Epilepsia, 46(8):1235–1240, 2005 Blackwell Publishing, Inc. C 2005 International League Against Epilepsy
Hyperorality in Epileptic Seizures: Periictal Incomplete Kl¨uver–Bucy Syndrome ∗ †Jozsef Janszky, †‡Andras Fogarasi, †Vafa Magalova, †Ingrid Tuxhorn, and †Alois Ebner ∗ Department of Neurology, University of P´ecs, P´ecs, Hungary; †Epilepsy Center Bethel, Bielefeld, Germany; and ‡Epilepsy Center, Bethesda Children’s Hospital, Budapest, Hungary
Summary: Purpose: To analyze systematically hyperorality associated with epileptic seizures and its relation to the localization of epileptic activity. Methods: To identify patients with periictal hyperorality, we reviewed video-recordings of 269 patients (aged 6–59 years) who had consecutively undergone presurgical evaluations including ictal video-EEG recordings and high-resolution magnetic resonance imaging (MRI) and had had epilepsy surgery because of intractable frontal (FLE) or temporal lobe epilepsy (TLE). Periictal hyperorality was defined if patients put or unambiguously intended to put nonfood items into their mouths during or after at least one of the reviewed seizures. For the further analysis, we included only patients with periictal hyperorality. We reviewed their medical records and reexamined their ictal video-EEG recordings. Results: We identified eight patients (six women) aged 8–59 years who had hyperorality during or after seizures. Seven patients had TLE, and one patient had frontal lobe epilepsy (FLE).
Three of these patients underwent right-sided surgery, whereas five patients had surgery on the left. Three patients exhibited ictal and five showed postictal hyperorality. Interictal EEG suggested bilateral interictal epileptiform discharges (IEDs) in three patients; in two other patients, no IEDs were detected. Ictal EEG suggested bilateral involvement in six cases. Patients with unilateral epileptiform activity had left TLE. Conclusions: Periictal hyperorality is a rare phenomenon occurring in 3% of the investigated epilepsy population. We suggest that periictal hyperorality is an ictal–postictal mental disturbance, an incomplete Kl¨uver–Bucy syndrome. In most patients, bilateral seizure activity plays an important role in the pathomechanism, but it would appear that left-sided epileptic activity without contralateral involvement also can cause periictal hyperorality. Key Words: Kl¨uver–Bucy syndrome—Amygdala— Postictal behavior—Presurgical evaluation of epilepsy—Ictal video-EEG recordings.
The Kl¨uver–Bucy syndrome (KBS) was first described in rhesus monkeys after bilateral temporal lobectomy (1) and is characterized by hypersexuality, excessive oral tendencies, dietary changes, loss of normal fear, lack of aggression, psychic blindness, and excessive attentiveness to visual stimuli. This syndrome also can occur in humans after bilateral temporal lobectomy (2), but it also can appear after herpes encephalitis, brain trauma, or in Pick or Alzheimer’s diseases (3). Although typical KBS seems to occur very rarely, some key features of KBS (incomplete KBS) can occur in many neurologic disorders. For example, hyperorality occurs in >80% of patients with frontotemporal dementia (4) and is characteristic of dementia associated with hippocampal sclerosis (5). Postictal hypersexuality in temporal lobe epilepsy (TLE) (6–8), or hypersexual behavior after TLE surgery (8,9) also are thought to be kinds of incomplete
KBS. There are three case reports of transient KBS after left-sided status epilepticus (10–12), and another case was reported in which recurrent postictal KBS occurred after a left temporal lobectomy (13). Recently two studies investigated periictal genital automatisms, a symptom of TLE seizures thought to be a part of the KBS spectrum (14,15). In the present study, our aim was to investigate systematically another characteristic of KBS: the hyperorality during or after epileptic seizures such as postictal or ictal behavior consisting of putting nonfood items into the mouth. Hyperorality is the most consistent phenomenon of human KBS (3). An analysis of hyperorality, as well as its relation to the seizure-onset region and spreading epileptic activity, may highlight its neurophysiologic mechanisms, its relation to specific localization or lateralization in the human brain. Furthermore, an understanding of the pathophysiology of hyperorality may have practical importance in everyday life because of the mortal danger of aspirating foreign items in general or in relation to epileptic seizures (12).
Accepted March 27, 2005. Address correspondence and reprint requests to Dr. J. Janszky at Ret u. 2. Department of Neurology, University of Pecs 7623, Pecs, Hungary. E-mail:
[email protected]
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To identify patients with periictal hyperorality in this retrospective study, we reviewed video-recordings of 269 patients (141 men, aged 6–59 years; mean age, 28.8 ± 13.1; mean age at epilepsy onset, 10.3 ± 8.6 years) who had consecutively undergone presurgical evaluations with ictal video-EEG recordings, had had epilepsy surgery because of intractable frontal lobe epilepsy (33 patients, aged 6–42 years) or because of pharmacoresistant TLE (236 patients, aged 6–59 years). Only patients older than 6 years were included because the seizure semiology of temporal and frontal lobe seizures in small children differs from that in adult seizures (16,17), and even healthy infants have oral activity independent of seizures (for example, thumb sucking or taking toys in their mouth). Epilepsy surgery was performed on the left in 136 and on the right side in 133 patients. The video recordings were reviewed by one of the authors (J.J., A.F., or V.M.). Periictal hyperorality was defined if patients put or unambiguously intended to put nonfood items into their mouths during or after at least one of the reviewed seizures. For the further analysis, we included only those patients who had periictal hyperorality. We reviewed their medical records and reexamined all of their video- and ictal EEG recordings again. Clinical examinations All patients underwent general medical, neurologic, psychiatric, and neuropsychological examinations at admission to our inpatient presurgical evaluation department. The clinical history and examinations were taken by physicians and psychologists blinded to the goals of this study. Long-term noninvasive video-EEG monitoring All patients underwent continuous long-term videoEEG monitoring lasting 2–7 days as part of their presurgical evaluation. EEG recordings with 32–64 channels were used; electrodes were placed according to the 10-10 system. Interictal EEG samples were automatically recorded and stored by computer. The location and frequency of interictal epileptiform discharges (IEDs) were assessed by visual analysis of interictal EEG samples of 2-min duration every hour. No automated spike-detection software was used. Ictal EEG data were recorded in files separate from the interictal files and were reevaluated again for this study. We used the criteria for lateralized, localized seizure onset and contralateral seizure propagation defined by Steinhoff et al. (18). Ictal and postictal periods were defined according to the periictal EEG recording and clinical seizure semiology. In two cases, however, the end of ictal EEG pattern could not be evaluated appropriately because of muscle artifacts of motor phenomena. In these cases, the seizure end was poorly defined according to the
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video recording. All recorded videos were reviewed once again for this study. Other investigations performed during presurgical evaluation All patients had high-resolution preoperative MRI taken by a 1.0- or 1.5-T scanner and included T1 -weighted threedimensional volume, proton density, fluid-attenuated inversion recovery (FLAIR), and T2 -weighted images. In some patients, a Wada test or functional MRI was performed if it was necessary for presurgical evaluation of memory and language functions. Our Wada test, speechand memory-activated functional MRI procedures have been described in our previously published studies (19– 21). RESULTS We could identify eight patients (six women, two men, 3% of the total investigated epilepsy population) aged 8–59 years who had hyperorality during or after their seizures. The clinical details are described in Table 1. Seven patients had TLE, and one patient had frontal lobe epilepsy (FLE). Three of these patients underwent rightsided surgery, whereas five patients had surgery on the left. A partial frontal lobectomy was performed on the FLE patient, whereas all seven TLE patients underwent an anterior temporal lobectomy. Histologic examinations were in agreement with the MRI results in all patients and revealed hippocampal sclerosis in seven cases, whereas focal cortical dysplasia without balloon cells was identified in one patient. The postoperative follow-up period ranged from 1 to 6 years. Five patients became seizure free after the surgery, but the other three patients continued to have seizures. Electroclinical correlation of periictal hyperorality Table 2 shows the results of presurgical evaluation including the reexamined ictal video and EEG recordings. According to our electroclinical evaluation, three patients exhibited ictal hyperorality (cases 6–8). It had never occurred at the seizure onset but 5–51 s after the start of clinical seizures during the seizure evolution. The EEG during ictal hyperorality could be properly evaluated in only one patient, who showed bilateral seizure pattern over the temporal regions, whereas in the other two patients, the ictal EEG was covered by muscle artifacts. The ictal hyperorality consisted of self-biting in one case, one patient exhibited biting of a blanket, and a third patient bit both himself and, occasionally, his blanket. In the periictal electroclinical correlations, five patients had postictal hyperorality (cases 1–5). Three of them had hyperorality immediately after the EEG seizure end, whereas the two other patients exhibited hyperorality 29 and 103 s after the seizure end, respectively. Four patients had postictal bilateral slow waves during the hyperoral behavior; one patient exhibited unilateral left-sided
M
W
W
W
W
W
M
W
1.
2.
3.
4.
5.
6.
7.
8.
5
3
12
3
9 mo
3
14
27
Age at onset (yr)
29
10
40
8
41
32
35
59
Age (yr)
—
—
—
Complex febrile seizure with R hemiconvulsion at age 9 mo
—
—
Meningitis at age 1.5 yr
—
Etiology
L HS
Focal cortical dysplasia in the anterior part of the R gyrus frontalis medialis
L HS
L HS
L HS
R HS
R HS
L HS
Structural MRI
Wada test: L speech, R memory dominance Wada test: L speech dominance, the memory performance was bilateral. PET: R frontopolar hypometabolism, ictal SPECT: R frontoorbitodorsal hypermetabolism Wada test: R speech and memory dominance. PET: bilateral mesiotemporal hypometabolism, L temporolateral hypometabolism
Wada test: L speech dominance, R memory dominance. f MRI: L speech f MRI: L speech and memory dominance
PET: R mesiotemporal hypometabolism
Wada test, f MRI: R speech and memory dominance PET: R temporal hypometabolism
Functional neuroimaging and Wada tests
Ambidextrous without neurologic signs, verbal memory deficit, IQ 93
R hemiparesis, severe verbal memory deficit, IQ 69 No neurologic signs, high intelligence (IQ 120), no memory deficit
No neurologic signs, high intelligence with memory deficits in nonverbal and verbal modalities
No neurologic signs, nonverbal memory deficit, low intellingence (IQ 66) No neurologic signs, IQ 86
No neurologic signs, verbal memory deficit, IQ 89 No neurologic signs, nonverbal memory deficit, IQ 94
Clinical and neuropsychological examination
Psychic (fear) aura, 3–10 CPSs/mo
Abdominal aura, 1–2 clusters of CPSs/mo, one episode of postictal psychosis with religious delusions at age 7 yr No aura, 1 CPS/day, occasionally GTCS Abdominal aura, 3–10 hypermotor-type CPSs/day
Abdominal aura, 1–2 CPSs/mo
Abdominal aura, 4 CPSs/mo, rarely GTCS Abdominal aura, 1 CPS/mo, occasionally GTCS, recurrent postictal psychoses with religious delusions and visual hallucinations Head aura, 3–5 CPSs/mo
Seizure history
W, woman; M, man; L, left, left-sided; R, right, right-sided; HS, hippocampal sclerosis; f MRI, functional MRI; CPS, complex partial seizure; PET, positron emission tomography; SPECT, single-photon emission tomography; GTCS, secondarily generalized tonic–clonic seizure.
Sex
Case
TABLE 1. Clinical history, neuroimaging, and neuropsychological data
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Genital automatisms
HO occurred in 1 of 2 recorded seizures starting with — bipedal and oral automatisms followed by automatism in the R hand; 29 s after the seizure, she put a magazine in her mouth and then bit a pen. After that, she licked the surface of the magazine 10–12 times — HO occurred in 1 of 3 recorded seizures consisting of loss of consciousness and oral automatisms. Immediately after the seizure ended, she took off her ring and tried to put it into her mouth, but was prevented from doing so by the EEG technician HO occurred in 1 of 6 recorded seizures. CPSs consisted of — oral and bimanual automatisms. Postictally she immediately started to eat a plant, and after another 10 s, she bit into an unpeeled orange HO occurred in 1 of 5 recorded seizures. The seizure started — with tonic posturing of the R upper extremity accompanied by hypermotor bipedal–bimanual automatisms; 18 s after the onset, she bit her arm HO occurred in 21 of 21 recorded seizures. Five seconds He fondled, grabbed his after intensive hypermotor-like bipedal–bimanual genitals postictally automatisms, he usually bit his R arm, occasionally R leg, L arm, or the blanket. No loss of consciousness occurred during these seizures HO occurred in 1 of 2 recorded seizures. During CPSs, she — had bipedal–bimanual automatisms and repetitive vocalization, 51 s after the onset, she bit the blanket, and after another 5 s, she bit the blanket again and held it in her mouth for 6 s
HO occurred in 1 of 5 recorded seizures. During a CPS, the In 2 of 5 seizures, he fondled patient showed oral and bipedal automatisms. Postictally genitals for a minute he started to fold the blanket, 103 s after the seizure’s end, he bit into the blanket, and after another 13 s, he bit off a small part of it, resulting in a 5-cm2 hole. After another seizure with similar semiology, he bit into an apple HO occurred in 1 of 2 recorded seizures. CPSs consisted of — oral and bipedal automatisms. Immediately after the seizure’s end, she licked the string of her trousers 2 times
Description of the seizures associated with periictal hyperorality L anterotemporal IEDs, L temporal seizure pattern during CPS
Interictal, ictal EEG
No IEDs, L seizure pattern during CPS followed by R seizure pattern
Automatisms with preserved responsiveness, ictal speech, L postictal nose wiping
Bilateral independent anteriotemporal IEDs, L temporal seizure pattern, followed by R temporal and bitemporal ictal involvement
L and occasionally R postictal R anteriofrontal IEDs, R nose wiping frontal seizure pattern followed by independent L frontal seizure pattern
Ictal aphasia in one seizure
Ictal speech, automatism with R temporal IEDs, R temporal preserved responsiveness, seizure pattern during CPS L nose wiping followed by independent L temporal seizure pattern Ictal speech, dystonia in the L R (in 86%) and L (in 14%) hand temporal IEDs, R temporal seizure pattern during CPS followed by L temporal seizure pattern L hand dystonia, L postictal R (in 81%) and L temporal nose wiping IEDs, L seizure pattern during CPS followed by independent R seizure pattern Postictal aphasia, L postictal L anteriotemporal seizure nose wiping pattern during CPS, no IEDs
R hand dystonia, L postictal nose wiping
Ictal, postictal lateralizing signs
Bitemporal seizure pattern
Cannot be evaluated due to artifacts Cannot be evaluated due to artifacts
L ATL, non–seizure free 2 yr after surgery
R frontal lesionectomy, seizure free 6 yr after surgery
L ATL, non–seizure free 2 yr after surgery
L ATL, seizure free 1 yr after the surgery
L ATL, seizure free 2 yr after surgery
Postictal bilateral delta waves Postictal L delta waves
R ATL, seizure free 2 yr after surgery
R ATL, non–seizure free 4 yr after surgery
L ATL, non–seizure free 2 yr postoperatively
Surgery, surgical outcome
Postictal bilateral slow waves
Postictal bilateral slow waves
Postictal bitemporal slow waves with artifacts
EEG during hyperorality
HO, hyperorality; L, left, left-sided; R, right, right-sided; CPS, complex partial seizure; IEDs, interictal epileptiform discharges; ATL, anterior temporal lobectomy; GTCS, secondarily generalized tonic–clonic seizure.
8.
7.
6.
5.
4.
3.
2.
1.
Case
TABLE 2. Data on presurgical video-EEG monitoring
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HYPERORALITY IN EPILEPTIC SEIZURES postictal exhaustion during the hyperorality. During postictal hyperorality, one patient ate a plant and, in another instance, an unpeeled orange; another patient bit theblanket; a third patient almost put her ring in her mouth; another patient repetitively licked the string of her trousers; and a fifth patient bit a pen and repetitively licked the surface of a magazine. The postictal hyperoral behavior was preceded by purposeful actions preparing to put the nonfood items into the mouth. For example, patient 1 folded the blanket for >10 s before putting it into his mouth and biting into it. Patient 4 struggled for 8 s trying to pull off her ring to put it into her mouth. In four of five patients, the postictal hyperorality showed a repetitive nature. Interictal EEG suggested bilateral IEDs in three patients; in two other patients, no IEDs were detected. Ictal EEG suggested bilateral involvement in six cases. Both of the patients without bilateral epileptiform activity had left TLE. The relation of periictal hyperorality with clinical seizure semiology Genital automatisms occurred in two patients, but only in one patient did they appear in the same seizure with hyperorality. Postictal nose wiping was the most frequent periictal lateralizing sign, occurring in six patients, but it showed false lateralization (contralateral to the seizure onset) in two patients. Ictal hand dystonia occurred in two patients contralateral to the epileptogenic regions and in one patient ipsilateral, indicating false lateralization. Bipedal automatism was unusually frequent in this predominantly mesial TLE population and was present in six patients (in one FLE and in five TLE patients). DISCUSSION Analyzing ictal videos of 269 presurgical epilepsy patients, we could identify eight patients in whom hyperorality (postictal in five and ictal in three cases) was present (i.e., this phenomenon occurred in 3% of patients). In comparison, the other systematically well-investigated periictal phenomenon within the KBS spectrum, the periictal genital automatism, occurs with a frequency of 5.5–11% (14,15). Genital automatisms occurred in two of our eight patients. Thus we can assume that its high occurrence among our patients indicates that both phenomena may be caused by similar mechanisms. Conversely, genital automatisms appeared in the same seizure with hyperorality only in one patient, who had ictal hyperorality (mostly self-biting) and postictal genital automatism in all of the 21 recorded seizures. Sexual automatisms (rhythmic hypermotoric pelvic and truncal movements) characteristic of FLE (22) did not occur in our patients. The preparatory actions performed by the patients with the purpose of putting the nonfood items into their mouths and the repetitive nature of hyperorality suggest that periictal hyperorality is an ictal–postictal mental disturbance,
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a part of the KBS spectrum and probably caused by a transient localized functional brain abnormality due to the epileptic activity. The nature of hyperorality seems to be different, as both cases of ictal self-biting were a part of hypermotor-type complex partial seizures (23,24), whereas patients with postictal hyperorality had no hypermotor seizures. Conversely, many common features seem to be associated with both postictal and ictal hyperorality: presence of postictal nose wiping, frequent bipedal–bimanual automatisms, and bilateral ictal or interictal epileptic activity. Furthermore, the border between ictal and postictal states could not be clearly defined, as we did not use intracranial electrodes, and in some cases, the ictal EEG seizure end could not be properly defined because of muscle artifacts. Because three of five patients had hyperorality immediately after the seizure end, it is hard to decide whether they have postictal or late-ictal hyperorality. KBS was first described in animals that underwent bitemporal lobectomies, and it occurs mostly in patients with various bitemporal disorders (1–3). Periictal genital automatism, supposedly a postictal KBS symptom, occurs mostly in patients with bitemporal seizure activity (15). In our patients, ictal seizure activity was bilateral in six of eight cases. The false lateralization of postictal nose wiping in two patients and ictal dystonia in another patient also suggest spread of interictal activity to the contralateral hemisphere (25,26). Moreover, in one of the two patients who had no signs of interictal or ictal bilateral epileptic activity on the EEG, bilateral postictal slow waves were present during the hyperorality as a sign of bilateral postictal exhaustion. Thus we can assume that in most patients, bilateral seizure activity plays an important role in the pathomechanism of periictal hyperorality. The two patients who showed no signs of interictal or ictal bilateral epileptic activity had left-sided TLE. Two case reports exist of KBS that developed after a unilateral, left anterior lobectomy (13,27), and three case reports exist of transient KBS after left-sided status epilepticus (10– 12). Therefore we may suppose that left-sided epileptic activity without contralateral involvement also can cause periictal hyperorality. Postictal nose wiping occurred in 75% of our patients. Even the patient with FLE exhibited postictal nose wiping. Postictal nose wiping appears in 46–51% of TLE patients, whereas this sign is rare in extratemporal epilepsy, occurring in only 10–12% (28,29). This phenomenon may be a result of the ictal upper-airway secretion generated by the seizure activation at the amygdala (26,29,30) Although the exact mechanism of KBS is unknown, it may be that the amygdalar damage is crucial in developing some symptoms (31). Six of our eight patients had bipedal automatisms, which are considered to be a sign of ictal involvement of the frontoorbital region (32), suggesting that not Epilepsia, Vol. 46, No. 8, 2005
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only the mesiotemporal regions but the involvement of frontoorbital areas also may play a role in the pathomechanism of periictal hyperorality. Acknowledgment: This work was supported by the Humboldt Foundation and a grant from the Deutsche Forschungsgemeinschaft (DFG-Eb 111/2-2). We gratefully thank Terri Shore Ebner, who carefully reviewed the manuscript as a native English speaker. We thank Dr. H. Holthausen for the clinical care of one of the pediatric patients.
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