Automatisms in Absence Seizures in Children with Idiopathic Generalized Epilepsy

ORIGINAL CONTRIBUTION Automatisms in Absence Seizures in Children With Idiopathic Generalized Epilepsy

Lynette G. Sadleir, MBChB, MD; Ingrid E. Scheffer, MBBS, PhD; Sherry Smith, RET, CNIM; Mary B. Connolly, MB, BCh, BAO; Kevin Farrell, MB, ChB

Background: Automatisms are well recognized to oc- influence of the following variables on the presence of au- cur in complex partial seizures; however, their occur- tomatisms was statistically analyzed: state of arousal (awake, rence in generalized epilepsies is not always appreci- drowsy, asleep), provocation (hyperventilation, photic ated. There has been considerable debate regarding the stimulation), age, and epilepsy syndrome. nature, triggers, and timing of automatisms in absence seizures. Results: Automatisms occurred in 163 of 405 seizures (40%) in 53 of 70 children (76%). Automatisms were more Objectives: To examine the frequency and nature of au- likely in longer seizures and hyperventilation. Only 23% tomatisms in new-onset absence seizures and assess the in- of spontaneous awake seizures had automatisms. Au- fluence of the state of arousal, provocation, age, and epi- tomatisms were similar for an individual child; how- lepsy syndrome on the presence and type of automatisms. ever, automatisms were not present in all their seizures. Age, epilepsy syndrome, or state of alertness had no effect Design: Analysis of absence seizures through video elec- troencephalogram (EEG) recordings. on the presence of automatisms.

Conclusions Setting: British Columbia’s Children’s Hospital, Van- : Automatisms are frequently seen during couver, British Columbia, Canada. childhood absence seizures. The high frequency of automatisms during EEG recordings is predominantly due Patients: Seventy consecutive children with new- to the effect of hyperventilation. Their preponderance dur- onset untreated absence seizures in idiopathic general- ing longer seizures may relate to opportunity for automa- ized epilepsy recruited between January 1, 1992, and June tisms to occur. The characteristic pattern of automa- 30, 1997. tisms suggests a reactive phenomenon to internal and external stimuli. Main Outcome Measures: Each seizure was analyzed for the presence and characteristics of automatisms. The Arch Neurol. 2009;66(6):729-734

UTOMATISMS ARE SEMICO- tient with cotton wool, which results in ordinated, repetitive mo- scratching during the seizure.2,3 It has been tor activities that are asso- suggested that scratching spontaneously Author Affiliations: ciated with impaired during an automatism may be a response Department of Paediatrics and awareness and occur in to an internal stimulus or an unseen stimu- Child Health, School of 1 3 Medicine and Health Sciences, bothA focal and generalized seizures. Re- lus. Thus, it was proposed that automa- 2-4 University of Otago, ports suggest that automatisms occur in tisms could be reactive to the internal and Wellington, New Zealand all children with absence seizures but not external environment and that they may (Dr Sadleir); Epilepsy Research in all seizures. Automatisms may be per- reflect the circumstance of the individual Centre and Departments of severative, when there is continuation of rather than an intrinsic property of the ab- Medicine and Paediatrics, an activity that commenced before the sei- sence seizure. This theory is consistent The University of Melbourne, Austin Health and Royal zure, or de novo, when automatisms start with reports that automatisms vary greatly Children’s Hospital, Melbourne, during the seizure. in complexity, location, and character from Australia (Dr Scheffer); and There has been debate regarding seizure to seizure within a single patient.2 Department of Pediatrics, whether automatisms are reactive or an in- A contrasting view is that automa- Division of Neurology, trinsic property of an absence seizure. The tisms are an intrinsic component of the sei- University of British Columbia observation that automatisms can be zure and are not random events.5,6 This and British Columbia’s Children’s Hospital, Vancouver, evoked suggests that automatisms can be draws on the observation that the clinical British Columbia, Canada influenced by external stimuli. De novo au- features of an absence seizure follow a ste- (Mss Smith and Connolly tomatisms can be induced by an external reotyped progression within an indi- and Mr Farrell). stimulus, for example, touching the pa- vidual, although not all clinical features are

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Features CAE CAE and PPR JAE JME Unclassified No. of children 37 10 8 6 9 Boys/girls, No. 15/22 3/7 1/7 3/3 6/3 Age at onset, mean (range), y 5.7 (2-10) 6.6 (4-0) 11.8 (11-6) 12.6 (11-5) 7.4 (1-3) Febrile seizures, % 18 20 0 0 0 Generalized tonic-clonic seizures, % 0 0 25 83 0 Myoclonic seizures, % 0 0 0 100 0 Primary or secondary family history, % 40 60 50 50 66 Seizures in hyperventilation, % 87 80 87 33 77 PPR, % 0 100 25 83 11

Abbreviations: CAE, childhood absence epilepsy; JAE, juvenile absence epilepsy; JME, juvenile myoclonic epilepsy; PPR, photoparoxysmal response.

present in every seizure.5,7,8 The earliest features tend to movements of the arms, hands, fingers, or legs. These automa- be irregular respiration and rhythmic myoclonic move- tisms were classified as simple if they were brief and the child was ments of the eyelids, followed by oral automatisms and only doing a single action, such as picking at his or her clothes. finally other motor automatisms. In addition, when clini- Complex limb automatisms were combinations of movements. cal features occur, they tend to do so at constant times Leg involvement could not be assessed in all seizures because only 5 the upper part of the body was videotaped in most seizures. Other during the seizure. automatisms, such as humming, were classified as other. No at- The objective of this study is to describe the clinical tempt was made to induce automatisms. features of automatisms during absence seizures in an un- Seizures with clinical signs were assessed for whether the selected group of children with new-onset idiopathic gen- clinical features were consistent with the temporal evolution eralized epilepsy before the initiation of antiepileptic described by Stefan and colleagues.5 The clinical features were therapy. We used a statistical model to examine the effect considered consistent with this theory if the order of events of various factors that could influence the presence of au- comprised (1) eye features (eye opening or abnormal move- tomatisms, such as age, epilepsy syndrome, state of alert- ment of the eye or eyeball), (2) oral automatisms, and then ness, and type of provocation. (3) limb automatisms. They were also considered consistent if there were only fragments of this temporal association: for example, if only oral automatisms were seen, then the seizure METHODS was included. If the order did not follow this progression, then the seizures were considered to be inconsistent with the The electroencephalography department of British Colum- temporal hypothesis. bia’s Children’s Hospital is a referral center for electroencepha- The epilepsy syndrome was classified according to the Inter- lographic (EEG) studies requested by family physicians, pe- national League Against Epilepsy 1989 proposal for the revised clas- diatricians, and pediatric neurologists. The departmental sification of epilepsies and epileptic syndromes.9 The children with database of 14 452 EEG recordings was searched for consecu- childhood absence epilepsy were further categorized based on the tive patients younger than 18 years who had at least 1 absence presence or absence of a photoparoxysmal response. seizure that was captured during a routine video EEG recording during a 51⁄2-year period between January 1, 1992, and June STATISTICAL ANALYSIS 30, 1997. The EEG studies were of sleep-deprived patients and included periods of hyperventilation and intermittent photic For each patient, data on multiple seizures were recorded. The stimulation (IPS). An absence seizure was defined as a clinical seizure was the basic unit of analysis. A statistical model ac- change associated with generalized spike and slow wave or mul- counting for multiple seizures per child and for variables that tiple spike and slow wave with a frequency of greater than 2.5 could potentially influence the presence of automatisms was Hz at the onset. The hospital records of patients with an ab- used. The variables considered were epilepsy syndrome, age, sence seizure were reviewed. Inclusion criteria for the study arousal (awake, drowsy, asleep), and provocation (hyperven- included normal intelligence, no previous or present use of an- tilation and IPS). tiepileptic drugs, and a normal interictal EEG background (ex- Because the occurrence of automatisms in different sei- cluding epileptiform discharges). Formal consent was ob- zures within the same patient was not likely to be indepen- tained for review of the video EEG recordings for research dent, a random-effects logistic regression model was used with purposes. a random patient effect. The log odds ratio of the patient ef- Two epileptologists (L.G.S. and K.F.), who were masked to fects was assumed normally distributed. The effects of vari- the epilepsy syndrome of the child, independently reviewed the ables are reported as odds ratio. The between-patient varia- video of each seizure at least 5 times. Only seizures with a clini- tion modeled by the random effect is reported as the median cal sign in which clear video information was available were odds ratio of the presence of automatisms between seizures from assessed for automatisms. 2 randomly chosen patients with identical age, syndrome, state, Automatisms were classified as oral, limb, or other. Oral and and provocation. limb automatisms were further classified as either simple or complex. Simple oral automatisms were simple movements of the RESULTS mouth or tongue that were repeated no more than twice during the seizure. Oral automatisms were complex if they were a combination of tongue and mouth movements or at least 3 simple The study population consisted of 70 children (35 girls) oral automatisms occurred in a seizure. Limb automatisms were (Table 1) in whom 405 absence seizures were ana-

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©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 Table 2. Clinical Features of Oral Automatisms Unclassified vs CAE CAE and PPR vs CAE Oral Automatism No. of Seizures JME vs CAE Swallowing 47 JAE vs CAE Mouthing 37 Chewing 34 Age Lip smacking 32 Lip licking 28 Duration per 10 s Grimacing 7 Yawning 6 Photic vs wake Sniffing 3 Hyperventilation vs wake Smiling 1 Sleep vs wake Sighing 1 Drowsy vs wake

Sneezing 1 0.01 0.10 1.00 10.00 Hiccuping 1 Odds Ratio of Automatisms Wriggling tongue 1 Shrugging nose 1 Biting lower lip 1 Figure 1. Odds ratio estimates for the occurrence of automatisms. Error bars indicate SD. CAE indicates childhood absence epilepsy; JAE, juvenile absence epilepsy; JME, juvenile myoclonic epilepsy; and PPR, photoparoxysmal response.

Table 3. Clinical Features of Manual Automatisms

70 All automatisms Manual Automatism No. of Seizures Oral automatisms Moving, wringing, fidgeting, playing with, 30 60 Manual automatisms scratching, or picking at hands or fingers Scratching, rubbing, picking at, or touching head 23 50 and neck or ears Scratching, rubbing, picking at, or touching any part 19 40 of face Scratching or moving legs 11 30 Seizures, % Moving or playing with arms or shoulders not 4 associated with any of the above 20 Readjusting or playing with blanket 3 Picking at clothes 2 10 Scratching body 1 0 Awake Drowsy Asleep Hyperventilation Photic (n = 47) (n = 99) (n = 21) (n = 194) (n = 44) lyzed. Automatisms were seen in 163 of the 405 sei- Figure 2. Percentage of seizures with automatisms in each state. zures (40%) in 53 of the 70 children (76%). Complex automatisms occurred in 61 seizures (15%) and 30 children (43%). Oral automatisms were observed in 130 ventilation were 6 times more likely to have automa- seizures (32%) and limb automatisms in 80 seizures tisms than those occurring spontaneously. Oral and (20%). Eighty-five of the 130 oral automatisms (65%) limb automatisms were more likely to be seen during and 56 of the 80 limb automatisms (70%) were simple. hyperventilation, with oral automatisms being more fre- The specific types of automatisms are listed in Table 2 quent (Figure 2). State of arousal or epilepsy syn- and Table 3. Humming was the only other type of drome had no effect on the presence of automatisms automatism observed and only occurred in 1 seizure in (Figures 1 and 2). 2 children. Automatisms were an inconsistent feature. Of the 70 Although the clinical features of automatisms varied children, 16 (23%) never had an automatism and 15 greatly from seizure to seizure for each child, there was (21%) had automatisms in every seizure (Figure 3). a tendency for a child to have either oral or manual au- The odds ratio for the occurrence of automatisms tomatisms. Automatisms in an individual tended to in- between 2 randomly selected seizures of the same dura- volve the same area of the body. For example, an indi- tion in the same state in 2 children of the same age and vidual might scratch his ear in the first seizure, pick the syndrome is 4.2. This value is of equivalent magnitude same ear in the second seizure, and scratch his head in to the effect observed for duration and hyperventilation, the third seizure. which implies that other factors, apart from the vari- Only duration of the seizure and provocation (hy- ables studied, influence the presence of automatisms. perventilation and IPS) had an effect on the presence of The average time to first automatism (either oral or automatisms (Figure 1). Increasing the duration of the manual) was 3.9 seconds (median, 3.0 seconds; SD, 3.6 seizure by 10 seconds doubled the likelihood of seconds; range,0.1-26.0 seconds) (Table 4). Oral automatisms occurring. Seizures recorded during IPS automatisms occurred significantly earlier than manual were 10 times less likely to have automatisms than ones (3.04 seconds; PϽ.001). The duration of the sei- spontaneous attacks, whereas seizures during hyper- zure also influenced the time of onset of the first

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8 No. of Seizures

0 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 Child

Figure 3. Distribution of the number of seizures with and without automatisms in each child.

Table 4. Types of Automatism and Their Time at Onset Table 5. Characteristics of Automatisms Not Conforming to the Theory of Stefan et al5 Type of No. of Mean (SD) Median (Range) Automatism Seizures Time at Onset, s Time at Onset, s No. of Temporal Relationship Seizures Oral simple 84 3.61 (3.25) 3.0 (0.1-14) Oral complex 46 2.82 (2.7) 2.0 (0.1-13) Oral automatisms simultaneous with the eye feature 17 Limb simple 56 6.43 (4.83) 5.0 (0.1-26) Oral automatisms before eye feature 14 Limb complex 24 8.42 (3.96) 7.5 (3.0-17) Manual automatisms before oral automatisms 2 Manual automatisms before eye feature 2 Oral automatisms before manual before eye feature 1 Head or body jerk before eye feature 5 automatism. With every increase of 1 second in dura- Other combination 23 tion of the clinical seizure, the time to the first automatism is 0.2 second later (PϽ.001) (eg, a clinical seizure that is 10 seconds longer will have the first automatism lighted the variability in automatisms, which are influ- 2 seconds later). enced by both environmental and intrinsic factors. For the 163 absence seizures in which automatisms Hence, we considered that automatisms were worthy of occurred, 64 (39%) did not follow the sequence sug- more detailed analysis. gested by Stefan et al.5 The way in which the progres- The incidence of automatisms in our study is lower sion of features differed from the hypothesis of Stefan et than the reported incidence of 88% to 100% of children al is detailed in Table 5. in other studies.2-4,6,11-13 This variation probably relates to differences in the study populations. Previous COMMENT studies2-4,6,11-13 include both children and adults with symptomatic generalized epilepsy and intractable We previously analyzed the clinical and electroen- absence seizures who were already receiving antiepilep- cephalographic features of absence seizures in a group tic drugs. In their study, Penry and colleagues3 of children with new onset idiopathic generalized epi- attempted to induce automatisms by stimulating their lepsy, but did not consider automatisms.10 We assessed patients during a seizure; we did not attempt to elicit the influence of state of arousal, provocation (hyperven- automatisms. In contrast, our study is of an unselected tilation and IPS), age, and epilepsy syndrome on seizure cohort of children with new-onset idiopathic general- duration, eye opening, eyelid movements, and level of ized epilepsy, who were referred for an EEG because of awareness. We found that the variation in the clinical staring spells, and who were not yet taking medication. features was determined by a complex interaction of The lower incidence of automatisms in our study may these variables and undetermined factors specific to the reflect these different populations and methods. On the child.10 Herein, we present a study of automatisms in other hand, our study is predicated on the patient hav- absence seizures. Previous studies2,3,5,6,11 have high- ing absence seizures during a routine EEG, which

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©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 means that patients with infrequent seizures may not our patients was consistent with the temporal theory have been included. of Stefan et al15 in 61% of seizures with automatisms. The clinical features of automatisms observed in our Although we observed an increased incidence of study were similar to those detailed in previous automatisms in longer seizures, there was no increase studies.2,3,6,11-13 For 56% of children, automatisms were in the likelihood of automatisms after 13 seconds of inconsistently present or varied in nature in their sei- seizure duration. Thus, it would appear that automa- zures; these findings confirmed the observations of tisms typically occur at a set time, and, unless artifi- other workers.2,3,11 cially induced by external stimuli, oral automatisms The nature of automatisms may be similar, but not occur 3 seconds before manual automatisms. identical, in the seizures of a child. For example, a child Our data synthesize the views of Penry et al and might have a variety of manual automatisms, such as Stefan et al, with evidence that there is an inherent pro- rubbing, picking, or scratching at her ear, in a succes- gression to a reactive phenomenon. Perhaps this stereo- sion of seizures. The automatisms, particularly those typical pattern of automatisms, with oral automatisms involving the upper limbs, were often directed toward beginning 2 to 3 seconds after seizure onset, followed 3 an object, such as an electrode, that may have been an seconds later by manual automatisms, reflects decreas- irritant. However, more often an environmental trigger ing inhibition of afferent inputs to the cortex as the sei- was not apparent. zure progresses. This theory would fit with the concept The impact of level of arousal, hyperventilation, and of reactive automatisms, which surmises some degree of photic stimulation on automatisms has not been awareness when the child is reacting to an internal or reported previously. Automatisms were 6 times more external stimulus. This theory is also supported by the likely to occur in seizures during hyperventilation than finding that awareness, as assessed by response testing, in spontaneous seizures in the awake state. Specifically, increases toward the end of the seizure.16,17 The pre- oral automatisms occurred in 28% of seizures in hyper- dominance of automatisms during provoked activities ventilation compared with 17% of spontaneous sei- rather than spontaneous seizures further supports their zures, and limb automatisms in 56% of seizures in reactive nature. hyperventilation compared with 9% of spontaneous seizures. The widely held view that automatisms, particu- Accepted for Publication: December 12, 2008. larly oral ones, are common in absence seizures2,3,6,13 Correspondence: Ingrid E. Scheffer, MBBS, PhD, Aus- may have arisen because most observed absence sei- tin Health, Level 1, Neurosciences Building, Banksia Street, zures occur when elicited by hyperventilation in the Heidelberg, Victoria 3081, Australia (scheffer@unimelb clinic and during an EEG recording. Several factors may .edu.au). contribute to the increased incidence of automatisms in Author Contributions: Study concept and design: Sadleir, hyperventilation. Although it is possible that the patho- Scheffer, Connolly, and Farrell. Acquisition of data: Sadleir, physiology of absence seizures in hyperventilation is Smith, Connolly, and Farrell. Analysis and interpreta- different, it is more likely that hyperventilation itself tion of data: Sadleir, Scheffer, Connolly, and Farrell. Draft- influences the clinical features. Hyperventilation is an ing of the manuscript: Sadleir, Scheffer, and Farrell. Criti- unnatural state in which people feel dizzy, “tingly,” and cal revision of the manuscript for important intellectual uncomfortable and often develop dry lips and mouth. content: Sadleir, Scheffer, Smith, Connolly, and Farrell. Thus, the automatisms may be reactive to these sensa- Statistical analysis: Sadleir. Obtained funding: Connolly tions and consequently may occur more frequently dur- and Farrell. Administrative, technical, and material sup- ing hyperventilation. port: Sadleir, Smith, and Farrell. Study supervision: Schef- Penry and Dreifuss11 suggested that automatisms are fer, Connolly, and Farrell. phenomena that are reactive to internal and external Financial Disclosure: None reported. stimuli rather than innate manifestations of absence sei- Additional Contributions: We acknowledge and thank zures. This theory is based on the finding that automa- Bendix Carstensen, MSc, Clinical Epidemiology & Bio- tisms can be induced and modified by external stimuli statistics Unit, Royal Children’s Hospital, Melbourne, Vic- and are not constantly present. It is supported by the toria, Australia, presently at Steno Diabetes Centre, Gen- increased incidence of automatisms during hyperventi- tofte, Denmark, for performing the statistical analysis in lation and the similar nature of automatisms if there is a this study. We also acknowledge the additional statisti- clear-cut irritant, such as an electrode. The increased cal assistance received from John Carlin, PhD, Clinical incidence of automatisms in longer seizures may reflect Epidemiology & Biostatistics Unit, Royal Children’s Hos- more opportunity for a reactive response. Automatisms pital, Melbourne, Victoria, Australia. were found to have no association with the inherent factors of age and epilepsy syndrome, a finding which is REFERENCES consistent with that of a previous report.2,14 An alternative view suggested that automatisms 1. Blume WT, Lüders HO, Mizrahi E, Tassinari C, van Emde Boas W, Engel J Jr. were innate rather than reactive phenomena. 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