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Keywords:

  • Epilepsy;
  • Nonconvulsive status epilepticus;
  • Electroencephalographic criteria;
  • Diagnosis criteria;
  • Clinical syndromes;
  • Electroencephalographic patterns;
  • Neonatal;
  • Infants;
  • Childhood;
  • Adults;
  • Late life

Summary

  1. Top of page
  2. Summary
  3. Methods
  4. Results
  5. Conclusion
  6. Disclosure
  7. References

Proceeding from the proposed classification of status epilepticus syndromes by Shorvon in 1994, we performed a systematic search for reports presenting electroencephalography (EEG) patterns of nonconvulsive status epilepticus (NCSE) on all syndromes in the classification, where possible. Using the online medical search engine PubMed for 22 different search strategies, EEG patterns supporting a diagnosis of NCSE were sought. From a total of 4,328 search results, 123 cases with corresponding EEG patterns could be allocated to underlying epilepsy syndromes. Based on the characteristic EEG patterns found for the different NCSE syndromes, we present a synthesis of the significant EEG morphologies and evolutions in the individual NCSE syndromes.

There have been many attempts at defining the electroencephalography (EEG) characteristics of nonconvulsive status epilepticus (NCSE) without a universally accepted definition. This lack of consensus arises because the EEG expression of NCSE does not exist in isolation, but reflects status epilepticus 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. Furthermore, what appears to one interpreter as status epilepticus is not to another reader, reflecting the “art” of EEG interpretation. Seizures and epilepsy syndromes have undergone an evolution that has moved beyond a classification of focal or generalized 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 progressed to incorporate the different NCSE types with clinical descriptions, but the specific EEG evidence for these types is found largely in individual reports, and often by description only. NCSE classification of EEG patterns should derive from the aggregate of published EEG patterns in the respective clinical subtype, supported by an analysis of these EEG studies. The analysis that follows presents 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, cerebral development, etiology, and syndrome.

Methods

  1. Top of page
  2. Summary
  3. Methods
  4. Results
  5. Conclusion
  6. Disclosure
  7. References

Proceeding from the proposed classification of status epilepticus syndromes (Table 1) in “Status epilepticus: its clinical features and treatment in children and adults” (Shorvon, 1994), we have performed a systematic search for reports presenting EEG patterns of NCSE using the online medical search engine PubMed (http://www.ncbi.nlm.nih.gov/sites/entrez) for the following 22 different search strategies:

Table 1. Nonconvulsive status epilepticus (NCSE) etiology or clinical context, forms, and response to treatment
SyndromeEtiology or clinical contextClinical formResponse to treatment or prognosis
  1. (adapted from the revised classifications of status epilepticus in children and adults; Shorvon, 1994)

  2. NCSE, nonconvulsive status epilepticus; CSE, convulsive status epilepticus; EEG, electroencephalography.

NCSE in the neonatal and infantile epilepsy syndromes
West syndromeVariousInfantile spasms with periods of NCSE with no clinical signs of ongoing epileptic activityPoor
Ohtahara syndromeVariousTonic spasmsPoor
Severe myoclonic epilepsy of infancy (Dravet syndrome)GeneticNonspecificPoor
NCSE in other forms of neonatal or infantile epilepsyVariousNonspecificVarious
NCSE in childhood   
Early-onset benign childhood occipital epilepsy (Panayiotopoulos syndrome)IdiopathicAutonomic status epilepticusExcellent
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 cryptogenicAtypical absence and other nonspecific formsGenerally poor
Electrical status epilepticus in slow-wave sleepVarious, usually cryptogenicNo clinical signs but ongoing electrographic activity in sleepNCSE usually remits but may leave intellectual deficits
Landau Kleffner syndromeVarious, usually cryptogenicClinical correlate of electrographic activity is severe speech disturbanceNCSE usually remits but may leave intellectual deficits
NCSE in adult life (and childhood) with epileptic encephalopathy   
NCSE in Lennox-Gastaut syndromeVarious, often cryptogenicAtypical absence status epilepticus and tonic status epilepticusPoor
NCSE in other forms of disrupted cerebral development (cryptogenic or symptomatic)Various, often cryptogenicVariousVariable
NCSE in adult life (and childhood) without epileptic encephalopathy   
Typical absence status epilepticusIdiopathic generalized epilepsyGeneralized absenceExcellent
Complex partial status epilepticus (limbic and nonlimbic origin)Various, symptomatic or cryptogenicComplex partialGood
NCSE in the postictal phase of CSEVariousConfusion state with psychiatric featuresGood
Subtle status epilepticusVariousComa with small irregular myoclonic jerksVariable
Aura continuaVarious -symptomatic or cryptogenicSimple partial (sensory, special sensory, cognitive)Good
NCSE in late adult life   
De novo absence status epilepticusPsychotropic drug withdrawal or idiopathic generalized epilepsyGeneralized absenceExcellent
Boundary syndromes   
Coma with epileptiform EEG changes
Epileptic behavioral disturbance or psychosis
Drug-induced or metabolic confusion state with epileptiform EEG changes
  1. For neonatal and infantile epilepsy syndromes “nonconvulsive status epilepticus,” “West syndrome,” “Ohtahara syndrome,” and “Dravet syndrome.”
  2. For childhood epilepsy syndromes “Panayiotopoulos syndrome,” “Ring chromosome 20 syndrome,” “Angelman syndrome,” “Rett syndrome,” “myoclonic astatic epilepsy,” “electrical status epilepticus,” and “Landau-Kleffner syndrome.”
  3. For epilepsy syndromes in childhood and adult life “Lennox-Gastaut syndrome,” “absence status epilepticus,” and “tonic status epilepticus.”
  4. For epilepsy syndromes in adulthood and late adult life “limbic status epilepticus,” “complex partial status epilepticus,” “late-onset nonconvulsive status epilepticus,” “late-life nonconvulsive status epilepticus,” “coma/nonconvulsive status epilepticus,” “epileptic psychosis,” “drug-induced status epilepticus,” and “metabolic status epilepticus.”

Electroencephalography patterns were reviewed by two EEG readers who reached consensus regarding presence of NCSE. The following criteria were used for the diagnosis of NCSE in early life as proposed in the section “Diagnosis of NCSE in children” of the Oxford conference report in 2005 (Walker et al., 2005). “A continuous or virtually continuous dysrhythmia or paroxysmal activity on the EEG is necessary. Furthermore, a continuous, abnormal electrical dysrhythmia may occur on the EEG and be difficult to equate with the clinical state. Such electrical status that occurs every time the child goes to sleep is seen in the Landau-Kleffner syndrome and some cases of Lennox-Gastaut syndrome. These continuous dysrhythmias may be acute or chronic.”

The diagnosis of NCSE ideally must consist of a combination of clinical and EEG features. Therefore, the following four clinical and electroencephalographic criteria for the 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 least 30 min. The word “clear” in the context of NCSE would imply that an adequate description of behavior before the onset of NCSE was available for comparison and the time of onset could have been defined given that the onset can be gradual and the duration of the NCSE prolonged.
  2. There must have been confirmation by clinical or neuropsychological examination of a clinical change.
  3. Continuous or virtually continuous paroxysmal episodes must have been present on the EEG.
  4. Continuous major seizures either tonic or clonic must have been absent.

All of the above criteria had to be fulfilled for the diagnosis of NCSE in early life. A clinical response to anticonvulsant medication such as intravenous/oral benzodiazepines with simultaneous improvement in the EEG and clinical symptoms added further support to the diagnosis if positive, but did not exclude the diagnosis if negative as proposed by Livingston and Brown (Livingston & Brown, 1987).

For NCSE in adults and late adult life the definition from the Oxford conference on NCSE (Walker et al., 2005) was used as follows: “The diagnosis of NCSE was primarily dependent on the presence of electrographic seizure activity. This allowed the inclusion, within the rubric of NCSE of a range of “boundary conditions” in which such activity occurred but in which there were no obvious clinical “seizures.” Electrographic seizure activity can take various forms, some of which clearly denote NCSE (clear-cut criteria) and some of which are less easy to interpret and probably denote NCSE only in some cases (equivocal criteria). The six “clear-cut” criteria included:

  1. Frequent or continuous focal electrographic seizures, with ictal patterns that wax and wane with change in amplitude, frequency, and/or spatial distribution.
  2. Frequent or continuous generalized spike wave discharges in patients without a prior history of epileptic encephalopathy or epilepsy syndrome.
  3. Frequent or continuous generalized spike-wave discharges, which showed significant changes in intensity or frequency (usually a faster frequency) when compared to baseline EEG, in patients with an epileptic encephalopathy/syndrome.
  4. Periodic lateralized epileptiform discharges (PLEDs) or bilateral independent periodic lateralized epileptiform discharges (BIPEDs) that occurred in patients in coma in the aftermath of a generalized tonic–clonic status epilepticus (subtle status epilepticus). EEG patterns, which were less easy to interpret included:
  5. Frequent or continuous EEG abnormalities (spikes, sharp waves, rhythmic slow activity, PLEDs, BIPEDs, generalized periodic epileptiform discharges (GPEDs), triphasic waves) in patients whose EEG showed no previous similar abnormalities, in the context of acute cerebral damage (e.g., anoxic brain damage, infection, trauma).
  6. Frequent or continuous generalized EEG abnormalities in patients with epileptic encephalopathies in whom similar interictal EEG patterns were seen, but in whom clinical symptoms were suggestive of NCSE.

Categories 3 and 6 reflect the problem of deciding the significance of spike-wave discharges in the setting of epileptic encephalopathy (e.g., Lennox-Gastaut syndrome) in which the ictal and interictal EEG patterns may be very similar. The differentiation of the two is problematic. Category 5 reflects the difficulty of differentiating patterns of epileptic discharges that may lie along an ictal-interictal continuum.

Results

  1. Top of page
  2. Summary
  3. Methods
  4. Results
  5. Conclusion
  6. Disclosure
  7. References

From a total of 4,328 search results, 123 cases with corresponding EEG patterns could be allocated to underlying epilepsy syndromes. Typical characteristic EEG patterns were found for the different NCSE syndromes. A synthesis of the significant EEG morphologies and evolutions of the individual NCSE syndromes arranged according to the classification of NCSE syndromes by Shorvon is provided in table 2. The corresponding EEG figures upon which our synthesis is based, can be found in the recent publication entitled “Electroencephalographic criteria for nonconvulsive status epilepticus: Synopsis and comprehensive survey” (Sutter & Kaplan, 2012).

Table 2. Prominent electrographic elements and electroencephalography (EEG) patterns for nonconvulsive status epilepticus (NCSE) syndromes
SyndromeProminent EEG patterns and evolution
  1. NCSE, nonconvulsive status epilepticus; PLEDs, periodic lateralized epileptiform discharges; GPEDs, generalized periodic epileptiform discharges; CSE, convulsive status epilepticus; EEG, electroencephalography.

NCSE in the neonatal and infantile epilepsy syndromes
West syndromeGeneralized continuous or waxing and waning high-voltage polymorphic slow wave discharges (>200 μV) 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.
Ohtahara syndromeContinuous burst-suppression pattern with repetitive bursts of high-voltage slow waves (200 to >400 μV) interspersed with multifocal, irregular spikes followed by periods of near isoelectric suppression.
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.
NCSE in other forms of neonatal or infantile epilepsyVarious forms as defined from the Oxford conference on NCSE (Walker et al., 2005).
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 μV) 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.
NCSE in other forms of childhood epileptic encephalopathies, syndromes, and etiologiesRing chromosome 20: 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.
Angelman syndrome: Generalized continuous or waxing and waning rhythmic sharp wave discharges with frontocentral predominance. Usually background activity is slow and/or suppressed.
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.
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 showed multifocal, erratic myoclonic jerks on a background of mild tonic contraction. The ictal activity then may blend into a burst-suppression pattern.
Electrical status epilepticus in slow-wave sleepGeneralized continuous rhythmic or irregular spike-and-wave discharges of up to 3 Hz during slow-wave sleep with a frontocentral, or posterior-temporal predominance. Usually background activity is slow and/or suppressed.
Landau Kleffner syndromeFocal, 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.
NCSE in adult life (and childhood) with epileptic encephalopathy 
NCSE in Lennox-Gastaut syndromeAtypical 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.
Tonic status epilepticus: Generalized repetitive runs of polyspikes at high frequencies of 16–20 Hz, beginning with low-voltage and increasing high-voltage (100 μV) 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.
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).
NCSE in adult life (and childhood) without epileptic encephalopathy 
SyndromeProminent elements or sequential arrangements
Typical absence status epilepticusGeneralized continuous or waxing and waning rhythmic 3–4 Hz spike and polyspike-slow-wave discharges predominantly anterior and usually with normal background activity.
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.
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.
NCSE in the postictal phase of CSEGeneralized 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.
Subtle status epilepticusGeneralized continuous or waxing and waning periodic epileptic discharges resembling GPEDs that may be interrupted by short periods of nearly isoelectric suppression over 3–5 s. Usually background activity is slow and/or suppressed.
Aura continuaUnilateral continuous or waxing and waning rhythmic spike-and-wave or high-voltage slow-wave discharges (>200 μV) usually with generalized slow and/or suppressed background activity.
NCSE in late adult life 
De novo absence status epilepticusGeneralized continuous or waxing and waning rhythmic 3–4 Hz spike, polyspike-slow-wave discharges predominantly anterior and usually with normal background activity.
Boundary syndromes 
Coma with epileptiform EEG changesGeneralized waxing and waning periodic epileptic discharges that resemble GPEDs with periods of nearly isoelectric suppression. Usually background activity is slow and/or suppressed.
Epileptic behavioral disturbance or psychosisVarious forms as defined from the Oxford conference on NCSE (Walker et al., 2005).
Drug-induced or metabolic confusion state with epileptiform EEG changesVarious forms as defined from the Oxford conference on NCSE (Walker et al., 2005).

Conclusion

  1. Top of page
  2. Summary
  3. Methods
  4. Results
  5. Conclusion
  6. Disclosure
  7. References

This study identifies and provides the various EEG patterns seen in NCSE from a syndromic perspective. A caveat is that published figures supporting the particular type of status epilepticus may be of inconsistent quality, warranting newer reports with better illustrations of several of the syndromes. Furthermore, some SE types lack any adequate illustrative figures. Included are borderline patterns and associations with seizures.

The compendium provides clinical and illustrative electroencephalographic descriptions that enable clinicians to approach and categorize NCSE within the context of specific syndromes with their clinical features and subtypes, rather than using previous descriptions and distinctions into complex partial (focal) and absence (generalized) subtypes. It is hoped that this compendium may help in moderating semiologic borderline disputes on NCSE.

Disclosure

  1. Top of page
  2. Summary
  3. Methods
  4. Results
  5. Conclusion
  6. Disclosure
  7. References

None of the authors has any conflict of interest to disclose.

The authors confirm that they have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

References

  1. Top of page
  2. Summary
  3. Methods
  4. Results
  5. Conclusion
  6. Disclosure
  7. References
  • Livingston JH, Brown JK. (1987) Non-convulsive status epilepticus resistant to benzodiazepines. Arch Dis Child 62:4144.
  • Shorvon SD. (1994) Status epilepticus: its clinical features and treatment in children and adults. Cambridge University Press, New York.
  • Sutter R, Kaplan PW. (2012) Electroencephalographic criteria for nonconvulsive status epilepticus: synopsis and comprehensive survey. Epilepsia 53(Suppl. 3):151.
  • 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: Epilepsy Research Foundation workshop reports. Epileptic Disord 7:253296.