NREM arousal parasomnias and their distinction from nocturnal frontal lobe epilepsy: a video EEG analysis

Abstract

Study objectives: To describe the semiological features of NREM arousal parasomnias in detail and identify features that can be used to reliably distinguish parasomnias from nocturnal frontal lobe epilepsy (NFLE).

Design: Systematic semiologial evaluation of parasomnias and NFLE seizures recorded on video-EEG monitoring.

Patients: 120 events (57 parasomnias, 63 NFLE seizures) from 44 subjects (14 males). Interventions. The presence or absence of 68 elemental clinical features was determined in parasomnias and NFLE seizures. Qualitative analysis of behavior patterns and ictal EEG was undertaken. Statistical analysis was undertaken using established techniques.

Results: Elemental clinical features strongly favoring parasomnias included: interactive behavior, failure to wake after event, and indistinct offset (all P < 0.001). Cluster analysis confirmed differences in both the frequency and combination of elemental features in parasomnias and NFLE. A diagnostic decision tree generated from these data correctly classified 94% of events. While sleep stage at onset was discriminatory (82% of seizures occurred during stage 1 or 2 sleep, with 100% of parasomnias occurring from stage 3 or 4 sleep), ictal EEG features were less useful. Video analysis of parasomnias identified three principal behavioral patterns: arousal behavior (92% of events); non-agitated motor behavior (72%); distressed emotional behavior (51%).

Conclusions: Our results broadly support the concept of confusion arousals, somnambulism and night terrors as prototypical behavior patterns of NREM parasomnias, but as a hierarchical continuum rather than distinct entities. Our observations provide an evidence base to assist in the clinical diagnosis of NREM parasomnias, and their distinction from NFLE seizures, on semiological grounds.

Figure 1

Results of the exhaustive CHAID Tree Analysis for the diagnosis of nocturnal events. This algorithm correctly identified 94% of the 120 nocturnal events in the study.

Figure 2

Schematic representation of common parasomnias, displayed as hierarchical combinations of the 3 fundamental behavior patterns on the y axis, and time (typically 1-10 min) on the x axis. Panel 1 represents a typical confusional arousal, comprising only normal arousal behaviours but of abnormal duration (19% of recorded events); panel 2 shows classical somnambulism with non-agitated motor behaviour, and normal arousal behaviours at onset, offset or both (35% of recorded events); panel 3 represents typical sleep terrors, with predominantly negative emotional behaviour often of sudden onset; calm motor and normal arousal behaviours are usually also seen during these events, either at onset or offset (26% of events); panel 4 is a mixed type, but comprising waxing and waning of the four behaviour types (19% of events). All events usually start in stage 3 or 4 NREM sleep, and end either in wakefulness or lighter NREM sleep. Sometimes episodes are brief (solid lines) and at other times prolonged (hatched lines).

Figure 3

EEG (transverse montage) during a prolonged parasomnia, showing a dissociation pattern; a clear α rhythm is seen in posterior channels consistent with the subject's posterior dominant rhythm, with anterior and midline theta activity and vertex sharp activity consistent with light NREM sleep. Timescale: 1 page = 10 seconds.

Figure 4

Schematic representation of the postulated relationship of arousal behavior to parasomnias and nocturnal seizures. During sleep, physiological stimuli (external or internal) or subclinical seizure discharges can induce indistinguishable arousal behaviors. In parasomnia subjects, these may evolve (heavy black arrows) to a clinical parasomnia or terminate with return to sleep or full waking. In individuals with nocturnal epilepsy (heavy grey arrows), clinically evident seizures with distinguishing characteristic behaviours and marked stereotypy may occur, or the event may terminate with full waking or return to sleep; it appears possible that subclinical seizures may also induce clinical parasomnias (dashed gray arrow).