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mise à jour du
10 mars 2005
Epilepsia
2002; 43; 11; 1372-1378
lexique
Hyperventilation-induced high-amplitude rhythmic slowing with altered awareness: a video-EEG comparison with absence seizures
Leanna M. Lum, Mary B. Connolly, Kevin Farrell, Peter K. H. Wong

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Purpose: Hyperventilation-induced high-amplitude rhythmic slowing (HIHARS) in children may be associated with clinical episodes of altered awareness. The presence of automatisms has been proposed as a distinguishing feature that helps to differentiate absence seizures from nonepileptic causes of decreased responsiveness. This retrospective, controlled, video-EEG study compared the clinical characteristics of episodes of HIHARS with loss of awareness with those of absence seizures.
 
Methods: The database of a tertiary Children's Hospital was searched for patients studied between April 1993 and April 1997 who had at least one episode of HIHARS with loss of awareness. The absence control group was obtained by selecting the next patient, after an HIHARS study subject, who met the following criteria: (a) had at least one absence seizure occurred during hyperventilation in the EEG recording, and (b) had a diagnosis of idiopathic generalized epilepsy. The video-EEG and medical histories of all patients were reviewed and summarized.
 
Results: We reviewed video-EEG recordings of 77 episodes of HIHARS with loss of awareness from 22 children and 107 absence seizures during hyperventilation from 22 children. Eye opening and eyelid flutter were seen more frequently in absence seizures, whereas fidgeting, smiling, and yawning occurred more frequently during HIHARS episodes. Arrest of activity, staring, and oral and manual automatisms were observed in both groups.
 
Conclusions: Automatisms are common in both HIHARS and absence seizures. Yawning, smiling, and particularly fidgeting occur more commonly and eye opening and eyelid flutter less commonly in HIHARS. However, episodes of HIHARS with loss of awareness clinically mimic absence seizures, and these conditions can be distinguished reliably only by EEG.
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DISCUSSION
 
Reduction in consciousness during voluntary HV was first reported by Davis and Davis (10) in 1939, when failure to respond to commands was observed with 2- to 3-Hz high-voltage sinusoidal activity. In 1947, Engel (1) described loss of consciousness and arrest of HV, with resumption of HV as the level of consciousness returned in six of nine patients. Consciousness was tested during the last 30 s of a 3-min HV period by presenting the patient with three objects to remember and with a multiplication problem. The reduction of consciousness correlated with the degree of EEG slowing and was most marked when frequency was < 5 Hz.
 
The first description of episodes of HIHARS with loss of awareness was in an abstract entitled "Pseudoabsences" (6). Three children were described with "extremely unusual" stereotyped attacks during HV, and the authors considered that these were nonepileptic events. Subsequent reports of episodic, altered awareness during HIHARS speculated on whether these episodes are epileptic seizures (3-5) or nonepileptic phenomena (2,6,7). In a study of 12 children with the EEG criteria for HIHARS, verbal recall and motor responsiveness to an auditory click were normal at baseline and during HV before slowing, but all children exhibited impaired verbal recall, and eight of 12 failed to respond to auditory clicks during an episode of HIHARS (2). The authors concluded that responsiveness could be impaired in healthy children without epilepsy. In that study, automatisms were not observed during the episodes of HIHARS, and the authors concluded that the presence of automatisms helped to differentiate absence seizures from nonepilepsy causes of decreased responsiveness.
 
The present study is the first to use video-EEG to analyze the clinical features of the episodes of HIHARS and to compare the data with those from a control population of children with absence seizures. Unlike Epstein et al. (2), we observed automatisms in all of our 22 patients. Automatism also were described in most other reports of HIHARS and altered awareness (3-7). Although automatisms were common in both the HIHARS and the absence control group, eye opening and eyelid flutter were seen more frequently in absence seizures. In contrast, fidgeting, smiling, and yawning occurred more frequently during HIHARS episodes. Yawning (3,6) and smiling (6) have been described previously as automatisms in HIHARS patients. Indeed, in his initial description of altered awareness during 11V, Engel (1) described excessive sighing and yawning. Arrest of activity, staring, and automatisms, both oral and manual, were observed in both groups. Although there are some differences in the patterns of automatisms between HIHARS and absence seizures, only fidgeting occurred exclusively in the HIHARS group, and the distinction between HIHARS and absence seizures can be made reliably only by using EEG.
 
The design of our study does not permit us to determine whether HIHARS is an epileptic seizure or a nonepileptic phenomenon. HIHARS has been described largely in children with neurologic symptoms or disease. A history of previous seizures was obtained in 12 of our 22 children, and many of the others had headache, school difficulties, or problems with concentration. This is similar to results in previous studies (2,7,15) and reflects very probably an ascertainment bias. Epileptic seizures are characterized by the co-occurrence of ictal EEG activity and behavioral change. The absence of spikes in episodes of HIHARS supports the view that the EEG abnormality is not epileptiform. However, rhythmic slow-wave activity without spikes has been described as an ictal EEG feature in nonconvulsive status (16). HIHARS with loss of clinical awareness is clearly associated with behavioral change, and many of the stereotyped features, including the automatisms, have been described in epileptic seizures. However, there have been no systematic studies of HV in normal children with video-EEG, and altered awareness during HV appears to be not uncommon in children (1). Despite careful clinical testing, altered awareness was detected in only 77 of the 233 episodes of HIHARS recorded in 22 patients in this study. It is likely that a much higher incidence of altered awareness would have been detected if the detailed testing described by Epstein et al. (2) had been performed. The occurrence of stereotyped behaviors, including automatisms, has been reported to relate to the length of the HIHARS discharge (3). We believe that the episodes described by Epstein et al. (2) represent one end of a
spectrum of severity of clinical change associated with HIHARS. The patients described in this study are those that could be detected by clinical testing. The degree of delta activity in HV in childhood is related to age, and the most pronounced responses occur in children aged 8 to 12 years (14). The age range of our patients with HIHARS (median, 9 years) was similar. This would be consistent with the concept that MORS with altered awareness represents one end of a spectrum of altered responsiveness in patients undergoing HV.
 
We believe that the incidence of HIHARS with altered awareness is affected by both awareness of the phenomenon and the rigor of the technical testing of awareness. Although it occurred in only 2.2 per thousand recordings overall during this study, the incidence increased with time or experience or both and had increased to 5.5 per thousand recordings in the last year of the study; the incidence in our laboratory over the past 12-month period is 7.4 per thousand recordings. In our study, HIHARS with altered awareness was observed only during HV. This is similar to nearly all other reports, and we are aware of only one description of altered awareness associated with the EEG features of HIHARS occurring outside HV (3). There is a temporal distinction between episodes of HIHARS with altered awareness and those of absence seizures. The duration of HV before to the onset of HIHARS with altered awareness was almost double that before the onset of an absence seizure in the control group, an observation made also by one other group (7). True absence seizures manifested early after the onset of HV, whereas HIHARS with alterations of awareness was never seen in the first 30 s of HV and appeared with a mean latency of >2 min. There also is a dissociation with the electrographic entity and the clinical alteration of awareness. Electrographically HIHARS appeared with a mean latency of 73 s; however, clinical manifestations did not appear until 139 s, suggesting that unlike three per second spike and wave, the clinical alterations in HIHARS are related to a cumulative physiologic change occurring during HV. Unlike that in one other study (7), recurrence of HIHARS with altered awareness in our study was uncommon, and only one of the 22 children demonstrated this change on a subsequent EEG. Thus whatever the nature of the event, the natural history includes resolution with or without treatment (7). It is our practice to inform the family that the episode is not epileptic, and we do not recommend antiepileptic treatment.
 
This study demonstrates that automatisms are observed commonly in children with HIHARS and altered awareness. The similarity in the clinical features and in the ages between those with HIHARS and those with absence seizures complicates the clinical diagnosis. Eye opening and eyelid flutter occur less often than in absence seizures, and yawning, smiling, and particularly fidgeting occur more frequently than in absence seizures.
  
 
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