Critérios de NCSE Kaplan 2012

Electroencephalographic criteria for nonconvulsive

status epilepticus: Synopsis and comprehensive survey*yRaoul Sutter and yPeter W. Kaplan

*Division of Neurosciences Critical Care, Departments of Anesthesiology and Critical Care Medicine,

The Johns Hopkins University School of Medicine, Baltimore, Maryland, U.S.A.; and yDepartment of Neurology,

The Johns Hopkins Bayview Medical Center, Baltimore, Maryland, U.S.A.

SUMMARY

There have been many attempts at defining the

electroencephalography (EEG) characteristics of

nonconvulsive status epilepticus (NCSE) without a

universally accepted definition. This lack of con-

sensus arises because the EEG expression of NCSE

does not exist in isolation, but reflects status epi-

lepticus under the variety of pathologic conditions

that occur with age, cerebral development,

encephalopathy, and epilepsy syndrome. Current

NCSE definitions include ‘‘boundary conditions,’’

in which electroencephalographic seizure activity

occurs without apparent clinical seizures. Further-

more, what appears to one interpreter as status epi-

lepticus, is not to another reader, reflecting the ‘‘art’’

of EEG interpretation. Seizures and epilepsy syn-

dromes have undergone an evolution that has

moved beyond a classification of focal or general-

ized conditions into a syndromic approach. It

seems appropriate to make similar changes in the

EEG analysis of the syndromes of NCSE. In effect,

the literature on epilepsy classification has pro-

gressed to incorporate the different NCSE types

with clinical descriptions, but the specific EEG evi-

dence for these types is found largely in individual

reports, and often by description only. NCSE clas-

sification of EEG patterns should derive from the

aggregate of published EEG patterns in the respec-

tive clinical subtype, supported by an analysis of

these EEG studies. The analysis that follows pre-

sents clinical descriptions and EEG patterns of

NCSE in the neonatal period, infancy, childhood,

adulthood, and late adulthood from a syndromic

perspective based on age, encephalopathy, cere-

bral development, etiology, and syndrome. Pro-

ceeding from the proposed classification of status

epilepticus syndromes in ‘‘Status epilepticus: its

clinical features and treatment in children and

adults’’ (published in 1994 by Cambridge Univer-

sity Press, New York), we have performed a sys-

tematic search for reports presenting EEG

patterns of NCSE using the online medical search

engine PubMed for 22 different search strategies.

EEG patterns were reviewed by two board-certi-

fied epileptologists who reached consensus

regarding presence of NCSE. From a total of 4,328

search results, 123 cases with corresponding EEG

patterns could be allocated to underlying epilepsy

syndromes. Typical characteristic, prominent

electrographic patterns, and sequential arrange-

ments are elucidated for the different NCSE syn-

dromes. This compendium of patterns by NCSE

syndrome classification with illustration of EEGs,

and delineation of electroencephalographic fea-

tures helps define the characteristics and semio-

logic borderlines among the types of NCSE.

KEY WORDS: Epilepsy, Nonconvulsive status

epilepticus, Electroencephalographic criteria,

Diagnosis criteria, Clinical syndromes, Electroen-

cephalographic patterns, Neonatal, Infants, Child-

hood, Adults, Late life.

Nonconvulsive status epilepticus (NCSE) has beendefined as a state of ongoing (or nonrecovery between)seizures without convulsions, usually for more than30 min (Shorvon, 1994; Kaplan, 1996). When diagnosingNCSE, the clinician faces challenges in correlating sug-gestive clinical features with electroencephalography(EEG) patterns to arrive at a diagnosis of NCSE. The con-

Address correspondence to Peter W. Kaplan, Department of Neurol-ogy, Johns Hopkins Bayview Medical Center, 301 Mason Lord Drive,Suite 2100, Baltimore, MD 21224, U.S.A. E-mail: [email protected] orRaoul Sutter, Division of Neurosciences Critical Care, Department ofAnesthesiology, Critical Care Medicine and Neurology, Johns HopkinsUniversity School of Medicine, Baltimore, Maryland, U.S.A. E-mail:[email protected] until July 2013; from August 2013 forward:Department of Neurology and Intensive Care Unit, University HospitalBasel, Petersgraben 4, 4031 Basel, Switzerland. E-mail [email protected]

Wiley Periodicals, Inc.ª 2012 International League Against Epilepsy

Epilepsia, 53(Suppl. 3):1–51, 2012doi: 10.1111/j.1528-1167.2012.03593.x

EEGS IN NONCONVULSIVE STATUS EPILEPTICUS

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firmation of NCSE is largely based on the EEG, given thenonspecific and pleomorphic clinical manifestations.Proposed EEG criteria for NCSE are directed mainly atforms of NCSE seen in adults (Young et al., 1996;Kaplan, 2007). This approach has not been used in pedi-atric patients, as the EEG appearance of NCSE in earlylife is fundamentally influenced by age, cerebralmaturity, presence of encephalopathy, and underlyingepilepsy syndromes, and NCSE does not lend itselfeasily to a set of EEG criteria. Several different epilepticencephalopathies occurring in neonatals, infants, andchildren may appear as continuous or subcontinuousepileptiform activity, such as in West syndrome, withhypsarrhythmia (Riikonen, 2005), and in other forms ofmalignant epilepsies of childhood, such as in Ohtahara(Ohtahara & Yamatogi, 2006) and Dravet syndrome(Dravet et al., 2005). In other less-specific cases,encephalopathy can be due to numerous etiologies,including peripartum anoxia, metabolic disorders, infec-tion, or developmental disturbances, in which NCSEmay present less-specific features.

For diagnosis, theart of and training forEEG interpretationare key to the identification of ‘‘seizures’’ or ‘‘seizure activ-ity,’’ since many epileptiform morphologies may not alonerepresent seizures. Some nonseizure, epileptiform exam-ples include ‘‘interictal’’ periodic discharges that may beseen focally, in a generalized pattern, independently/bilat-erally, or when brought out by stimulation—periodiclateralized epileptiform discharges (PLEDs), generalizedperiodic epileptiform discharges (GPEDs), bilateralindependent periodic lateralized epileptiform discharges(BIPLEDs), and stimulus-induced rhythmic, periodic, orictal discharges (SIRPIDs), respectively. These dischargeshave been described as lying along an ictal–interictal con-tinuum ranging from the interictal isolated epileptiformdischarge (Chong & Hirsch, 2005), through clustering, oran increased frequency of periodic discharges, to seizuresand status epilepticus. There has been an ongoing effortreflected in three international colloquia to define EEGcriteria of NCSE (Walker et al., 2005; Shorvon et al.,2007; Trinka & Shorvon, 2009). One challenge to this cor-ralling of EEG characteristics under one roof has been therecognition that just as there are many epilepsies, there aremany types of status epilepticus and hence NCSE. Overthe last 20 some years, with the increasing recognition ofNCSE—initially identified in ambulatory confusedpatients, and in mildly confused hospitalized patients—therehas been increasing identification in lethargic andcomatose patients in intensive care units.

EEG definitions for NCSE have been attempted byreducing the EEG analysis and diagnosis to one of patternswith particular characteristics. These were judged to reflectspecial, diagnostically important characteristics in fre-quency, amplitude, morphology, and evolution domains.Such efforts have led to criteria that may loosely fit all types

of NCSE. However, they largely and reliably are applicableto the more obvious cases of NCSE, and avoid the morecontentious middle-ground that may lie further down the ic-tal–interictal continuum. What is needed to supplementEEG definitions for NCSE is an approach contoured to thespecific settings and syndromes in which these states exist,and culled from peer-reviewed literature that establishedstatus in these cases with EEG documentation. These tai-lored characterizations would help differentiate moreclearly seizures or status epilepticus from nonseizures,leaving less of an uncertain middle-ground, and wouldreside in a syndromic context for the various NCSEs.

Previously published criteria include descriptions of themorphologies, discharge frequencies, evolution patterns,and secondary criteria for NCSE (Young et al., 1996; Cla-assen et al., 2004; Kaplan, 2007). Includedarecharacteristicsof EEG evolution, rhythmicity, and response to antiepilepticdrugs (AEDs). However, the determination of statusepilepticus on EEG is inevitably subjective. In most publi-cations on these entities, authors make the ‘‘leap’’ to adiagnosis of status epilepticus without providing objectivecriteria of frequency, amplitude, morphology, and evolu-tion of EEG characteristics, and often without showing theEEG. Illustrative figures of the EEG patterns are oftenabsent, may be ambiguous, or may show only the most evi-dent cases.

With these caveats in mind, this compendium providesthe various EEG patterns seen in NCSE from a syndromicperspective, and expands on acute symptomatic formsbased on etiology.

Material and Methods

Setting and designThis observational study was performed at the depart-

ment of Neurology, Johns Hopkins Bayview MedicalCenter in Baltimore, Maryland, U.S.A. It is a compendiumof EEG patterns for NCSE in the neonatal period, infancy,childhood, adulthood, and late life.

Data and case collectionA systematic search for case reports, case series, or

reviews presenting EEG patterns of NCSE in a syndromiccontext was performed using the online medical searchengine PubMed (http://www.ncbi.nlm.nih.gov/pubmed) for22 search strategies (Table 1) according to the proposedrevised classification of status epilepticus syndromes byShorvon (1994) (Table 2). Cases that present figures of EEGpatterns meeting the criteria for NCSE, as defined below, inassociation with underlying epilepsy or ‘‘boundary’’ syn-dromes as classified in Table 1 were selected by criticalreview of two board-certified epileptologists (RS andPWK). For all syndromes, one representative EEG figureand the corresponding clinical and EEG description wasselected. For all the other identified cases, clinical and


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R. Sutter and P. W. Kaplan

EEG descriptions are provided. The quality of images var-ied depending on the resolutions of the image sources.‘‘Boundary syndromes’’ were defined as conditions inwhich it was not clear to what extent the symptoms weredue to NCSE (Shorvon, 1994). We classified ‘‘boundarysyndromes’’ into the three following categories: (1) myo-clonic status epilepticus in coma in the context of acutesevere brain injury; (2) epileptic psychosis and behaviordisturbance; and (3) confusional states with epileptiformEEG changes (drug-induced or metabolic). In each,patients had clinical nonconvulsive symptoms with ongo-ing seizure activity on the EEG interpreted as NCSE.

Consensus on whether the EEG patterns and clinicalsyndromic descriptions were consistent with NCSE wasreached after a second critical review. The EEG criteriafor NCSE are presented below.

Criteria for NCSENCSE in early life can be viewed as an epileptic

response influenced and configured by cerebral develop-ment and integrity, the presence or absence of encephalop-athy, the underlying epilepsy syndrome, and the

neuroanatomic location of seizure activity. It denotes arange of conditions in which EEG seizure activity isprolonged and results in typical clinical nonconvulsivesyndromes.

The following criteria were used for the diagnosis ofNCSE in early life as proposed in the section ‘‘Diagnosisof NCSE in children’’ of the Oxford conference report in2005 (Walker et al., 2005). Therefore, a continuous or vir-tually continuous dysrhythmia or paroxysmal activity onEEG is necessary. Furthermore, a continuous, abnormalelectrical dysrhythmia may occur on EEG and be difficultto equate with the clinical state. Such electrical status thatoccurs every time the child goes to sleep is seen in Lan-dau-Kleffner syndrome and some cases of Lennox-Gas-taut syndrome. These continuous dysrhythmias may beacute or chronic.

The diagnosis of NCSE ideally must consist of a combi-nation of clinical and EEG features. Therefore, the follow-ing four clinical and electroencephalographic criteria forthe diagnosis of NCSE in early life were used:1 Clear clinical change in behavior (manifested as

changes in cognition, memory, arousal affect, ataxia,motor learning, and motor behavior) that lasted at least30 min. The word ‘‘clear’’ in the context of NCSEimplies that an adequate description of behavior beforethe onset of NCSE was available for comparison andthe time of onset could have been defined, given thatthe onset can be gradual and the duration of the NCSEprolonged.

2 There must have been confirmation by clinical or neu-ropsychological examination of a clinical change.

3 Continuous or virtually continuous paroxysmal epi-sodes must have been present on EEG.

4 Continuous major seizures either tonic or clonic musthave been absent.All of the above criteria had to be fulfilled for the

diagnosis of NCSE in early life. A clinical response toanticonvulsant medication such as intravenous/oral ben-zodiazepine with simultaneous improvement in theEEG and clinical symptoms added further support tothe diagnosis if positive, but did not exclude the diag-nosis if negative as proposed by Livingston & Brown(1987).

For NCSE in adults and late adulthood, the definitionfrom the Oxford conference on NCSE (Walker et al., 2005)was used as follows: (1) The diagnosis of NCSE was depen-dent primarily on the presence of electrographic seizureactivity. This allowed the inclusion, within the rubric ofNCSE, of a range of ‘‘boundary conditions’’ in which suchactivity occurred but in which there were no obvious clini-cal ‘‘seizures.’’ (2) Electrographic seizure activity can takevarious forms, some of which clearly denote NCSE (clear-cut criteria) and some of which are less easy to interpret andprobably denote NCSE only in some cases (equivocal crite-ria). The six ‘‘clear-cut’’ criteria included:

Table 1. Search strategies used for data

acquisition in PubMed

Life period Search terms

Search

results (n)

Neonatal and infantile

epilepsy syndromes

‘‘Nonconvulsive status

epilepticus [title]’’

287

‘‘West syndrome [title]’’ 378

‘‘Ohtahara syndrome [title]’’ 39

‘‘Dravet syndrome [title]’’ 106

Childhood epilepsy

syndromes

‘‘Panayiotopoulos

syndrome [title]’’

68

‘‘Ring chromosome

20 syndrome [title]’’

15

‘‘Angelman syndrome [title]’’ 465

‘‘Rett syndrome [title]’’ 1,325

‘‘Myoclonic astatic epilepsy [title]’’ 36

‘‘Electrical Status epilepticus [title]’’ 52

‘‘Landau-Kleffner syndrome [title]’’ 190

Epilepsy syndromes in

childhood and

adulthood

‘‘Lennox-Gastaut syndrome [title]’’ 274

‘‘Absence status epilepticus [title]’’ 22

‘‘Tonic status epilepticus [title]’’ 7

Epilepsy syndromes in

adulthood and

late adulthood

‘‘Limbic status epilepticus [title]’’ 33

‘‘Complex partial status

epilepticus [title]’’

91

‘‘Late-onset nonconvulsive

status epilepticus’’

52

‘‘Late-life nonconvulsive


3

‘‘Coma nonconvulsive


367

‘‘Epileptic psychosis [title]’’ 47

‘‘Drug-induced status epilepticus’’ 65

‘‘Metabolic status epilepticus’’ 406


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EEG Criteria for NCSE

Table 2. NCSE etiology or clinical context, forms, and response to treatment

Syndrome

Etiology or clinical

context Clinical form

Response to

treatment or prognosis

NCSE in the neonatal and infantile epilepsy syndromes

West syndrome Various Infantile spasms with periods of

NCSE with no clinical signs of

ongoing epileptic activity

Poor

Ohtahara syndrome Various Tonic spasms Poor

Severe myoclonic epilepsy of infancy (Dravet syndrome) Genetic Nonspecific Poor

NCSE in other forms of neonatal or infantile epilepsy Various Nonspecific Various

NCSE in childhood

Early onset benign childhood occipital epilepsy

(Panayiotopoulos syndrome)

Idiopathic Autonomic status epilepticus Excellent

NCSE in other forms of childhood epileptic

encephalopathies, syndromes, and etiologies, (e.g., ring

chromosome 20, Angelman syndrome, myoclonic–astatic

epilepsy, other childhood myoclonic encephalopathies)

Various, usually

genetic or

cryptogenic

Atypical absence and other

nonspecific forms

Generally poor

Electrical status epilepticus in slow-wave sleep Various, usually

cryptogenic

No clinical signs but ongoing

electrographic activity in sleep

NCSE usually remits

but may leave

cognitive deficits

Landau-Kleffner syndrome Various, usually

cryptogenic

Clinical correlate of

electrographic activity is

severe speech disturbance

NCSE usually remits

but may leave

cognitive deficits

NCSE in adulthood (and childhood) with epileptic

encephalopathy

NCSE in Lennox-Gastaut syndrome Various, often

cryptogenic

Atypical absence status

epilepticus and tonic status

epilepticus

Poor

NCSE in other forms of disrupted cerebral development

(cryptogenic or symptomatic)

Various, often

cryptogenic

Various Variable

NCSE in adulthood (and childhood) without epileptic

encephalopathy

Typical absence status epilepticus Idiopathic

generalized

epilepsy

Generalized absence Excellent

Complex partial status epilepticus (limbic and

nonlimbic origin)

Various -

symptomatic or

cryptogenic

Complex partial Good

NCSE in the postictal phase of TCSE Various Confusional state with psychiatric

features

Good

Subtle status epilepticus Various Coma with small irregular

myoclonic jerks

Variable

Aura continua Various -

symptomatic or

cryptogenic

Simple partial (sensory, special

sensory, cognitive)

Good

NCSE in late adulthood

De novo absence status epilepticus Psychotropic drug

withdrawal or

idiopathic

generalized

epilepsy

Generalized absence Excellent

Boundary syndromes

Coma with epileptiform EEG changes

Epileptic behavioral disturbance or psychosis

Drug-induced or metabolic confusional state with

epileptiform EEG changes

Adapted from the revised classifications of status epilepticus in children and adults according to Shorvon (1994).

NCSE, nonconvulsive status epilepticus; EEG, electroencephalography.


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1 Frequent or continuous focal electrographic seizures,with ictal patterns that wax and wane with change inamplitude, frequency, and/or spatial distribution.

2 Frequent or continuous generalized spike-wave dis-charges in patients without a previous history of epilep-tic encephalopathy or epilepsy syndrome.

3 Frequent or continuous generalized spike-wave dis-charges, which showed significant changes in intensityor frequency (usually a faster frequency) when comparedto baseline EEG, in patients with an epileptic encepha-lopathy or epilepsy syndrome.

4 PLEDs or BIPEDs that occurred in patients in coma inthe aftermath of a generalized tonic–clonic status epi-lepticus (subtle status epilepticus).

5 EEG patterns that were less easy to interpret included:Frequent or continuous EEG abnormalities (spikes,sharp-waves, rhythmic slow activity, PLEDs, BIPEDs,GPEDs, triphasic waves) in patients whose EEGsshowed no previous similar abnormalities, in thecontext of acute cerebral damage (e.g., anoxic braindamage, infection, trauma).

6 Frequent or continuous generalized EEG abnormalitiesin patients with epileptic encephalopathies in whomsimilar interictal EEG patterns were seen, but in whomclinical symptoms were suggestive of NCSE.Categories 3 and 6 reflect the problem of deciding the

significance of spike-wave discharges in the setting of epi-leptic encephalopathy (e.g., Lennox-Gastaut syndrome) inwhich the ictal and interictal EEG patterns may be verysimilar. The differentiation of the two is problematic. Cat-egory 5 reflects the difficulty of differentiating patterns ofepileptic discharges that may lie along an ictal–interictalcontinuum.

Results

From a total of 4,328 search results, 125 cases withclinical descriptions and EEG patterns met the criteriafor NCSE. For each syndrome, one representative EEGpattern is presented and reports from all identified EEGpatterns are compounded and indexed separately(Figs. 1–43). We note that the quality of the EEG fig-ures may be limited. This arises from the literature-based source of the images.

A synthesis of the significant EEG morphologies andevolutions of the individual NCSE syndromes arrangedaccording to the classification of NCSE syndromes ofShorvon (1) is provided in Table 3.

Discussion

To our knowledge, this is the first study analyzingand assembling the clinical and EEG patterns of

NCSE from a syndromic perspective. An unambigu-ous definition of NCSE that adequately covers alltypes including ‘‘boundary syndromes’’ remains elu-sive. There are several conditions in which there isgood evidence of ongoing electrographic epileptiformactivity but in which the clinical symptoms are notconventionally considered to be epileptic. The defini-tion proposed and accepted during the Oxford confer-ence on NCSE (Walker et al., 2005) defines NCSEas a range of conditions in which electrographic sei-zure activity is prolonged and results in nonconvul-sive clinical symptoms. This derives from an earlierdefinition (Shorvon, 1994). Some points are worthemphasizing. (1) The definition is dependent primarilyon the presence of electrographic seizure activity.This allows the inclusion, within the rubric of NCSE,of a range of ‘‘boundary conditions’’ as describedabove. In addition, (2) electrographic seizure activitycan take various forms. Some segments of EEG pat-terns that were presented in the reviewed reports didnot qualify for NCSE, although the clinical descrip-tions were suggestive of status and were excludedfrom this study. The reasons for exclusion wereabsence of epileptic elements, such as lack of rhyth-mic activity, lack of progression, and no waxing andwaning of ictal patterns (i.e., no change in amplitude,frequency, and/or spatial distribution). This may beexplained by the fact that the published EEG excerptsmostly show no more than 10–20 s of recording,whereas the cited changes sometimes may developover much more than just a few seconds. On studyof the illustrated electrographic NCSE patterns, partic-ular elements were identified that were seen in mostsyndromes, but were not always part of the currentsuggested criteria for NCSE (Table 3). Because theseelements may contribute substantially to recognitionand diagnosis of the corresponding NCSE syndromes,we suggest adding them to the current criteria.

Summary

This study identifies and provides the various EEG pat-terns seen in NCSE from a syndromic perspective. In addi-tion, it explores borderline patterns and associations withseizures, and it provides clinical and illustrative electroen-cephalographic descriptions that enable the clinicians toapproach and categorize NCSE within the context of spe-cific syndromes with clinical features and subtypes, ratherthan using previous distinctions into complex partial(focal) and absence (generalized) subtypes. It is hoped thatthis compendium will help in moderating semiologic bor-derline disputes on NCSE.


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Table 3. Prominent electrographic elements and EEG patterns for NCSE syndromes

Syndrome Prominent elements or sequential arrangements

NCSE in the neonatal and infantile

epilepsy syndromes

West syndrome Generalized continuous or waxing and waning high-voltage polymorphic slow wave

discharges (>200 lV) with interspersed multifocal, irregular spikes and sharp waves

usually followed by voltage attenuation and irregular 2–4 Hz slow wave discharges.

There may be periods of suppression of background activity or a continuous

burst-suppression pattern (Fig. 1A–F)

Ohtahara syndrome Continuous burst-suppression pattern with repetitive bursts of high-voltage slow waves

(200 to >400 lV) interspersed with multifocal, irregular spikes followed by periods of near

isoelectric suppression (Fig. 2A,B)

Severe myoclonic epilepsy

of infancy (Dravet syndrome)

Continuous or waxing and waning, periodic or pseudoperiodic frontal or frontotemporal spikes,

which may be followed by slow waves in the awake tracing. Spikes tend to be triphasic instead

of biphasic and subclinical discharges are slower than in Lennox–Gastaut syndrome.

There are no polyspikes in sleep, and discharges that mimic tonic discharges show no

recruiting pattern. No clinical tonic or electromyographic features on video EEG awake and

sleep records. Usually background activity is slow and/or suppressed (Fig. 3)

NCSE in other forms of neonatal or

infantile epilepsy

Various forms as defined from the Oxford conference on NCSE (Walker et al., 2005) (Figs. 4 and 5).

NCSE in childhood

Early-onset benign childhood occipital

epilepsy (Panayiotopoulos syndrome)

Waxing and waning low-voltage fast and rhythmic epileptic activity of 1–2.5 Hz predominantly

in the occipital regions, increasing in voltage (>200 lV) and decreasing in frequency with

rapid bilateral frontotemporal spreading that is followed by rhythmic spike-and-wave discharges

with occipital predominance. Usually background activity is slow and desynchronized (Fig. 6A–E)

NCSE in other forms of childhood

epileptic encephalopathies, syndromes,

and etiologies

Ring chromosome 20 syndrome: Generalized continuous or waxing and waning repetitive irregular

spikes with frontal predominance, followed by rhythmic or irregular high-amplitude slow waves

at 3–4 Hz with interspersed multifocal, irregular spikes. Usually the frequency of the

spike-and-wave discharges increases, and the slow waves can get polymorphic. Usually

background activity is slow and/or suppressed (Fig. 7A–C).

Angelman syndrome: Generalized continuous or waxing and waning rhythmic sharp wave

discharges with frontocentral predominance. Usually background activity is slow and/or

suppressed (Fig. 8A,B).

Rett syndrome: Continuous or waxing and waning unilateral, multifocal or generalized

spikes usually during 50% of slow wave sleep. Usually background activity is disorganized and

desynchronized (Fig. 9A–D).

Myoclonic-astatic epilepsy syndrome: Generalized continuous or waxing and waning slow wave

discharges of 2–3 Hz with interspersed multifocal, irregular spikes, polyspikes, and slow wave

complexes. Electromyographic channels show multifocal, erratic myoclonic jerks on a

background of mild tonic contraction. The ictal activity then may blend into a burst-suppression

pattern (Fig. 10)

Electrical status epilepticus in

slow-wave sleep

Generalized continuous rhythmic or irregular spike-and-wave discharges of up to 3 Hz during

slow-wave sleep with a frontocentral, or posterotemporal predominance. Usually background

activity is slow and/or suppressed (Fig. 12)

Landau–Kleffner syndrome Focal, multifocal or generalized continuous or nearly continuous repetitive high-voltage spike

or spike-and-wave discharges, which are activated in slow-wave sleep. The epileptic activity

usually involves the dominant temporal area. Usually background activity is slow and/or

suppressed (Fig. 13)

NCSE in adulthood (and childhood)

with epileptic encephalopathy

NCSE in Lennox–Gastaut syndrome Atypical absence status epilepticus: Generalized continuous or waxing and waning irregular

2–2.5 Hz spike and polyspike-slow-wave discharges predominantly frontotemporal and

usually with normal background activity (Fig. 14A,B).

Tonic status epilepticus: Generalized repetitive runs of polyspikes at high frequencies

of 16–20 Hz, beginning with low-voltage and increasing high-voltage (100 lV) and a

10 Hz recruiting rhythm of high-voltage from onset. The runs of polyspikes can be interspersed

with slow waves. Background activity may be disorganized and desynchronized (Fig. 15)

NCSE in other forms of disrupted cerebral

development (cryptogenic or symptomatic)

Various forms as defined from the Oxford conference on NCSE (Walker et al., 2005) (Figs 16 and 17)

Continued


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Table 3. Continued.

Syndrome Prominent elements or sequential arrangements

NCSE in adulthood (and childhood) without

epileptic encephalopathy

Typical absence status epilepticus Generalized continuous or waxing and waning rhythmic 3–4 Hz spike and polyspike-slow-wave

discharges predominantly anterior and usually with normal background activity (Fig. 18)

Complex partial status epilepticus

(limbic and nonlimbic origin)

Limbic: Continuous or waxing and waning periodic or pseudoperiodic sharp wave discharges

interspersed with low-voltage spikes and polyspike-and-waves with uni- or bilateral frontocentral

predominance and usually generalized slow and/or suppressed background activity. Waxing and

waning rhythmic delta activity, only (Fig. 19).

Nonlimbic: Continuous or waxing and waning periodic or pseudoperiodic sharp waves and

spike-and-wave discharges with unilateral, focal onset and frequent seizure progression into

generalized sharp wave and slow, and/or suppressed wave discharges usually with frontal

predominance and generalized slow background activity (Fig. 20)

NCSE in the postictal phase of TCSE Generalized or partial continuous or waxing and waning periodic epileptic discharges that resemble

PLEDs or GPEDs with a frontal predominance and usually generalized slow background

activity (Fig. 21A,B)

Subtle status epilepticus Generalized continuous or waxing and waning periodic epileptic discharges resembling GPEDs

that may be interrupted by short periods with nearly isoelectric suppression of 3–5 s.

Usually background activity is slow and/or suppressed (Fig. 22)

Aura continua Unilateral continuous or waxing and waning rhythmic spike-and-wave or high-voltage slow-wave

discharges (>200 lV) usually with generalized slow and/or suppressed background

activity (Figs. 23–30)

NCSE in late adult life

De novo absence status epilepticus Generalized continuous or waxing and waning rhythmic 3–4 Hz spike, polyspike-slow-wave

discharges predominantly anterior and usually with normal background activity (Fig. 31)

Boundary syndromes

Coma with epileptiform EEG changes Generalized waxing and waning periodic epileptic discharges that resemble GPEDs with periods of

nearly isoelectric suppression. Usually background activity is slow and/or suppressed (Fig. 34)

Epileptic behavioral disturbance or

psychosis

Various forms as defined from the Oxford conference on NCSE (Walker et al., 2005) (Figs. 36–38)

Drug-induced or metabolic confusional

state with epileptiform EEG changes

Various forms as defined from the Oxford conference on NCSE (Walker et al., 2005) (Figs. 39–43)

NCSE, nonconvulsive status epilepticus; PLEDSs, periodic lateralized epileptiform discharges; GPEDs, generalized periodic epi-

leptiform discharges.


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Electroencephalographic Illustrations

and Clinical Descriptions

Index Page1. NCSE occurring in the neonatal and infantile epilepsy syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

1a. NCSE in West syndrome (Blitz-Nick-Salaam, infantile spasms) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

1b. NCSE in Ohtahara syndrome (early infantile epileptic encephalopathy with suppression-bursts) . . . . . . . . . . . . . . 12

1c. NCSE in severe myoclonic encephalopathy of infancy (Dravet syndrome) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

1d. NCSE in other forms of neonatal or infantile epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

(i) Ring chromosome 14 syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

(ii) Systemic lupus erythematosus with encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

2. NCSE occurring only in childhood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

2a. NCSE in early onset benign childhood occipital epilepsy (Panayiotopoulos syndrome) . . . . . . . . . . . . . . . . . . . . . . 14

2b. NCSE in other forms of childhood epileptic encephalopathies, syndromes, and etiologies. . . . . . . . . . . . . . . . . . . . 16

(i) Ring chromosome 20 syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

(ii) Angelman syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

(iii) Rett syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

(iv) Myoclonic–astatic epilepsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

(v) NCSE in other myoclonic epilepsies in childhood (i.e., Lafora body disease) . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

2c. NCSE in electrical status epilepticus in slow-wave sleep (ESES) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

2d. NCSE in Landau-Kleffner syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

3. NCSE occurring in both childhood and adulthood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

With epileptic encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

3a. NCSE in the Lennox-Gastaut syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

(i) Atypical absence status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

(ii) Tonic status epilepticus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

3b. Other forms of NCSE in patients with learning disability or disturbed cerebral development (cryptogenic orsymptomatic) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

Without epileptic encephalopathy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

3c. Typical absence status epilepticus in idiopathic generalized epilepsy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

3d. Complex partial status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

(i) Limbic status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

(ii) Nonlimbic complex partial status epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

3e. NCSE in the postictal phase of tonic–clonic status epilepticus (TCSE) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30

3f. Subtle status epilepticus (myoclonic status after convulsive status epilepticus). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30

3g. Aura continua . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30

(i) Sensory symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30

(ii) Special sensory symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32

(iii) Autonomic symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32

(iv) Cognitive symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34

4. NCSE in late adulthood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35

4a. De novo absence status epilepticus of late onset . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35

4b. Other forms of NCSE in late adulthood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37


8


5. Boundary syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39

5a. Coma with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39

(i) Cryptogenic encephalitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39

(ii) Hypoxic encephalopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39

5b. Epileptic behavioral disturbance or psychosis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

5c. Drug-induced or metabolic confusional state with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45

(i) Drug-induced confusional state with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45

(ii) Metabolic confusional state with epileptiform EEG changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49


9


NCSE Occurring in the

Neonatal and Infantile Epilepsy

Syndromes

1a. NCSE in West syndrome (Blitz-Nick-Salaam,infantile spasms)

Case 1Clinical/EEG description (Saito et al., 2010): A girl

known for having West syndrome since the age of3 months. EEG during wakefulness (Fig. 1A,C–E) andsleep (Fig. 1B,F). Figure 1A,B were recorded at the age of

8 months, Figure 1C,D at the age of 1 year and 6 months,and Figure 1E,F at the age of 1 year and 8 months. Wide-spread high-voltage slow waves, spikes, and sharp wavesare observed at the age of 8 months, particularly duringsleep (Fig. 1A,B). In Figure 1C, diffuse epileptiform dis-charges occupy the tracing, when the patient showed pro-longed unresponsiveness without convulsive motions.The mother’s voice calling the name of patient (Fig. 1D;arrow) elicits a right-sided predominantly tonic seizurelasting several seconds. The epileptiform discharges arerelatively localized to the right posterior areas inFigure 1E,F.

Figure 1.

(A–F) NCSE in West syndrome (Saito et al., 2010). Calibration: Sensitivity not known.

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Case 2Clinical/EEG description (Coulter, 1986): A 3-year

6-month-old boy with known West syndrome showedrepetitive flexion of the neck and hips every 2–3 s dur-ing status epilepticus. He raised his arms, and thenrelaxed until the next spasm occurred. On some occa-sions his eyes were deviated to the right and the rightleg jerked more than the left, but flexion spasms of thehead and trunk were always present. Diffuse high-volt-age bursts of polymorphic slow waves with interspersedspikes followed by voltage attenuation; single or serialsharp waves followed by a high-voltage slow waveswith interspersed spikes and voltage attenuation; andsharp and slow waves followed by irregular 2–4 Hz

activity. Occasionally lateralized it was also at timesseen diffusely. On many occasions, the voltage attenua-tion of one spasm was terminated by the onset of thenext spasm. Scattered multifocal spikes, diffuse spikesand slow waves, and bursts of diffuse voltage attenua-tion persisted after status epilepticus.

Although EEG resembled a burst-suppression pattern atthese times, it could be distinguished because of the docu-mented clinical spasms that accompanied the periods ofvoltage attenuation. On other occasions, an individualspasm was followed by a few seconds of disorganizedslowing and multifocal spikes (hypsarrhythmia) beforethe next clinical spasm, which clearly distinguished theEEG from a burst-suppression pattern.

A

B

Figure 2.

(A,B) NCSE in Ohtahara

syndrome (Saneto & Sotero

de Menezes, 2007).

Calibration: 1 s per

horizontal unit; 100 lV per

vertical unit.

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1b. NCSE in Ohtahara syndrome (early infantileepileptic encephalopathy with suppression-bursts)

Case 1Clinical/EEG description (Saneto & Sotero de Mene-

zes, 2007): All EEG recordings from the first 5 years of agirl with Ohtahara syndrome showed a burst-suppressionpattern consisting of high-amplitude bursts, 400–2,000 lV, slow waves intermixed with multifocal spikesfollowed by near isoelectric suppression during wake andsleep states (Fig. 2A). A representative of burst-suppres-sion pattern is shown when the patient was approximately1 year old. This epoch (Fig. 2A) shows high-amplitudebursts of slow delta waves intermixed with multifocalspikes followed by near isoelectric suppression. A repre-sentative of burst-suppression pattern is presented whenthe patient was approximately 5 years old (Fig. 2B). Thisepoch shows high-amplitude bursts of slow delta waveswith reduced multifocal spikes compared with the EEGpattern seen at a younger age. This high-amplitude slow-ing is again followed by near isoelectric suppression asseen in the EEG from a younger age.

Case 2Clinical/EEG description (Fusco et al., 2001): A

53-day-old female infant had alternation betweenwakefulness with eyes open and a state of apparentsleep with eyes closed, regular respiration, and poorresponse to external stimuli. During sleep there was asubtle sign concurrent with an EEG burst discharge,

consisting of a brief arrest of respiration. Tonicspasms were continuous on awakening and duringwakefulness. In wakefulness there was a burst-suppres-sion pattern with asymmetric discharge, more evidentover the left side. There was tonic contraction of bothdeltoid muscles for the whole discharge and discontin-ued at the end of it. The discharge was spikier overthe left hemi-megalencephalic hemisphere.

Case 3Clinical/EEG description (Fusco et al., 2001): A new-

born girl showed persistent burst-suppression pattern.Each burst was associated with a complex tonic contrac-tion involving the trunk, the arms, and the neck. Repetitiveand at times periodic tonic seizures were associated withbursts of high-voltage generalized polymorphic poly-spikes with frontocentral dominance. Between the burststhere was suppression.

Case 4Clinical/EEG description (Al-Futaisi et al., 2005): A

girl with Ohtahara syndrome had suppression periods>40 s between high-amplitude 1-mV spike bursts lastingup to 5 s. Low-amplitude (30-lV) slow rhythmic (0.3–0.7 Hz) sharp and slow waves gradually built up over theright temporocentroparietal regions (T6, C4, and P4) dur-ing the period of suppression period. These rhythmic slowsharp waves and slow waves over the right hemispherepersisted during the entire EEG without clinical signs.High-amplitude bursts were off-scale at this sensitivity.

Figure 3.

NCSE in Dravet syndrome (Nabbout et al., 2008). Calibration: 1 s per horizontal unit; 100 lV per vertical unit.

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1c. NCSE in severe myoclonic encephalopathy ofinfancy (Dravet syndrome)

Case 1Clinical/EEG description (Nabbout et al., 2008): An

EEG pattern in the adolescent course. It combined fron-tal spikes (as couplet or triplet), which may have beenfollowed by slow waves on the awake tracing. Sleepmay have been activated 5–10 s of subclinical dis-charges of 8–9 Hz (Fig. 3). In Dravet syndrome, (1)spikes tend to be triphasic instead of biphasic, (2) sub-clinical discharges are slower (at 8–9 Hz) than in Len-nox-Gastaut syndrome, (3) there are no polyspikes insleep, and (4) discharges that mimic tonic dischargesshow no recruiting pattern and no clinical tonic or elec-tromyography features on video-EEG awaking andsleeping records.

There were no polyspikes in sleep, and discharges thatmimic tonic discharges show no recruiting pattern and no

clinical tonic or electromyography features on video-EEGawaking and sleeping records.

Case 2Clinical/EEG description (Moseley et al., 2011): A

10-month-old boy developed continuous right facialtwitching, left upper extremity tonic posturing, andaccompanying oxygen desaturations. EEG revealed con-tinuous generalized polyphasic periodic as well as rightfrontotemporal and left temporal epileptiform discharges.

Case 3Clinical/EEG description (Wakai et al., 1996): lctal

EEG of a 1-year 7-month-old boy disclosed persisting irreg-ular spike-and-wave complexes in the left hemisphere, pre-dominantly in the occipital and occipitotemporal areas.After administration ofdiazepam and midazolam, frequencyof the spike-and-wave complexes gradually decreased,although the occipital spikes remained.

Figure 4.

NCSE in ring chromosome 14 syndrome (Giovannini et al., 2010). Calibration: 1 s per horizontal unit; 50 lV per

vertical unit.

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1d. NCSE in other forms of neonatal or infantileepilepsy

(i) Ring chromosome 14 syndrome

Case 1Clinical/EEG description (Giovannini et al., 2010):

At the age of 15 months this boy had afebrile repeti-tive seizures during sleep with staring, loss of con-sciousness, breathing difficulties, and generalizedhypertonus, followed by four-limb clonias with a rightmild predominance, resembling status epilepticus. EEGduring seizure revealed bifrontal delta waves followedby an abrupt, 3-s flattening of background activityafter which rhythmic anterior triphasic slow waveswith intermingled spikes appeared. This was followedby left frontotemporal fast rhythmic spikes with rapiddiffusion to the right frontotemporal regions. Thisactivity rapidly generalized with prolonged irregularspike-waves, mostly 2–2.5 complexes/s, and stoppedabruptly after 2 min with a diffuse flattening, followedby the reappearance of background rhythms. EEGrecording showed bilateral frontal high-voltage contin-uous delta activity (Fig. 4; above) concomitant with abehavior characterized by confusion, hypotonia,

alternating gestural automatisms, and vegetative symp-toms. Continuous delta activity was resolved afterintravenous bolus of phenytoin (Fig. 4; below).

(ii) Systemic lupus erythematosus with encephalopathy

Case 1Clinical/EEG description (Korff & Nordli, 2007): An

11-year-old girl with systemic lupus erythematosus,seizures, and encephalopathy. EEG revealed PLEDs (pari-etal and posterior temporal irregular pseudorhythmicpolyspike-and-wave discharges) with left-hemisphere pre-dominance, but with a more diffuse manifestation (Fig. 5).

2. NCSE Occurring Only in

Childhood

2a. NCSE in early onset benign childhood occipitalepilepsy (Panayiotopoulos syndrome)

Case 1Clinical/EEG description (Specchio et al., 2010):

Ictal recording (video-EEG) of a 7-year-old girl(Fig. 6A). The ictal discharge starts in sleep over the leftoccipital area with low-voltage fast activity, increasing

Figure 5.

NCSE in systemic lupus erythematosus with encephalopathy (Korff & Nordli, 2007). Calibration: 1 s between gray

vertical lines; 100 lV between horizontal lines.

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in amplitude and decreasing in frequency, and quicklyinvolving temporal and parietal areas. This epilepticactivity persists over the right occipital area as indepen-dent spike-and-wave activity lasting 22 s. After 50 s,eyes are open and tachycardia is evident. (Fig. 6B) At3 min, discharge is bilateral, and there are more pro-nounced slow waves over left posterior area (Fig. 6C).Next there is eye deviation and vomiting with EEGcharacterized by 2.5-Hz spike-and-waves over the leftoccipital region and delta waves over the frontal andtemporal areas (Fig. 6D,E). After 7 min, the patient hascomplete loss of consciousness (Fig. 6D), after whichthe seizure ends (Fig. 6E); slow waves are evident andinvolve mainly the left hemisphere.


Ictal recording of a boy 4 years 6 months of age. Sei-zure onset is characterized by subclinical low-voltagefast activity over the right occipital region duringnon–rapid eye movement (non-REM) phase II sleep.This activity persists over 3 min and child opens hiseyes; rhythmic spikes are also evident over the rightposterior region. After 4 min, wider epileptic activity,increasing in amplitude and decreasing in frequency,is evident over the right occipital area. The child isunresponsive and the ictal discharges are more diffuse.

After 11 min, over the occipital regions, high-voltagespikes-and-waves are evident (1–2 Hz), and on thebilateral frontal areas, there are high-amplitude rhyth-mic sharp waves synchronous with the occipital activ-ity. At this stage, both tachycardia and tachypnea areevident on electrocardiography and airflow traces,respectively. The patient also has some episodes ofretching. After 15 min, diazepam is administered intra-venously and the epileptic activity becomes less rhyth-mic. After 19 min, the seizure gradually ends withslow sharp waves on the posterior regions of lowervoltage on the right side.


Ictal EEG of a child showed right temporooccipitalspikes with delta waves over the left frontal area andvertex during chewing automatisms and left eye devia-tion. After 8 min, the activity persisted and tachycardiawas evident (150 beats/min). This was followed byleft-sided eyelid clonic jerks with persistent spike-and-wave discharges, more pronounced over the right pos-terior areas, which became more rhythmic a few min-utes later during abdominal clonic jerks. Seizure endedafter midazolam was administered intravenously, anddelta waves have involved the right hemisphere withhigher amplitude over temporooccipital traces.

Figure 6.

(A–E) NCSE in Panayiotopoulos syndrome (Specchio et al., 2010). Calibration: Sensitivity not known.

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2b. NCSE in other forms of childhood epilepticencephalopathies, syndromes, and etiologies

(i) Ring chromosome 20 syndrome

Case 1Clinical/EEG description (Inoue et al., 1997): A

14-year-old girl with repetitive spikes in the rightfrontal region (Fig. 7A), followed by 3–4 Hz slowwaves and frontal dominant bilateral 3-Hz spike-and-wave complexes (Fig. 7B). Spike-and-wave complexesgradually lost the spike component with increasingfrequency and became polymorphous (Fig. 7C).

The seizure lasted 39 min. Verbal response wasimpaired to various degrees, ranging from simpleslowness, perseveration, and inappropriate utterance tomuteness.

Case 2Clinical/EEG description (Inoue et al., 1997): A 21-

year-old woman evinced frontal dominant irregular high-voltage slow waves with occasional spikes that lasted40 min. The patient looked ‘‘indifferent and weary.’’Verbal responses were short and often inappropriate.Complex mental action such as calculation or thinkingwas impossible.

Figure 7.

(A–C) NCSE in ring chromosome 20 syndrome (Inoue et al., 1997). Calibration: 1 s per horizontal unit; 50 lV per

vertical unit (as shown in Fig. 13C).

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year-old woman with seizures at the age of 7 years thatlasted up to 120 min. Frontal dominant slow-wave rhythmgradually increasing in amplitude with slow waves andspikes. The patient’s mental state fluctuated. She was muteand motionless when high-voltage slow waves becamefaster or were accompanied by spikes.


year-old man with first seizures at the age of 11 years.Irregular slow waves over the anterior region werereplaced by 3–4 Hz repetitive spikes or spike-and-wave complexes, which then decreased in frequency.The amplitude of the spikes and slow waves werehigher on the right side. He was mute and his move-ments were slow.

Case 5Clinical/EEG description (Jacobs et al., 2008): A

4-year-old boy with up to 30 seizures a day of four recog-nizable types: (1) prolonged atypical absences; (2) tonic

posturing of the arms, extension of the neck and head turn-ing to the left; (3) nocturnal hypermotor seizures withagitation; and (4) focal seizures with terror, visual halluci-nations, and impaired consciousness. EEG changes duringprolonged absences consisted of generalized suppression,2–3 Hz rhythmic slow waves and 1 Hz spike-and-slow-wave activity over both hemispheres with some focality.Variable EEG patterns with rhythmic slow waves andspike and slow waves recorded focally, followed by low-voltage fast activity during the tonic phase of the seizure.

(ii) Angelman syndrome

Case 1Clinical/EEG description (Weber, 2010): A 7-year-

old boy with developmental delay was diagnosed for thefirst time at the age of 6 months. At the age of 30 monthshe had convulsive status epilepticus and at the age of 5years he had atypical absences. He showed a change in hisbehavior with reduced activity and eye contact. His readi-ness to laugh was prominently reduced. EEG revealedcontinuous epileptic discharge with high-voltage sharpwaves (Fig. 8A,B).

A

B

Figure 8.

(A,B) NCSE in Angelman

syndrome (Weber, 2010).

Calibration: 1 s every four

vertical lines; sensitivity not

known.

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(iii) Rett syndromeCase 1

Clinical/EEG description (Nissenkorn et al., 2010):These patients with Rett syndrome showed evolution ofEEG epileptic pattern in Rett syndrome according to age:Left central spikes during sleep in a 2-year-old girl(Fig. 9A). Multifocal spikes and disorganized backgroundactivity in a 3-year 6-month-old girl (Fig. 9B). Multifocaland generalized epileptic activity during 50% of slow-wave sleep in a 6-year-old patient (Fig. 9C). Generalizedepileptic activity during sleep that fulfills the criteria forESES (electric status epilepticus during slow sleep) at theage of 7 years (Fig. 9D).

(iv) Myoclonic–astatic epilepsy

Case 1Clinical/EEG description (Guerrini & Aicardi, 2003):

A 4-year 6-month-old boy with myoclonic status epilepti-cus after carbamazepine. The child was unresponsive andin a sort of ‘‘stupor’’ accompanied by multifocal and gen-eralized myoclonic jerks. EEG showed diffuse slow waveswith intermingled multifocal, irregular spikes, and wavecomplexes (Fig. 10; left). Electromyographic channelsshowed multifocal, erratic myoclonic jerks on a back-ground of mild tonic contraction. Figure 10 (right) showspolygraphic recording performed 24 h after withdrawal of

carbamazepine in the same boy who was awake andresponsive. There was rhythmic background activity andno epileptiform activity.

Case 2Clinical/EEG description (Kobayashi et al., 2007):

EEG from a boy during a series of spasms with a burst-suppression pattern during sleep with early myoclonicencephalopathy. The ictal activity of spasms blends withthe postseries burst-suppression pattern. Myoclonusoccurs in association with EEG bursts during sleep.

(v) NCSE in other myoclonic epilepsies in childhood (i.e.,Lafora body disease)

Case 1Clinical/EEG description (Fernandez-Torre et al.,

2011): A 19-year-old woman with progressive myoclonusepilepsy of Lafora type. A tactile stimulus (Fig. 11; blackarrow) elicited a burst of epileptiform discharges in keep-ing with the definition of stimulus-induced rhythmic, peri-odic, ictal discharges (SIRPIDs).

Case 2Clinical/EEG description (Corkill & Hardie, 1999): A

15-year-old boy with eyelid myoclonia during eye closure.Frequent multifocal, spontaneous, and action myoclonic

A B

C D

Figure 9.

(A–D) NCSE in Rett syndrome (Nissenkorn et al., 2010). Calibration: 1 s per horizontal unit; 100 lV per vertical

unit.

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Figure 10.

NCSE in myoclonic–astatic epilepsy (Guerrini & Aicardi, 2003). Calibration: 1 s per horizontal unit; 100 lV per

vertical unit. Mas, masseter; Orb, oris and OO, orbicularis oris; Delt, deltoid; W Ext, wrist extensors; W Flex, wrist

flexors; APB, abductor pollicis brevis; Quad, quadriceps; L, left; R, right; AV, common average reference.

Epilepsia ILAE

Figure 11.

NCSE in other childhood myoclonic encephalopathies; Lafora body disease (Fernandez-Torre et al., 2011).

Calibration: 1 s per horizontal unit; 100 lV per vertical unit.

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jerks affected the upper limbs. EEG showed absence statusepilepticus with generalized polyspike-and-wave activitywith photosensitivity (at 10 Hz).

Case 3Clinical/EEG description (Dhamija et al., 2011): A

10-month-old boy with myoclonic jerks. During myo-clonic status epilepticus, EEG recording showed continu-ous generalized epileptiform discharges associated withbody jerking, consistent with myoclonic status epilepticus.EEG showed 1–2 Hz generalized spike-and-wave dis-charges corresponding with myoclonic jerks. A longitudi-nal bipolar EEG montage revealed maximal dischargesover bicentral parietooccipital regions.

2c. NCSE in electrical status epilepticus in slow-wavesleep (ESES)

Case 1Clinical/EEG description (Van Hirtum-Das et al.,

2006): A 5-year-old girl with receptive and expressivelanguage problems. In sleep: spike and sharp wave dis-charges over the vertex, left frontoparietal, and rightcentral head regions independently (Fig. 12; before

subpial transection). These discharges occupied >85% ofstage III sleep.

Case 2Clinical/EEG description (Tassinari et al., 2000): A

7-year-old boy during slow-wave sleep. EEG showedcontinuous, diffuse 2.5-Hz spike-and-wave activity, ofhigher amplitude on the left side. During REM sleep,diffuse spike-and-wave discharges disappeared,whereas focal left frontotemporal spikes without con-tralateral diffusion reappeared.

Case 3Clinical/EEG description (Coutelier et al., 2008): An

8-year-old girl with subtle seizures with eyelid myoclonia.Sleep-EEG showed nearly continuous and bitemporalspike-and-wave complexes, while in frontocentral areas,only slow waves were recorded.

Case 4Clinical/EEG description (Zhang et al., 2010): A

5-year-old boy had frequent epileptiform discharges whilehe was awake. During sleep the EEG revealed continuousspike-and-wave discharges.

Figure 12.

NCSE in ESES (Van Hirtum-Das et al., 2006). Calibration: 1 s between vertical lines; 100 lV per vertical unit.

Epilepsia ILAE


20


2d. NCSE in Landau-Kleffner syndrome

Case 1Clinical/EEG description (Nickels & Wirrell, 2008):

A 6-year-old boy with Landau-Kleffner syndrome hadmarkedly increased frequency of left centrotemporal peri-odic spike and slow-wave complexes during sleep(Fig. 13).

3. NCSE Occurring in Both

Childhood and Adulthood

With epileptic encephalopathy

3a. NCSE in the Lennox-Gastaut syndrome

(i) Atypical absence status epilepticus

Case 1Clinical/EEG description (Livingston & Brown,

1987): A 7-year-old girl with prolonged and recurrentfebrile seizures and drop attacks. EEG showed rhythmicand polymorphic diffuse delta activity of 1.5–2 Hz with-out response to benzodiazepines (Fig. 14A,B).

Case 2Clinical/EEG description (Dravet et al., 1986): An 8-year-

old girl with constant confusion, isolated or generalized myo-clonias, and drop attacks. Absence status with subcontinuousslowwaves, spike-and-wavesand polyspike-and-waves.

Case 3Clinical/EEG description (Ohtsuka et al., 1999): A 1-

year 10-month-old girl. At 3 years and 3 months of age,she began to have atypical absences and brief head-nod-ding seizures in addition to complex partial seizures.These atypical absences and brief head-nodding seizuresappeared in a cluster and evolved into NCSE, duringwhich she became unresponsive with frequent head nod-ding. EEG revealed multifocal spike-and-waves, whichwere mainly bilateral midtemporal. The patient’s headnodded repeatedly in a sitting position. There was adecrease in response to external stimuli. Although theelectromyogram was not recorded on this EEG, thepatient’s mother activated the marker at the time of thehead-nodding seizures. On another occasion, no dis-charges were detected by the electromyogram at the timeof the head-nodding seizures, which were associated withdiffuse spike-wave bursts.

Figure 13.

NCSE in Landau-Kleffner syndrome (Nickels & Wirrell, 2008). Calibration: 1 s between vertical lines; 30 lV/mm.

Epilepsia ILAE


21



year 3-month old girl with left-frontal spike-and-waves.The patient had frequent head-nodding seizures in a sittingposition with a decrease in response to external stimuli.Electromyogram showed that discharges from bilateraltrapezius muscles suddenly disappeared at the time of abrief atonic seizure, which was time-locked by a diffusespike-and-wave burst.


year 2-month-old boy with frequent head-nodding sei-zures in a sitting position with a decrease in response toexternal stimuli. EEG showed relatively synchronous, dif-fuse, 1.5–2 Hz slow spike-and-wave bursts (left-side dom-inant) when the patient showed a decrease in response toexternal stimuli.

Case 6Clinical/EEG description (Bauer & Trinka, 2010):

A 33-year-old woman with late onset Lennox-Gastautsyndrome (onset at age 16 years). EEG 3 days afterstart of an atypical absence status (obtundation andoccasional twitches) showed continuous generalizedsharp and slow waves at 2 Hz, dominant over the ante-rior regions. The pattern also can be read as triphasicwaves.

(ii) Tonic status epilepticus

Case 1Clinical/EEG description (Dravet et al., 1986): Tonic

status in a girl aged 11 years 7 months. Diffuse, fastrhythms followed by a burst of high-voltage polyspikesintermixed with slow waves (Fig. 15 top). Clinically: shortapnea, followed by superficial polypnea and tachycardia.

A

B

Figure 14.

(A,B) NCSE as atypical absence status epilepticus (Livingston & Brown, 1987). Calibration: 1 s per horizontal unit;

100 lV per vertical unit.

Epilepsia ILAE


22


At the end, intensive muscular activity recorded on the leftmuscles. Figure 15; bottom: A long seizure (55 s) involv-ing principally the left hemisphere, with only anteriorrapid rhythms and slow waves on the right. No clinicalexpression.

Case 2Clinical/EEG description (Tassinari et al., 1972): A

child with state of confusion with frequent myoclonicjerks, either massive, segmental or discrete. The EEGshowed nearly continuous diffuse spike-and-waves ofhigh amplitude and variable frequency, most markedanteriorly. This was followed by absence status withconfusion and discrete myoclonic jerks. EEG showeddiffuse spike and polyspike-and-wave discharges. Spikeand waves persisted between seizures with confusion.Before injection: Discharges of subcontinuous general-ized spike and waves and polyspikes-and-waves, some-times accompanied by repeated clonias recorded fromthe right deltoid. A few seconds after intravenous injec-tion of 10 mg of diazepam tonic seizures appeared withan EEG characterized by rhythmic spikes, accompaniedby intense tonic contraction.

Case 3Clinical/EEG description (Tassinari et al., 1972):

A patient with apnea and bradycardia without motor mani-festations, and on EEG fast spikes lasting 4–6 s. Thewhole episode lasted 45 min. Before activation—bursts ofangular diffuse theta waves. After generalized tonic–clo-nic seizures following intravenous injection of 500 mg ofpentylenetetrazol the EEG is characterized by diffuse,continuous slow spike-and-waves appearing immediatelyafter the postcritical depression that followed the grandmal seizure.

Case 4Clinical/EEG description (Bittencourt & Richens,

1981): Several week-long episodes of minor statusoccurred, in which this girl looked vacant, with occasionaltwitching of the face and hands. She then had tonic sei-zures with sleep or drowsiness. EEGs showed a slowspike-and-wave abnormality, sometimes with atypicalabsences and bursts of repetitive spikes. From the datasummarized it can be concluded that diazepam injected asa bolus caused tonic status epilepticus with concomitantbursts of repetitive spikes on the EEG.

Figure 15.

Tonic status epilepticus (Dravet et al., 1986). Calibration: 1 s per horizontal unit; 100 lV per vertical unit.

Epilepsia ILAE


23


A

B

Figure 16.

(A,B) NCSE in learning disability or disturbed cerebral development (Dirik et al., 2006). Calibration: 1 s between

vertical prominent lines; sensitivity not known.

Epilepsia ILAE


24


EEG record showed atypical spike-and-wave bursts,the period varying between 2 and 3 Hz. Bursts ofrepetitive spikes at 16–20 Hz and amplitudes of up to100 lV were more prominent anteriorly and series ofbursts of repetitive spikes, intercalated with largeamplitude slow waves.

3b. Other forms of NCSE in patients with learningdisability or disturbed cerebral development(cryptogenic or symptomatic)

Case 1Clinical/EEG description (Dirik et al., 2006): An 18-

month-old boy with global neurodevelopmental delay and

decreased alertness. In Figure 16A EEG during sleep statedemonstrates generalized slow-wave discharges and somespikes between slow-wave discharges. Figure 16B showsdisappearance of epileptiform activity 24 h afterintravenous valproic acid treatment; however, there is stillsome slowing.

Case 2Clinical/EEG description (Shin et al., 2011): A 7-

year-old girl with cerebral palsy and extensive bilateralpolymicrogyria. She has generalized 1–2 Hz spike andwaves over several hours while she is taking valproate,levetiracetam, and clobazam (Fig. 17A). Figure 17Bshows slowing before complete remission.

A

B

Figure 17.

(A,B) NCSE in learning disability or disturbed cerebral development (Shin et al., 2011). Calibration in A: 1 s between

prominent vertical lines; 30 mV/mm. Calibration in B: 1 s between prominent vertical lines; 7 mV/mm.

Epilepsia ILAE


25


Without epileptic encephalopathy

3c. Typical absence status epilepticus in idiopathicgeneralized epilepsy

Case 1Clinical/EEG description (Cascino,1993): Apatientwith

typical absence status epilepticus. EEG showed generalizedcontinuous 3-Hz spike-and-wave activity that is anterior pre-dominant during typical absence status epilepticus (Fig. 18).

Case 2Clinical/EEG description (Akman, 2010): In this

patient with typical absence status epilepticus EEGshowed irregular diffuse spike-and-wave discharges thatare sometimes synchronous with 3 Hz.

Case 3Clinical/EEG description (Genton et al., 2008):

Patient appeared confused, slow, drowsy. EEG showedalmost continuous generalized spike-and-wave and poly-spike-and-wave discharges at 3 Hz. Intravenous injectionof diazepam induced a transient effect, with patientregaining full consciousness, and partially recalling theevent; concomitantly EEG showed a normal backgroundactivity with only rare generalized polyspike-and-wavedischarges. After 15 min, SE reappeared with EEG show-ing pseudo rhythmic bursts of spike-and-wave and polys-pike-wave discharges.

Case 4Clinical/EEG description (Genton et al., 2008): An

adult patient with absence status characterized by mildimpairment of consciousness and by motor impersistence.EEG shows discontinuous short bursts of slow polyspike-and-waves. When asked to close his eyes, the patientrhythmically opened them concomitantly with the spikecomponent of the polyspike-and-wave complexes on theEEG, despite the reiteration of the order.

Case 5Clinical/EEG description (Korff & Nordli, 2007): A

6-year-old child with unresponsiveness and subtle twitch-ing of the corner of the mouth. EEG showed continuousrhythmic generalized spike-and-wave discharges withfrontal predominance.


2011): A 27-year-old woman known for having GTCSwith mutism and no other precipitating factors in her per-sonal history. No further description available. EEGshowed presence of continuous polyspike-and-wave andspike-and-wave complexes in keeping with the diagnosisof typical absence status epilepticus.

3d. Complex partial status epilepticus

(i) Limbic status epilepticus

Case 1Clinical/EEG description (Nahab et al., 2008): A 57-

year-old woman with a 2-month history of refractory sim-ple partial seizures. She had right upper extremity clonicmovements that progressed to a GTCS. These developedinto frequent episodes of clonic right face, arm, and occa-sionally leg movements without alteration of awareness.Epilepsia partialis continua of unclear etiology was diag-nosed. Seizure onset was seen over the left frontocentralregion. Frequent epileptiform discharges over the leftfrontocentral region correlating with clinical seizure activ-ity (Fig. 19).

Case 2Clinical/EEG description (Kirkpatrick et al., 2011): A

19-year-old woman with behavioral problems, emotionallability with religious verbalizations. She displayedpersonality changes and bizarre behaviors, responding to

Figure 18.

Typical absence status

epilepticus in idiopathic

generalized epilepsy

(Cascino, 1993).



vertical unit.

Epilepsia ILAE


26


hallucinations and reacting aggressively. EEG showedgeneralized rhythmic delta activity. The evolution of theEEG pattern is difficult to appreciate based on one 10-sepoch.

Case 3Clinical/EEG description (Bayreuther et al., 2009):

This 25-year-old woman had unusual headache, auditoryhallucinations, and extreme anxiety, consistent withpanic attacks. She had fluctuating consciousness withtemporal and spatial disorientation and recurrent chew-ing movements. Over a 4-week period she developedcomplex abnormal movements, with stereotypic epi-sodes of brief repetitive dystonic posturing of the lefthemiface and left upper limb, severe orofacial dyskine-sias leading to injury of the lips, bruxism, hypersaliva-tion, oromandibular dystonia with tongue protrusion,and episodes of opisthotonus. During the first EEG, thepatient was confused with oroalimentary automatisms.EEG showed right hemispheric 1-Hz rhythmic activity.After intravenous diazepam, the patient became respon-sive and EEG improved markedly with reappearance ofthe alpha rhythm.

Case 4Clinical/EEG description (Espay et al., 2006): A

68-year-old woman with anti-Hu antibodies, rapidlyevolving impairment in consciousness, and EEG evidenceof lateralized pseudoperiodic sharp-wave discharges.Ataxia and sensory neuropathy developed within the firsttwo weeks. EEG on admission showed predominantlyright pseudoperiodic sharp waves, spike-and-wavecomplexes, and subsequent pseudoperiodic complexes.Background was poorly organized with intermixed,almost continuous, irregular and generalized sharp waves.

Case 5Clinical/EEG description (Kaplan et al., 2012): A

51-year-old woman had a 10-month history of rapidprogressive dementia, partial seizures, sudden dystonicmovements, and hyponatremia. EEG showed waxing andwaning generalized 2–4 Hz rhythmic delta activity. After5 mg of midazolam the patient began interacting.

Case 6Clinical/EEG description (Kaplan et al., 2012): A 21-

year-old woman began having brief delusional thoughts

Figure 19.

Limbic status epilepticus (Nahab et al., 2008). Calibration: 1 s between vertical lines; sensitivity not known.

Epilepsia ILAE


27


with hallucinations, altering ‘‘between dreams andreality,’’ that became persistent. Clinical examinationrevealed unresponsiveness to voice, touch, or command,and a right gaze preference with increased tone of the fourlimbs without spontaneous movements. EEG showedanterior rhythmic 2.5–3 Hz delta waves. Background wassuppressed, runs lasted >4 s, and there was no change withnoxious stimuli, indicating that this was not frontal inter-mittent rhythmic delta activity (FIRDA).

(ii) Nonlimbic complex partial status epilepticus

Case 1Clinical/EEG description (Akman, 2010): A 2-year-

old child with left-sided pachygyria presented with inter-mittent brief habitual seizures. EEG shows continuousfocal seizure lateralized to the left hemisphere (Fig. 20).

Case 2Clinical/EEG description (Stayman & Abou-Khalil,

2011): A 51-year-old woman with evolution of bizarrebehavior such as placing her cell phone in the microwave,placing a glass tumbler into the blender while attempting

to make herself a cocktail, and perseverative behaviorssuch as repeating ‘‘channel 168’’ while manipulating thetelevision remote. She had deficits in recall, attention, andjudgment. EEG revealed irregular frontal delta activitybilaterally.

Case 3Clinical/EEG description (Sensoy et al., 2009): An 11-

month-old female infant was unconscious and responsiveto only painful stimuli at admission. Left central facialparalysis was detected and she had no swallow reflex or gagreflex. Brain magnetic resonance imaging (MRI) showedlesions in both frontotemporal lobes. EEG showed persis-tent epileptic activity at the second hospitalization.

Case 4Clinical/EEG description (Cascino, 1993): A patient

with complex partial status epilepticus with a simple par-tial onset. Simple partial onset with focal epileptiform dis-charge was seen in the right superior frontal region (F4electrode). With seizure progression there was a loss ofconsciousness and the development of generalized back-ground slowing.

Figure 20.

Nonlimbic complex partial status epilepticus (Akman, 2010). Calibration: 1 s between prominent vertical lines;

sensitivity not known.

Epilepsia ILAE


28


A

B

Figure 21.

(A,B) NCSE in the postictal phase of TCSE (Langheinrich et al., 2005). Calibration: 1 s per horizontal unit; 100 lV

per vertical unit.

Epilepsia ILAE


29


Case 5Clinical/EEG description (Kikumoto et al., 2009):

Patient at the time of diagnosis of complex partial status epi-lepticus. Ictal EEG showed 1.5–3 Hz irregular slow spikeand waves and polyspike and waves mixed with 14–16 Hzfast activity, observed predominantly in the left hemisphere.

3e. NCSE in the postictal phase of tonic–clonic statusepilepticus (TCSE)

Case 1Clinical/EEG description (Langheinrich et al., 2005):

A 39-year-old woman in a stuporous state over 6 daysafter tonic–clonic status epilepticus. On day 6 the womanwas found to be drowsy, feverish (temperature 39.0�C),not eating or drinking, slow to obey simple commands,and having attacks every few minutes; she had slight stiff-ening of the whole body with rolling up of the eyeslasting <10 s. The EEG (Fig. 21A) showed widespreadbursts of spike and slow-wave activity with a frontalpreponderance.

Case 2Clinical/EEG description (Shorvon & Trinka, 2010):

A 24-year-old woman after a GTCS with prolonged mildfluctuating impairment of consciousness. EEG showedpolyspike-and-waves, periodic generalized polyspikes-and-waves. There was preserved alpha rhythm seenbetween the generalized polyspikes-and-waves.

Case 3Clinical/EEG description (Shorvon & Trinka, 2010):

A 50-year-old man after a GTCS with prolonged postictalcoma. EEG revealed periodic lateralized epileptiformactivity over the left frontocentral leads.

Case 4Clinical/EEG description (Korff & Nordli, 2007): A 10-

year-old girl in convulsive status epilepticus. EEG obtainedafter convulsions resolved but while still unresponsiveshowedperiodic discharges ofnonconvulsive statusepilepti-cus following convulsive status epilepticus. There were righthemisphere periodic sharp waves with a slow repetition rate.

Case 5Clinical/EEG description (Korff & Nordli, 2007): A

12-year-old girl with prolonged unresponsiveness afterconvulsive status. EEG showed bilateral periodic lateral-ized epileptiform discharges (rhythmic 1 Hz spike-and-wave discharges).

3f. Subtle status epilepticus (myoclonic status afterconvulsive status epilepticus)

Case 1Clinical/EEG description (Arzimanoglou & Resnick,

2011): A 39-year-old woman with viral encephalitis and sec-ondarygeneralized convulsive status epilepticus, thencoma-tose with mild bilateral facial twitching. EEG showed subtlestatus epilepticus with generalized periodic discharges inter-rupted by short generalized flat periods (Fig. 22).

3g. Aura continua

(i) Sensory symptoms

Case 1Clinical/EEG description (Manford & Shorvon,

1992): 23-year-old man with ‘‘butterfly sensations,’’ oftenfelt in the abdomen but not specifically localized,sometimes persisting after the seizure. During prolonged

Figure 22.

Subtle status epilepticus

(Arzimanoglou & Resnick,

2011). Calibration: 1 s per


vertical unit.

Epilepsia ILAE


30


Figure 23.

Aura continua with sensory

symptoms (‘‘butterfly

sensations’’) (Manford &

Shorvon, 1992). Calibration:

1 s per horizontal unit;


Epilepsia ILAE

A

B

Figure 24.

(A,B) Aura continua with

special sensory symptoms

(anxiety) (Brigo et al., 2011).

Calibration: 1 s between

vertical lines; sensitivity

100 lV/mm.

Epilepsia ILAE


31


epigastric sensation, there was rhythmical slow activ-ity, predominantly in the right frontocentral leads (Fig. 23).

(ii) Special sensory symptoms

Case 1Clinical/EEG description (Brigo et al., 2011): A 60-

year-old with prolonged fear and anxiety. EEG showedcontinuous, rhythmic 2.5-Hz spike-and-wave activity lat-eralized to the right, with maximal amplitude in the pari-etotemporal region (Fig. 24A).

(iii) Autonomic symptoms

Case 1Clinical/EEG description (Panayiotopoulos, 2004):

A child with Panayiotopoulos syndrome. EEG (Fig. 25A)

showed high-amplitude spike-and-waves recorded fromthe bifrontal regions before onset of the electrical dis-charge, which was also purely bifrontal. Marked tachycar-dia appeared 13 min from the onset of the electricaldischarge, when this had become diffuse. There wastachycardia and ictus emeticus.

Case 2Clinical/EEG description (Koutroumanidis et al.,

2005): A 5-year-old child with emetic symptoms and otherautonomic phenomena. EEG showed bifrontal spikes thatincreased during sleep, with additional independentinterictal left centrotemporal spikes. The seizure startedfrom stage II sleep with fast activity over the bifrontal areas.After 12 min from onset he had change in heart rate from65–120 beats/min. Level of cognition fluctuated betweenreduced awareness and complete unresponsiveness.

A

B

Figure 25.

(A,B) Aura continua with

autonomic symptoms

(visceral, tachycardia)

(Panayiotopoulos, 2004).

Calibration in A: 2 s per


vertical unit. Calibration in

B: 1 s per horizontal unit;


Epilepsia ILAE


32


Figure 26.

Aura continua with cognitive symptoms (isolated alexia) (Kutluay et al., 2007). Calibration: 1 s per horizontal unit;

sensitivity not known.

Epilepsia ILAE

Figure 27.

Aura continua with cognitive

symptoms (altered memory

task, alexia, and acalculia in

ictal neuropsychological

assessment) (Profitlich et al.,



vertical unit.

Epilepsia ILAE


33


(iv) Cognitive symptoms

Case 1Clinical/EEG description (Kutluay et al., 2007): A 57-

year-old man with fluctuations in mental status and aninability to read. During the seizures he was unable toanswer questions and had nystagmoid movements of theeyes to the right. Brain MRI revealed fluid-attenuatedinversion recovery (FLAIR) hyperintensities over the left

occipitotemporal region. EEG showed ictal activity overthe left temporooccipital region with a maximal field atthe O1, T3, and T5 electrode sites and intermittent focalslowing over the left posterior head region. Four electro-graphic seizures came from the left temporooccipitalregion lasting 150–220 s. Ictal pattern started with peri-odic sharp waves from the left temporooccipital region,followed by rhythmic 8–9 Hz discharges.

Figure 28.

Aura continua with

cognitive symptoms (altered

vigilance, comprehension,

writing, ideomotor praxis,

motor and memory tasks, as

well as altered

visuoconstructive tasks and

old memory in ictal

neuropsychological

assessment) (Profitlich

et al., 2008). Calibration: 1 s

per horizontal unit; 150 lV

per vertical unit.

Epilepsia ILAE

Figure 29.

Aura continua with

cognitive symptoms (altered

mood and affect in ictal

neuropsychological

assessment) (Profitlich

et al., 2008). Calibration: 1 s

per horizontal unit; 70 lV

per vertical unit.

Epilepsia ILAE


34


Case 2Clinical/EEG description (Profitlich et al., 2008): A

42-year-old man with altered memory. Speech revealedthe use of neologisms and perseverations. Counting, nam-ing, and fluency were reduced. He had alexia, acalculia,and apraxia. EEG revealed bilateral generalized spike andspike-and-wave activity with frontal emphasis (Fig. 27).


31-year-old woman with reduced psychomotor speeds,learning, and memory. Ictal neuropsychological testshowed altered vigilance, comprehension, writing, ideo-motor praxis, motor and memory tasks, as well as alteredvisuoconstructive tasks and old memory. EEG showedcryptogenic generalized bifrontal spike activity with rightemphasis (Fig. 28).


49-year-old man with altered mood and affect. EEG

revealed cryptogenic generalized high-amplitude rhyth-mic 10–12 Hz alpha activity (Fig. 29).

Case 5Clinical/EEG description (DeToledo et al., 2000): A

69-year-old woman with episodes of inability to talk,without any other motor or cognitive impairment. Epi-sodes lasted as long as 24 h. During aphasia EEG showed3.5-Hz paroxysmal discharges (continuous spikes), maxi-mal over the right frontal and central regions (Fig. 30).

4. NCSE in Late Adulthood

4a. De novo absence status epilepticus of late onset

Case 1Clinical/EEG description (Szucs et al., 2008): A 55-

year-old woman with strange states lasting for hours ordays when she could not care for herself, was disoriented,could not perform everyday activities, and sometimesbecame paranoid and aggressive. At admission, she wasextremely slow, smiling, vague, and confused. EEG

Figure 30.

Aura continua with cognitive symptoms (isolated aphasia respectively speech arrest) (DeToledo et al., 2000).

Calibration: Sensitivity not known.

Epilepsia ILAE


35


revealed continuous, generalized, 3–4 Hz spike-and-wavepattern during her slow, disoriented state (Fig. 31).

Case 2Clinical/EEG description (Genton et al., 2008): EEG

of a 53-year-old confused, slow, and drowsy man showedalmost continuous generalized spike-and-wave and poly-spike-and-wave discharges at 3 Hz. Intravenous injectionof diazepam induced a transient effect, with patientregaining full consciousness and partially recalling theevent. After 15 min, status epilepticus reappeared withEEG showing pseudorhythmic bursts of spike-wave andpolyspike-and-wave discharges.

Case 3Clinical/EEG description (Szucs et al., 2008): A

56-year-old housewife with sparse, generalized tonic–clonic convulsions as well as frequent ‘‘smallseizures’’ with absence-like features. Her movementsand speech were unusually slow; she had small,episodic jerks of the jaw; and she seemed to be absent,disoriented, and strange. EEG showed continuous

2.5–3.5 Hz spike-and-wave pattern, which disap-peared after intravenous injection of diazepam. Herpsychomotor activity improved and she became ori-ented and responsive.

Case 4Clinical/EEG description (Szucs et al., 2008): A 63-

year-old woman with tonic–clonic seizures followed bystupor, with no verbal or metacommunicative contact; shestared in a rigid, vague way. She sat or lay and remained inforced positions in a catatonic manner. EEG showed con-tinuous, generalized, 2.5–4 Hz spike-, polyspike-and-wave pattern during patient’s stuporous state.

Case 5Clinical/EEG description (Pro et al., 2011): A 72-year-

old woman with acute onset of altered consciousness for 5 h.The episodes were characterized by acute onset of mentalconfusion and ideomotor slowing, apraxia, and speecharrest, without motor abnormalities or incontinence. EEGshowed generalized spike and polyspike-and-wave dis-charges at 3–3.5 Hz of higher voltage in the anterior regions.

Figure 31.

De novo absence status epilepticus of late onset (Szucs et al., 2008). Calibration: 1 s between prominent vertical

lines; sensitivity not known.

Epilepsia ILAE


36



2011): A 74-year-old woman with slowness in mentalactivity. She was confused and disoriented to person,time, and place. There were no automatisms ormyoclonic jerks. EEG showed nearly continuous gener-alized spike-and-wave and polyspike-and-wave dis-charges. At that time, the woman was perplexed andconfused.


2011): A 79-year-old woman with abnormal behaviorwho was confused and disoriented. When she was coma-

tose, EEG revealed continuous ongoing seizure activityconstituted by synchronous high-voltage epileptiform dis-charges with brief periods of flattening. Focal sharp waveslocalized in the left centroparietal area and vertex after theinjection of 10 mg of diazepam.

4b. Other forms of NCSE in late adulthood

Case 1Clinical/EEG description (Thomas et al., 1995): A 47-

year-old man with rhythmic bilateral clonic twitching ofthe lower part of the face, lasting up to 5 h. Opening of themouth when seizure developed provoked a brief arrest ofthe myoclonus, whereas closing the mouth did not modify

A

B

Figure 32.

(A,B) NCSE in late adulthood with opercular origin (Thomas et al., 1995). Calibration in A: 3 s per horizontal unit;

100 lV per vertical unit. Calibration in B: 1 s per horizontal unit; 75 lV per vertical unit.

Epilepsia ILAE


37


the seizures (Fig. 32B; MO = mouth open, MC = mouthclosed). EEG revealed opercular myoclonic–anarthric sta-tus epilepticus. Myoclonias were recorded as muscularpotentials over the right temporal area (associated leftfacial palsy) and produced 5–10 mm amplitude quiveringof the inferior jaw with no evidence of associated corticalepileptiform EEG activity. During recording, eyes andmouth were opened.

Case 2Clinical/EEG description (Thomas et al., 1995): A

33-year-old right-handed man with sudden expressiveaphasia lasting 5 h. Ten months later, he had perma-nent rhythmic lingual movements. EEG showedcontinuous slow periodic myoclonias occurring with3.5–4 s frequency involving the tongue and the hypo-

pharyngeal area. Top trace showed occurrence ofrhythmic, 2-Hz clonic seizure with a transient postictalsilent period. Myoclonus was preceded on surfaceEEG by a biphasic component localized over the leftinferofrontal (F3-F7) and left centrotemporal (C3-T3)areas (arrowheads). Back-averaging of 50 consecutivetraces showed that the biphasic component precededmyoclonia onset a )160 msec delay.

Case 3Clinical/EEG description (Thomas et al., 1995): A

62-year-old man developed severe permanent dysarthriawith buccofacial apraxia associated with a bilateral lowercentral facial palsy. There was no impairment of compre-hension or vigilance. Brain MRI showed a right operculartumor. EEG revealed opercular myoclonic–anarthric

A

B

Figure 33.

(A,B) NCSE in late

adulthood with sporadic

Jakob-Creutzfeldt disease

(Espinosa et al., 2010).



vertical unit.

Epilepsia ILAE


38


status epilepticus due to opercular oligodendrogliomawith recurrent left hemifacial somatomotor seizures. Sta-tus epilepticus was characterized by bilateral middle-amplitude slow myoclonias involving lips, chin, and softpalate with no evidence of associated cortical epileptiformEEG abnormality.

Case 4Clinical/EEG description (Espinosa et al., 2010): A

64-year-old woman with sporadic Jakob-Creutzfeldtdisease. Autopsy revealed spongiform changes in corti-cal and subcortical sections. Interictal EEG showedpoorly organized background, generalized slowing, andperiodic epileptiform discharges at a frequency of1–1.5 Hz greater over the right temporal region(Fig. 33A). The ictal EEG revealed bilateral synchro-nous high-amplitude, periodic sharp wave dischargesthat evolve in morphology and frequency (Fig. 33B),followed by intermittent brief diffuse suppression with-out changes in behavior.

Case 5Clinical/EEG description (Bauer & Trinka, 2010): A

65-year-old woman with Jakob-Creutzfeldt disease. Afterintravenous injection of 4 mg clonazepam, no change ofcontinuously repeated and rhythmic 1–2 Hz ‘‘triphasic’’waves, no spikes.

5. Boundary Syndromes

5a. Coma with epileptiform EEG changes

(i) Cryptogenic encephalitis


2011): A 39-year-old woman in deep coma after crypto-genic encephalitis showed continuous epileptiformdischarges consisting of rhythmic sharp waves andsharp-and-slow-wave complexes at 2.5–3 Hz (Fig. 34).

(ii) Hypoxic encephalopathy

Case 1Clinical/EEG description (Holtkamp & Meierkord,

2011): A 56-year-old comatose man after global cerebralhypoxia following ventricular fibrillation had dominatingGPEDs at 2 Hz showing maximum amplitudes in bifrontalregions (Fig. 35A). Between the bursts the EEG activitywas extremely flat. Five minutes after intravenous admin-istration of 2 mg lorazepam, GPEDs disappeared andthere was widespread low-amplitude activity at the end ofthe trace (Fig. 35B). The changes after administration ofbenzodiazepines were not associated with any clinicalimprovement.

Figure 34.

Coma with epileptiform EEG changes in cryptogenic encephalitis (Fernandez-Torre et al., 2011). Calibration: 1 s per

horizontal unit; 100 lV per vertical unit.

Epilepsia ILAE


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Case 2Clinical/EEG description (Lowenstein & Aminoff,

1992): A 72-year-old man after cardiac arrest with repeti-tive motor activity of the mouth and extremities. EEGshowed continuous spike-and-wave activity.


1992): A 31-year-old man after cardiac arrest withfrequent, stereotyped episodes in which there were clonicmovements on the left side of the face and right lowerextremity. EEG revealed mixed frequency backgroundactivity with episodic accentuation and occasional sharptransients.


1992): A 79-year-old man with idioventricular cardiac

rhythm and hypotension was unresponsive with absentpupillary light responses, oculocephalic reflex, cornealreflex, and deep tendon reflexes. No clinical seizures wereobserved. Twenty-four hours after admission he showedepisodes of repetitive sharp waves, slightly more markedon the left.


76-year-old comatose woman after status asthmaticus hadcontinuous and very regular generalized 2–3 Hz spike-and-wave activities 8 h after onset of status asthmaticus.


63-year-old man with coma after cardiac arrest showedperiodic multiple spikes on a nearly flat background activ-ity on day 2.

A

B

Figure 35.

(A,B) Coma with

epileptiform EEG changes in

hypoxic encephalopathy

(Holtkamp & Meierkord,



vertical unit.

Epilepsia ILAE


40



49-year-old woman in a coma was on respirator due tointoxication with sedative drugs. She had no brainstemreflexes and EEG showed a burst-suppression pattern.


58-year-old man with coma after cardiac arrest showed aburst-suppression pattern containing spikes with shortinterval on day 3 after the initial event.


53-year-old man in a coma after traumatic brain injury.EEG showed BIPLEDs with a unilateral burst-suppressionpattern over the right hemisphere.

5b. Epileptic behavioral disturbance or psychosis

Case 1Clinical/EEG description (Chiara et al., 2011): A

76-year-old woman with dementia looked distracted andvacant, and replied to questions after a brief pause andwith inadequate answers. She had trouble speaking, and

was uncooperative, disoriented, had a fixed gaze, andwas unresponsive to any stimuli. She had oroalimentaryautomatisms and jerking of the right foot. EEG showedtheta–delta activity with sporadic low-voltage spikesprevalent in the bilateral frontotemporal regions(Fig. 36).

Case 2Clinical/EEG description (Valko et al., 2009): A 63-

year-old right-handed woman who was confused, agitated,dysarthric, and incoherent in her thoughts had widespreadright hemispheric attenuation and periodic frontallyaccentuated focal epileptic discharges consistent with thediagnosis of a NCSE. Periodic 1.5-Hz epileptic dischargeswere seen with right frontal predominance (Fig. 37A).

Case 3Clinical/EEG description (Sethi et al., 2010): A 93-

year-old woman with acute right temporooccipital stroke.Video-EEG recording revealed frequent brief right hemi-spheric focal seizures, every 5–10 min. There was 9–10 Hz rhythmic activity in the right posterior temporalleads evolving to spread across the entire right hemispherewith intermixed sharp waves and spike-and-wave dis-charges (Fig. 38A–D).

Figure 36.

Epileptic behavioral disturbance in association with dementia (Chiara et al., 2011). Calibration: 1 s between vertical

lines; sensitivity not known.

Epilepsia ILAE


41


A

B

Figure 37.

(A,B) Epileptic behavioral disturbance in association with cerebral autosomal dominant arteriopathy with

subcortical infarcts and leukoencephalopathy (CADASIL) (Valko et al., 2009). Calibration: 1 s per horizontal unit;


Epilepsia ILAE


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A

B

Figure 38.

(A–D) Epileptic behavioral disturbance with frequent throat clearing (Sethi et al., 2010). Calibration: 1 s per

horizontal unit; 50 lV per vertical unit.

Epilepsia ILAE


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C

D

Figure 38b.

Continued.

Epilepsia ILAE


44


5c. Drug-induced or metabolic confusional state withepileptiform EEG changes

(i) Drug-induced confusion state with epileptiform EEGchanges

Case 1Clinical/EEG description (Anzellotti et al., 2011): A

64-year-old woman on cefixime followed by confusion

had continuous generalized spike or double-spike andslow-wave discharges, which were occurring at a fre-quency of 3–3.5 Hz and amplitudes of 100–120 lV(Fig. 39A), with sporadic inscription of polyspikes at afrequency of 14–15 Hz and amplitudes of 90–100 lV.

Case 2Clinical/EEG description (Thabet et al., 2009): A 15-

year-old girl on hemodialysis and cefepime who had

A

B

Figure 39.

(A,B) Drug-induced confusional state with epileptiform EEG changes by cefixime (Anzellotti et al., 2011).

Calibration: 1 s between vertical lines; sensitivity 7 lV/mm.

Epilepsia ILAE


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myoclonic arm jerks and become unresponsive. EEGrevealed generalized spike and sharp wave activity com-patible with NCSE (Fig. 40A). Repeated EEG after cefe-pime withdrawal was normal (Fig. 40B).

Case 3Clinical/EEG description (Piccinelli et al., 2000): A

12-year-old boy on tiagabine became less active and reac-

tive than usual. Subcontinuous EEG abnormalities duringNCSE with high-amplitude 3–4 Hz sharp waves withirregular runs of atypical spike-and-wave complexes overthe anterior regions of both hemispheres.

Case 4Clinical/EEG description (Knake et al., 1999): A 32-

year-old woman on tiagabine with mental clouding of

A

B

Figure 40.

(A,B) Drug-induced confusional state with epileptiform EEG changes by cefepime (Thabet et al., 2009).

Calibration: 1 s between prominent vertical lines; sensitivity 15 lV/mm.

Epilepsia ILAE


46


>4 hours. She had never experienced absences lasting formore than a minute before treatment with tiagabine. Dur-ing status epilepticus for >6 h EEG showed intermittentgeneralized slowing and spike-and-wave complexes.

Case 5Clinical/EEG description (Imperiale et al., 2003): A

30-year-old woman who developed NCSE during tiaga-bine adjunctive therapy. EEG during tiagabine-associatedNCSE episode showed diffuse slowing of background

rhythm and frequent spike-and-wave discharges on righttemporal derivations spreading to contralateral regions.After intravenous injection of 4-mg lorazepam, EEGrevealed clear improvement of background activity withappearance of left temporal spike-wave discharges associ-ated with rare contralateral sharp waves.

Case 6Clinical/EEG description (Mangano et al., 2003): A

4-year-old patient who developed NCSE following

A

B

Figure 41.

(A,B) Drug-induced confusional state with epileptiform EEG changes by tiagabine (Piccinelli et al., 2000). Calibration:

1 s per horizontal unit; 100 lV per vertical unit.

Epilepsia ILAE


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A

B

Figure 42.

(A,B) Drug-induced confusional state with epileptiform EEG changes by topiramate (Brandt et al., 2010).

Calibration: 1 s per horizontal unit; 10 lV per vertical unit.

Epilepsia ILAE


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tiagabine as add-on treatment for refractory partial sei-zures. Ictal EEG, while patient was confused and unre-sponsive, showed generalized subcontinuous spike-and-sharp-wave discharges during tiagabine.

Case 7Clinical/EEG description (Brandt et al., 2010): A 21-

year-old man with idiopathic generalized epilepsy whoingested about 8,000 mg of topiramate concentration of144.6 lg/ml. EEG showed a nearly continuously general-ized seizure pattern with changing maximum, most fre-quently left frontal respectively left frontotemporal withwide potential field (Fig. 42A,B after intravenous injec-tion of lorazepam).

(ii) Metabolic confusional state with epileptiform EEGchanges

Case 1Clinical/EEG description (Funabe et al., 2009): A

47-year-old woman with repeated unconsciousnessand abnormal behavior. The high plasma ammonialevel was not always associated with neurobehavioralsymptoms (unconsciousness, disorientation, abnormalbehavior, and epilepsy), but paroxysmal EEG dis-charges were invariably associated with these symp-toms. Intravenous injection of diazepam improvedneurobehavioral symptoms and EEG discharges(Fig. 43A: before treatment; Fig. 43B: after treatmentof citrullinemia).

A B

Figure 43.

(A,B) Metabolic confusional state with epileptiform EEG changes in citrullinemia and ammonemia in adult-onset type

II citrullinemia (CTLN2) (Funabe et al., 2009). Calibration: 1 s per horizontal unit; 50 lV per vertical unit.

Epilepsia ILAE


49


Disclosure

None of the authors has any conflicts of interest to disclose regardingthis research activity. Raoul Sutter is supported by the Research Funds ofthe University of Basel, the Scientific Society of Basel, and the GottfriedJulia Bangerter-Rhyner Foundation. We confirm that we have read theJournal’s position on issues involved in ethical publication and affirmthat this report is consistent with those guidelines.

References

Akman CI. (2010) Nonconvulsive status epilepticus and continuous spikeand slow wave of sleep in children. Semin Pediatr Neurol 17:155–162.

Al-Futaisi A, Banwell B, Ochi A, Hew J, Chu B, Oishi M, Otsubo H.(2005) Hidden focal EEG seizures during prolonged suppressionsand high-amplitude bursts in early infantile epileptic encephalopathy.Clin Neurophysiol 116:1113–1117.

Anzellotti F, Ricciardi L, Monaco D, Ciccocioppo F, Borrelli I, ZhuzhuniH, Onofrj M. (2011) Cefixime-induced nonconvulsive status epilepti-cus. Neurol Sci 33:325–329.

Arzimanoglou A, Resnick T. (2011) Diagnosing and treating epilepticdrop attacks, atypical absences and episodes of nonconvulsive statusepilepticus. Epileptic Disord 13(Suppl. 1):S1–S2.

Bauer G, Trinka E. (2010) Nonconvulsive status epilepticus and coma.Epilepsia 51:177–190.

Bayreuther C, Bourg V, Dellamonica J, Borg M, Bernardin G, Thomas P.(2009) Complex partial status epilepticus revealing anti-NMDAreceptor encephalitis. Epileptic Disord 11:261–265.

Bittencourt PR, Richens A. (1981) Anticonvulsant-induced status epilep-ticus in Lennox–Gastaut syndrome. Epilepsia 22:129–134.

Brandt C, Elsner H, Furatsch N, Hoppe M, Nieder E, Rambeck B, EbnerA, May TW. (2010) Topiramate overdose: a case report of a patientwith extremely high topiramate serum concentrations and nonconvul-sive status epilepticus. Epilepsia 51:1090–1093.

Brigo F, Ferlisi M, Fiaschi A, Bongiovanni LG. (2011) Fear as the onlyclinical expression of affective focal status epilepticus. EpilepsyBehav 20:107–110.

Cascino GD. (1993) Nonconvulsive status epilepticus in adults and chil-dren. Epilepsia 34(Suppl. 1):S21–S28.

Chiara C, Giovanni A, Giovanni P, Antonella B, Federica A, FrancescaU, Fabrizio V, Mario T. (2011) Nonconvulsive seizures and demen-tia: a case report. Int J Alzheimers Dis Apr 13:690305.

Chong DJ, Hirsch LJ. (2005) Which EEG patterns warrant treatment inthe critically ill? Reviewing the evidence for treatment of periodicepileptiform discharges and related patterns. J Clin Neurophysiol22:79–91.

Claassen J, Mayer SA, Kowalski RG, Emerson RG, Hirsch LJ. (2004)Detection of electrographic seizures with continuous EEG monitor-ing in critically ill patients. Neurology 62:1743–1748.

Corkill RG, Hardie RJ. (1999) An unusual case of Lafora body disease.Eur J Neurol 6:245–247.

Coulter DL. (1986) Continuous infantile spasms as a form of status epi-lepticus. J Child Neurol 1:215–217.

Coutelier M, Andries S, Ghariani S, Dan B, Duyckaerts C, van Rijckevor-sel K, Raftopoulos C, Deconinck N, Sonderegger P, Scaravilli F,Vikkula M, Godfraind C. (2008) Neuroserpin mutation causes electri-cal status epilepticus of slow-wave sleep. Neurology 71:64–66.

DeToledo JC, Minagar A, Lowe MR. (2000) Persisting aphasia as thesole manifestation of partial status epilepticus. Clin Neurol Neuro-surg 102:144–148.

Dhamija R, Moseley BD, Wirrell EC. (2011) Clinical reasoning: a 10-month-old boy with myoclonic status epilepticus. Neurology 76:e22–e25.

Dirik E, Yis U, H�daoglu O, Kurul S. (2006) Nonconvulsive statusepilepticus and neurodevelopmental delay. Pediatr Neurol 35:209–212.

Dravet C, Natale O, Magaudda A, Larrieu JL, Bureau M, Roger J, Tassi-nari CA. (1986) Status epilepticus in the Lennox–Gastaut syndrome.Rev Electroencephalogr Neurophysiol Clin 15:361–368.

Dravet C, Bureau M, Oguni H, Fukuyama Y, Cokar O. (2005) Severemyoclonic epilepsy in infancy: Dravet syndrome. Adv Neurol 95:71–102.

Espay AJ, Kumar V, Sarpel G. (2006) Anti-Hu-associated paraneoplasticlimbic encephalitis presenting as rapidly progressive non-convulsivestatus epilepticus. J Neurol Sci 246:149–152.

Espinosa PS, Bensalem-Owen MK, Fee DB. (2010) Sporadic Creutz-feldt-Jakob disease presenting as nonconvulsive status epilepticuscase report and review of the literature. Clin Neurol Neurosurg112:537–540.

Fernandez-Torre JL, Rebollo M, Gutierrez A, Lopez-Espadas F, Hernan-dez-Hernandez MA. (2011) Nonconvulsive status epilepticus inadults: electroclinical differences between proper and comatoseforms. Clin Neurophysiol 123:244–251.

Funabe S, Tanaka R, Urabe T, Kawasaki S, Kobayashi K, Hattori N.(2009) A case of adult-onset type II citrullinemia with repeated non-convulsive status epilepticus. Rinsho Shinkeigaku 49:571–575.

Fusco L, Pachatz C, Di Capua M, Vigevano F. (2001) Video/EEG aspectsof early-infantile epileptic encephalopathy with suppression-bursts(Ohtahara syndrome). Brain Dev 23:708–714.

Genton P, Ferlazzo E, Thomas P. (2008) Absence status epilepsy: delin-eation of a distinct idiopathic generalized epilepsy syndrome. Epilep-sia 49:642–649.

Giovannini S, Frattini D, Scarano A, Fusco C, Bertani G, Della GiustinaE, Martinelli P, Orteschi D, Zollino M, Neri G, Gobbi G. (2010) Par-tial epilepsy complicated by convulsive and nonconvulsive episodesof status epilepticus in a patient with ring chromosome 14 syndrome.Epileptic Disord 12:222–227.

Guerrini R, Aicardi J. (2003) Epileptic encephalopathies with myoclonicseizures in infants and children (severe myoclonic epilepsy and myo-clonic-astatic epilepsy). J Clin Neurophysiol 20:449–461.

Holtkamp M, Meierkord H. (2011) Nonconvulsive status epilepticus: adiagnostic and therapeutic challenge in the intensive care setting.Ther Adv Neurol Disord 4:169–181.

Imperiale D, Pignatta P, Cerrato P, Montalenti E, Ravetti C, BennaP. (2003) Nonconvulsive status epilepticus due to a de novo contra-lateral focus during tiagabine adjunctive therapy. Seizure 12:319–322.

Inoue Y, Fujiwara T, Matsuda K, Kubota H, Tanaka M, Yagi K, Yama-mori K, Takahashi Y. (1997) Ring chromosome 20 and nonconvul-sive status epilepticus. A new epileptic syndrome. Brain 120:939–953.

Jacobs J, Bernard G, Andermann E, Dubeau F, Andermann F. (2008)Refractory and lethal status epilepticus in a patient with ring chromo-some 20 syndrome. Epileptic Disord 10:254–259.

Kaplan PW. (1996) Nonconvulsive status epilepticus. Semin Neurol16:33–40.

Kaplan PW. (2007) EEG criteria for nonconvulsive status epilepticus.Epilepsia 48(Suppl. 8):39–41.

Kaplan PW, Rossetti AO, Kaplan EH, Wieser H-G. (2012) Proposition:limbic encephalitis may represent limbic status epilepticus. A reviewof clinical and EEG characteristics. Epilepsy Behav 24:1–16.

Kikumoto K, Yoshinaga H, Kobayashi K, Oka M, Ohtsuka Y. (2009)Complex partial status epilepticus in children with epilepsy. BrainDev 31:148–157.

Kirkpatrick MP, Clarke CD, Sonmezturk HH, Abou-Khalil B. (2011)Rhythmic delta activity represents a form of nonconvulsive status ep-ilepticus in anti-NMDA receptor antibody encephalitis. EpilepsyBehav 20:392–394.

Knake S, Hamer HM, Schomburg U, Oertel WH, Rosenow F. (1999) Ti-agabine-induced absence status in idiopathic generalized epilepsy.Seizure 8:314–317.

Kobayashi K, Inoue T, Kikumoto K, Endoh F, Miya K, Oka M, Yoshina-ga H, Ohtsuka Y. (2007) Relation of spasms and myoclonus to sup-pression-burst on EEG in epileptic encephalopathy in early infancy.Neuropediatrics 38:244–250.

Korff CM, Nordli DR Jr. (2007) Diagnosis and management of noncon-vulsive status epilepticus in children. Nat Clin Pract Neurol 3:505–516.

Koutroumanidis M, Rowlinson S, Sanders S. (2005) Recurrent auto-nomic status epilepticus in Panayiotopoulos syndrome: video/EEGstudies. Epilepsy Behav 7:543–547.


50


Kutluay E, Pakoz B, Yuksel A, Beydoun A. (2007) Nonconvulsive statusepilepticus manifesting as pure alexia (alexia without agraphia). Epi-lepsy Behav 10:626–628.

Langheinrich TC, Chattopadhyay A, Kuc S, Reuber M. (2005) Prolongedpostictal stupor: nonconvulsive status epilepticus, medication effect,or postictal state? Epilepsy Behav 7:548–551.

Livingston JH, Brown JK. (1987) Non-convulsive status epilepticusresistant to benzodiazepines. Arch Dis Child 62:41–44.

Lowenstein DH, Aminoff MJ. (1992) Clinical and EEG features of statusepilepticus in comatose patients. Neurology 42:100–104.

Manford M, Shorvon SD. (1992) Prolonged sensory or visceral symp-toms: an under-diagnosed form of non-convulsive focal (simple par-tial) status epilepticus. J Neurol Neurosurg Psychiatry 55:714–716.

Mangano S, Cusumano L, Fontana A. (2003) Non-convulsive status epi-lepticus associated with tiagabine in a pediatric patient. Brain Dev25:518–521.

Moseley BD, Wirrell EC, Nickels K. (2011) Generalized periodic epilep-tiform discharges in a child with Dravet syndrome. J Child Neurol26:907–910.

Nabbout R, Desguerre I, Sabbagh S, Depienne C, Plouin P, Dulac O,Chiron C. (2008) An unexpected EEG course in Dravet syndrome.Epilepsy Res 81:90–95.

Nahab F, Heller A, Laroche SM. (2008) Focal cortical resection for com-plex partial status epilepticus due to a paraneoplastic encephalitis.Neurologist 14:56–59.

Nickels K, Wirrell E. (2008) Electrical status epilepticus in sleep. SeminPediatr Neurol 15:50–60.

Nissenkorn A, Gak E, Vecsler M, Reznik H, Menascu S, Ben Zeev B.(2010) Epilepsy in Rett syndrome – the experience of a National RettCenter. Epilepsia 51:1252–1258.

Ohtahara S, Yamatogi Y. (2006) Ohtahara syndrome: with special refer-ence to its developmental aspects for differentiating from early myo-clonic encephalopathy. Epilepsy Res 70(Suppl. 1):S58–S67.

Ohtsuka Y, Sato M, Oka E. (1999) Nonconvulsive status epilepticus inchildhood localization-related epilepsy. Epilepsia 40:1003–1010.

Panayiotopoulos CP. (2004) Autonomic seizures and autonomic statusepilepticus peculiar to childhood: diagnosis and management. Epi-lepsy Behav 5:286–295.

Piccinelli P, Borgatti R, Perucca E, Tofani A, Donati G, Balottin U.(2000) Frontal nonconvulsive status epilepticus associated with high-dose tiagabine therapy in a child with familial bilateral perisylvianpolymicrogyria. Epilepsia 41:1485–1488.

Pro S, Vicenzini E, Randi F, Pulitano P, Mecarelli O. (2011) Idiopathiclate-onset absence status epilepticus: a case report with an electro-clinical 14 years follow-up. Seizure 20:655–658.

Profitlich T, Hoppe C, Reuber M, Helmstaedter C, Bauer J. (2008) Ictalneuropsychological findings in focal nonconvulsive status epilepti-cus. Epilepsy Behav 12:269–275.

Riikonen R. (2005) The latest on infantile spasms. Curr Opin Neurol18:91–95.

Saito Y, Sugai K, Nakagawa E, Sakuma H, Komaki H, Sasaki M, Hoshi-no K. (2010) Non-convulsive status epilepticus and audiogenic sei-zures complicating a patient with asymmetrical epileptic spasms.Brain Dev 32:583–587.

Saneto RP, Sotero de Menezes M. (2007) Persistence of suppression-bursts in a patient with Ohtahara syndrome. J Child Neurol 22:631–634.

Sensoy G, Sayli TR, Guven A, Kanmaz G. (2009) Infantile nonconvul-sive status epilepticus caused by herpes encephalitis. J Pediatr Neu-rosci 4:139–141.

Sethi NK, Torgovnick J, Sethi PK, Arsura E. (2010) Nonconvulsive sta-tus epilepticus presenting with throat clearing as part of clinical sei-zure semiology. Clin EEG Neurosci 41:50–52.

Shin HW, O’Donovan CA, Boggs JG, Grefe A, Harper A, Bell WL,McCall WV, Rosenquist P. (2011) Successful ECT treatment formedically refractory nonconvulsive status epilepticus in pediatricpatient. Seizure 20:433–436.

Shorvon SD. (1994) Status epilepticus: its clinical features and treatmentin children and adults. Cambridge University Press, New York.

Shorvon S, Trinka E. (2010) Nonconvulsive status epilepticus and the po-stictal state. Epilepsy Behav 19:172–175.

Shorvon SD, Trinka E, Walker MC. (2007) The proceedings ofthe First London Colloquium on Status Epilepticus – UniversityCollege London, April 12-15, 2007. Introduction. Epilepsia 48(Sup-pl. 8):1–3.

Specchio N, Trivisano M, Claps D, Battaglia D, Fusco L, Vigevano F.(2010) Documentation of autonomic seizures and autonomic statusepilepticus with ictal EEG in Panayiotopoulos syndrome. EpilepsyBehav 19:383–393.

Stayman A, Abou-Khalil B. (2011) FDG-PET in the diagnosis of com-plex partial status epilepticus originating from the frontal lobe. Epi-lepsy Behav 20:721–724.

Szucs A, Barcs G, Jakus R, Rasonyi G, Lalit N, Hollo A, Kelemen A,Janszky J, Halasz P. (2008) Late-life absence status epilepticus: afemale disorder? Epileptic Disord 10:156–161.

Tassinari CA, Dravet C, Roger J, Cano JP, Gastaut H. (1972)Tonic status epilepticus precipitated by intravenous benzodiazepinein five patients with Lennox–Gastaut syndrome. Epilepsia 13:421–435.

Tassinari CA, Rubboli G, Volpi L, Meletti S, d’Orsi G, Franca M, SabettaAR, Riguzzi P, Gardella E, Zaniboni A, Michelucci R. (2000)Encephalopathy with electrical status epilepticus during slow sleepor ESES syndrome including the acquired aphasia. Clin Neurophysiol111(Suppl. 2):94–102.

Thabet F, Al Maghrabi M, Al Barraq A, Tabarki B. (2009) Cefepime-induced nonconvulsive status epilepticus: case report and review.Neurocrit Care 10:347–351.

Thomas P, Borg M, Suisse G, Chatel M. (1995) Opercular myoclonic-an-arthric status epilepticus. Epilepsia 36:281–289.

Trinka E, Shorvon S. (2009) The proceedings of the innsbruck collo-quium on status epilepticus. Epilepsia 50(Suppl. 12):1–2.

Valko PO, Siccoli MM, Schiller A, Wieser HG, Jung HH. (2009) Non-convulsive status epilepticus causing focal neurological deficits inCADASIL. BMJ Case Rep bcr.07.2008.0529.

Van Hirtum-Das M, Licht EA, Koh S, Wu JY, Shields WD, Sankar R.(2006) Children with ESES: variability in the syndrome. EpilepsyRes 70(Suppl. 1):S248–S258.

Wakai S, Ikehata M, Nihira H, Ito N, Sueoka H, Kawamoto Y, HayasakaH, Chiba S. (1996) ‘‘Obtundation status (Dravet)’’ caused by complexpartial status epilepticus in a patient with severe myoclonic epilepsyin infancy. Epilepsia 37:1020–1022.

Walker M, Cross H, Smith S, Young C, Aicardi J, Appleton R, Aylett S,Besag F, Cock H, DeLorenzo R, Drislane F, Duncan J, Ferrie C,Fujikawa D, Gray W, Kaplan P, Koutroumanidis M, O’Regan M,Plouin P, Sander J, Scott R, Shorvon S, Treiman D, Wasterlain C,Wieshmann U. (2005) Nonconvulsive status epilepticus: epilepsyresearch foundation workshop reports. Epileptic Disord 7:253–296.

Weber P. (2010) Levetiracetam in nonconvulsive status epilepticus in achild with Angelman syndrome. J Child Neurol 25:393–396.

Young GB, Jordan KG, Doig GS. (1996) An assessment of nonconvul-sive seizures in the intensive care unit using continuous EEG moni-toring: an investigation of variables associated with mortality.Neurology 47:83–89.

Zhang J, Talley G, Kornegay AL, Edwards JC. (2010) Electrical statusepilepticus during sleep: a case report and review of the literature. AmJ Electroneurodiagnostic Technol 50:211–218.


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