemia
may increase morbidity and mortality (Waterhouse et al., 1998). This
hypothesis is strengthened by studies linking poststroke seizures
with decreased long-term survival. However, additional studies are
needed to elucidate of the role of cEEG after stroke and to identify
stroke patients with increased risk for seizures and SE (Bladin et al.,
2000; Burneo et al., 2010). Currently, the strength of recommenda-
tion for cEEG in this context seems to be weak (Claassen et al.,
2013; Sutter et al., 2013a).
QUANTITATIVE EEG FOR AUTOMATED
SEIZURE DETECTION
Recording, manual review, and interpretation of cEEG is
labor intensive. This calls for effective methods to assist in rapid and
accurate seizure detection as they would greatly reduce the costs of
cEEG monitoring and enhance the quality of patient care. The wide
range of neurologic and systemic disorders that may cause seizures
and SE in critically ill patients may result in EEG seizure patterns
that can differ substantially from seizures in patients with chronic
epilepsy in outpatient units. For example, some NCSz patterns may
strongly resemble organized rhythmic triphasic wave patterns seen in
metabolic encephalopathies (Bearden et al., 2008), and differentia-
tion between such patterns and true seizures is challenging (Kaplan
and Schlattman, 2012). Hence, current seizure detection algorithms
perform either with low sensitivity and/or a high false detection
rate in the ICUs. However, a recent preliminary investigation of
a novel ICU EEG analysis and seizure detection algorithm revealed
promising results (Sackellares et al., 2011). The new algorithm
performed on 24 prolonged EEG recordings with a mean sensitivity
of 90% and a mean false detection rate of 0.07/hour. In comparison,
two commercial detection products performed with lower sensitiv-
ities (13 and 10%) and higher false detection rates (1.04/hour and
0.01/hour). These findings suggest that the novel algorithm has
potential to be the basis of clinically useful software that can assist
ICU staff in timely identification of clinically hidden seizures and
Copyright Ó 2016 by the American Clinical Neurophysiology Society
Detect Subtle and Nonconvulsive SE
SE. Further studies on larger cohorts are needed to investigate the
performance of such novel algorithms in different critical illnesses.
EEG FOR CLOSE TREATMENT MONITORING
Besides seizure detection, cEEG is recommended for SE
treatment monitoring. Once AEDs are administered, cEEG is
required to confirm seizure cessation. In SE resistant to first-line
(i.e., benzodiazepines) and second-line AEDs (i.e., phenytoin,
valproate, levetiracetam, or phenobarbital), intravenous anesthetics
are recommended to induce an EEG burst-suppression pattern
(Holtkamp et al., 2003), or an isoelectric EEG (Kaplan, 2003)dan
algorithm in which cEEG is an integral part. However, recent single
center studies report concerning results regarding the use of
anesthetics to treat refractory SE. Increased morbidity and mortality
was reported in association with the use of anesthetics for therapeutic
coma in SE independent of important clinical confounders (Kowal-
ski et al., 2012; Marchi et al., 2015; Sutter et al., 2014). However, it
is too early to change the current treatment guidelines as the
evidence is limited to these observational single-center studies. In
addition, many patients subsequently developed NCSz after SE is
controlled (Claassen et al., 2001), but it remains unclear if prolonged
postictal monitoring ameliorates outcome.
CURRENT RECOMMENDATIONS
Based on a systematic review, the European Society of
Intensive Care Medicine published a consensus statement with
recommendations on the use of cEEG in critically ill patients
(Claassen et al., 2013)drecommendations almost congruent with
earlier American reviews (Sutter et al., 2013a). Table 2 presents
a synthesis based on the strongest current recommendations and
a tentative grading of importance of cEEG for seizure or SE
detection.
CONCLUSIONS
Continuous EEG is increasingly seen as an essential bedside
neuromonitoring device for dynamic real-time information regarding
brain function and for uncovering SE without convulsions, which is
likely to improve patients’ outcomes by early diagnosis and
shortening of SE duration. However, this time-consuming and
labor-intensive technique calls for a more targeted use in patients
with defined risk profiles for SE. Therefore, current European and
American guidelines strongly recommend the use of cEEG in
selected ICU populations with generalized convulsive SE to uncover
transformation into SSE, in refractory SE, TBI, SAH, ICH, survived
cardiac arrest, encephalitis, or in coma without primary brain injury.
They also recommend cEEG over intermittent EEG for therapy
monitoring of SE with or without treatment refractoriness. Most
recommendations are based on low levels of evidence calling for
larger prospective studies to refine guidelines for a more selective
use of cEEG.
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