Genital automatisms: Reappraisal of a remarkable but ignored symptom of focal seizures

Epilepsy & Behavior 80 (2018) 84–89

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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh

Genital automatisms: Reappraisal of a remarkable but ignored symptom of focal seizures Hava Özlem Dede, Nerses Bebek ⁎, Candan Gürses, Leyla Baysal-Kıraç, Betül Baykan, Ayşen Gökyiğit Istanbul University, Istanbul Faculty of Medicine, Clinic Neurophysiology Department, Turkey

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Article history: Received 29 August 2017 Revised 22 December 2017 Accepted 22 December 2017 Available online xxxx Keywords: Genital automatisms Hand automatisms Drug-resistant epilepsy Semiology

a b s t r a c t Objectives: Genital automatisms (GAs) are uncommon clinical phenomena of focal seizures. They are defined as repeated fondling, grabbing, or scratching of the genitals. The aim of this study was to determine the lateralizing and localizing value and associated clinical characteristics of GAs. Methods: Three hundred thirteen consecutive patients with drug-resistant seizures who were referred to our tertiary center for presurgical evaluation between 2009 and 2016 were investigated. The incidence of specific kinds of behavior, clinical semiology, associated symptoms/signs with corresponding ictal electroencephalography (EEG) findings, and their potential role in seizure localization and lateralization were evaluated. Results: Fifteen (4.8%) of 313 patients had GAs. Genital automatisms were identified in 19 (16.4%) of a total 116 seizures. Genital automatisms were observed to occur more often in men than in women (M/F: 10/5). Nine of fifteen patients (60%) had temporal lobe epilepsy (right/left: 4/5) and three (20%) had frontal lobe epilepsy (right/left: 1/2), whereas the remaining two patients could not be classified. One patient was diagnosed as having Rasmussen encephalitis. Genital automatisms were ipsilateral to epileptic focus in 12 patients and contralateral in only one patient according to ictal–interictal EEG and neuroimaging findings. Epileptic focus could not be lateralized in the last 2 patients. Genital automatisms were associated with unilateral hand automatisms such as postictal nose wiping or manual automatisms in 13 (86.7%) of 15 and contralateral dystonia was seen in 6 patients. All patients had amnesia of the performance of GAs. Conclusion: Genital automatisms are more frequent in seizures originating from the temporal lobe, and they can also be seen in frontal lobe seizures. Genital automatisms seem to have a high lateralizing value to the ipsilateral hemisphere and are mostly concordant with other unilateral hand automatisms. Men exhibit GAs more often than women. © 2017 Elsevier Inc. All rights reserved.

1. Introduction Ictal clinical lateralizing signs are particularly beneficial in presurgical investigation of refractory epilepsy. Some of these frequent or rare semiologic phenomena have well-known high lateralizing and localizing value reaching 90–100%, whereas some others seemed less reliable [1–4]. An exhaustive body of literature has evaluated many of these semiologic features, whereas GAs remain largely underinvestigated. Their frequency has been reported as 3–11.4%, which suggests that this phenomenon is not rare but underestimated. Genital automatisms occurred relatively frequently in temporal lobe seizures (16%) and relatively rarely (4%) in frontal lobe epilepsy (FLE) [5]. The lateralizing value of GA is controversial.

Genital automatisms defined as repeated fondling, grabbing, or scratching of the genitals are detected in focal seizures [5]. They must be differentiated from other sexual and orgasmic auras, genital sensory phenomena, and hypermotor sexual automatisms. The localizing value for these phenomena is debatable. It was reported that subtle genital automatisms such as fondling and genital grabbing were more typical of temporal lobe seizures, whereas hypermotor seizures such as pelvic or truncal movements were prevalent in FLE [6]. We aimed to evaluate the lateralization and localization value of GAs and associated clinical characteristics to draw attention to these underestimated epileptic phenomenon as a valuable semiologic characteristic. 2. Material and methods

Abbreviations: EEG, electroencephalography; FLE, frontal lobe epilepsy; GAs, genital automatisms; LOC, loss of consciousness; MRI, magnetic resonance imaging; PET, positron-emission tomography; SUDEP, sudden unexpected death in epilepsy; TLE, temporal lobe epilepsy; VEM, video-EEG monitoring. ⁎ Corresponding author at: Istanbul University, Istanbul Faculty of Medicine, Department of Neurology and Clinical Neurophysiology, Millet Avenue, Fatih/Istanbul, Turkey. E-mail address: [email protected] (N. Bebek).

https://doi.org/10.1016/j.yebeh.2017.12.023 1525-5050/© 2017 Elsevier Inc. All rights reserved.

2.1. Patient selection We retrospectively studied 313 consecutive patients with medically refractory seizures who were admitted to the epilepsy monitoring unit at the Epilepsy Center, Istanbul Faculty of Medicine, Istanbul University,

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between 2009 and 2016, for the presence of GAs. All patients underwent long-term video-EEG monitoring (VEM) for more than 24 h with scalp electrodes, in addition to their detailed presurgical evaluation. Clinical and electrophysiologic seizures showing GAs were included and evaluated with a standard protocol [7]. 2.2. Data collection tools The video-electroencephalography (EEG) recording technique, performed using scalp electrodes (International 10–20 System), was in accordance with international guidelines developed by the American Electroencephalographic Society for video-EEG monitoring in patients with epilepsy [8]. Scalp EEG analysis was performed using bipolar longitudinal-transverse and referential montages by experienced clinical neurophysiologists. The EEG recordings of all patients were examined to evaluate the subsistence of background abnormalities, both nonepileptiform and epileptiform interictal activity, ictal discharges, and postictal slowing. Additionally, we evaluated interictal scalp EEG, ictal semiology, and neuro-imaging findings. Highresolution 3 T MRI was performed according to a standard protocol, and interictal PET and formal neuropsychological evaluations were performed. We evaluated invasive ictal EEG in one patient (N7). Epileptic focus definition was based on accordant findings in these investigations. Our main indicator was the scalp EEG ictal signs to determine the seizure onset zone. The other signs were accepted as supplementary methods. If we could not lateralize the seizure onset zone with the main or supplementary methods, we described this as “nonlateralized”. One patient (N7) who had two seizures with GAs showed switch of lateralization phenomenon. If the scalp EEG ictal signs lateralization switched to the contralateral hemisphere, we accepted this phenomena as “switch of lateralization”. Bilateral asynchrony was more than 1 Hz frequency difference between the two sides and the duration must be at least 10 s [9]. 2.3. Genital automatisms We defined GAs as stereotyped, repetitive manipulation of genitals for grabbing, scratching, or rubbing, for longer than 3 s [5]. We categorized GAs according to the time of occurrence: “early” period: first 10 s from the beginning of seizure; “late” period, the last 10 s; “intermediate” period, between these; and “postictal” period, after the end of seizure activity on EEG. All video-EEG records were reviewed by two examiners (NB, HOD) who were blinded to the history and seizure outcome in order to detect seizures with GAs, and to evaluate their electroclinical semiology. Consensus was established for all patients. Genital sensations such as numbness, tingling, pain, and unpleasant feeling in the genitals are classified as somatosensory auras. Sexual auras are usually experienced as erotic pleasant feelings or thoughts [10]. None of our patients reported any of these sensations. We used the Engel classification system for postoperative outcomes in patients who had epilepsy surgery [11,12]. Class I: free of disabling seizures, Class II: rare disabling seizures (“almost seizure-free”), Class III: worthwhile improvement, and Class IV: no worthwhile improvement. All patients were informed, and written consent was obtained. The local ethics committee approved the study (2015-1029).

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Three patients had GAs in multiple seizures. The 10th patient had 3, and the 7th and 9th patients had 2 seizures with GAs; the remainder had only one (Table 1). All GAs were subtle hand automatisms, none involving pelvic thrusting or hypermotor behavior. Of the 16 ictal GAs, 6 were seen in the early period, 7 in the late, and 3 in the intermediate periods. Genital automatisms were seen postictally in three seizures. Nine patients had hippocampal sclerosis, 3 patients had frontal encephalomalacia, and 1 patient had Rasmussen encephalitis. Two patients had no lesions. During VEM, all patients who performed GAs had focal seizures with LOC and were amnestic of the GAs. The patient with Rasmussen encephalitis had a secondarily generalized focal seizure. No patients reported a history of a genital somatosensorial aura. None of the patients experienced any apparent autonomic symptoms such as orgasm during the seizures associated with GAs, and in male patients, no penile erection or ejaculation was observed. According to EEG findings, ictal seizure onset was localized in the anterior temporal region in 8 patients. Genital automatisms were on the same side as the ictal onset in seven patients (87.5%). Only in one patient (N2) the ictal activity started in the right temporal region, and GA occurred on the contralateral (left) side. Ictal onset was in the left frontal lobe in one patient (N11) and in bilateral anterior regions in another patient (N1); it could not be localized in 5 patients with ictal scalp EEG. In four of these patients whose ictal EEGs were uninformative, ictal semiology, interictal EEG, and cranial MRI findings were concordant with the lateralization of GAs to the ipsilateral hemisphere (Fig. 1A-B). Two patients could not be lateralized using scalp EEG or other auxiliary methods (Fig. 2). One patient (N7) who had two seizures with GAs showed switch of lateralization phenomenon ictal activity began in the left temporal region and spread to the right temporal region. Genital automatisms started in the left hand, then continued in the right hand with simultaneous ictal seizure activity (Fig. 3A-B). This patient was additionally evaluated with invasive EEG (bilateral deep hippocampal electrodes), because of bilateral ictal, interictal electrophysiological and radiological findings. Two seizures were recorded during invasive EEG, which showed seizure onset in the left anterior temporal region, ipsilateral to GAs (Fig. 4). Genital automatisms were seen together with unilateral hand automatisms such as postictal nose wiping or manual automatisms in 13 (86.7%) of 15 patients accompanied by unilateral dystonia in 6 (42.8%) patients. Unilateral manual automatisms were ipsilateral and concordant with GAs in 11 (84.6%) patients, unilateral dystonias were 100% contralateral with GAs. Four patients underwent to epilepsy surgery. Two had good outcomes (Engel's class 1) with a follow-up of ≥ 2 year. Two patients had surgery within the past 6 months (N7, N12) with no postoperative complications. Four patients declined surgery. One patient was evaluated recently and is awaiting surgery. One patient with right hippocampal sclerosis (N5) who was a candidate for surgery died before surgery in 2012 of probable SUDEP. This patient experienced 5–6 seizures per month despite multiple antiepileptic drugs. He had no cardiac disease or history of any other illness. 4. Discussion

3. Results We observed GAs in 15 (4.8%) of 313 patients. The mean age of patients was 32.3 ± 9.4 years (range, 15–50 years). The majority (10 men and 5 women; 66.7%) of patients who exhibited GAs were men. The mean seizure onset age was 13.2 ± 10.5 years (range, 1– 38 years). The mean seizure frequency for the last three months was 4.9 ± 4.19 (range, 1–15). One hundred sixteen seizures in total were recorded from these patients. We detected GAs in 19 of 116 seizures.

Genital and sexual seizure manifestations represent underinvestigated and rare clinical phenomena during or after seizures and can be subdivided into (1) sexual auras, (2) genital auras, (3) sexual automatisms, and (4) GAs [13]. The frequency of GAs was reported as 3– 11.4% [5]. Genital automatisms were detected in 4.8% of our patients. A possible role of the temporal lobe in sexual behavior was originally reported by Klüver and Bucy [14] who demonstrated that bilateral temporal lobectomy in monkeys produced hypersexuality. Previous studies that investigated the lateralization and localization value of

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Table 1 Demographic, clinic, and electrophysiological features of patients. Age of Etiology onset of epilepsy

Cranial MRI

Cranial PET

Ictal EEG

Interictal EEG

Side of GA

Timing

1/M/50

38

Unknown cause

Nl

NP

Bilat FT

Left FT

Right

2/M/15

2

Right MTLE-HS

Right HS

Right T

Right T

Right T

Left

3/M/32

11

Right HS

1

Left HS

Bi-temporal Right T Bi FT right N left Left T Nonlat. Left FT

Right

4/M/36

Structural-metabolic causes Left MTLE-HS

5/M/43

33

Right MTLE-HS

Right HS

NP

Right FT

6/F/38

13

Left MTLE-HS

Left HS

Left T

7/M/32

2

Left MTLE-HS

Left HS

8/M/25

12

Rasmussen

Right hemiatrophy

9/M/42

14

Structural-metabolic causes

Right F NP encephalomalacia

10/F/27

9

Left O, F Left F Nonlat. Left FCT encephalomalacia Left F DNET Bi-temporal Left F Left F

Right T

Nonlat

NP

Nl Left FT

11/M/23

6

Structural-metabolic causes Left F DNET

12/F/32

15

Right MTLE-HS

13/F/27

20

Left MTLE-HS

Right HS, Right T dysplasia Left HS

14/F/41 15/M/22

9 13

Unknown cause Left MTLE-HS

Nl Left HS

Concomitant hand automatisms

Ictal Semiology

Number of recorded seizures/with GA

Final clinical status

Right manipulating

Arrest N left MA N right GA

5/1

Refused surgery

Right nose wiping

Bilateral MA N Left GA N right nose wiping

6/1

Refused surgery

Right nose wiping Left nose wiping, right dystonia

OA N left version N right nose wiping N right GA Left nose wiping N right hand dystonia N left GA

45/1

Left

Intermediate Slow wave on anterior of hemispheres Early Sharp wave on right temporal lobe Late Generalized slow wave Early Artifacts

Right FT

Right

Late

Slow and sharp wave on right FT

None

OA N eye deviation to right Nright GA

6/1

Left FT

Left FT

Left

Early

Slow and sharp wave on left FT

Left nose wiping, right dystonia

Left version N right dystonia N left GA N left nose wiping N confusion

2/1

Left T

Left FT

Bilat FT

Left N onset right N end

Early and late

*Onset: rhythmic theta waves on left FT *End: generalized slow and sharp wave

Left manipulating, right dystonia

1) arrest N left MA N left GA N right dystonia N right GA 2) left MA N right dystonia N left GA

Right F

Nonlat. Left FT

Right

Latepostictal

Slow wave on left FC

Right manipulating, left dystonia

Right FT

Right

Late

Slow wave on right FT

Right manipulating

Left

Early

Left version N tonic N clonic posture N right arm flexion 4 postur N left force deviation N postictal right GA 1) gastric sensation N right deviation N right GA 2) right GA N right MA N right nose wiping Right MA N right dystonia N left GA N left MA 1) voicing N left head deviation N right version N tonic N clonic postures N left GA N right dystonia 2) right head deviation N clonic postures N postictally GA 3) voicing N right version N clonic posture N tonic posture N postictally left GA N postictally agitation Right T

3/2: GAs were on left sides in all of two seizures. Twice GAs were seen in one of the seizure. The first GA in the left side, the second one in the right side (in late period) 12/1

Candidate for invasive EEG monitoring Left amygdalohippocampectomy (2014) postsurgery seizure frequency 2/year SUDEP in 2012; when waiting for right amygdala hippocampectomy Left amygdalohippocampectomy (2012): postsurgery non seizure Post surgery

Right FT

EEG during GA

Artifacts Left

1 late, 2 postictally

Right FT

Right

Intermediate Artifacts

Left FT

Left FT

Left

Late

Nonlat Left FT

CP Left FT

Right Left

Intermediate Artifacts Early Sharp wave on left temporal lobe

1) Spike and wave on anteriors of hemispheres 2) Generalized slow wave 3) Generalized slow waves

Rhythmic slow waves on left FT

Bilateral manipulating Right dystonia

Right manipulating Left Nose wiping, right dystonia None Left Nose wiping

3/1

Refused surgery

3/2: GAs are on the right side in all of two seizures

Refused surgery

3/1

Candidate for invasive EEG

10/3

Candidate for invasive EEG

3/1

Postsurgery

Right dystonia N left MA N sol GA N left nose wiping

4/1

Candidate invasive EEG

Awaking from sleep N right GA Left GA N turn head to right N left nose wiping

7/1 4/1

Candidate for invasive EEG Waiting for surgery

(DNET: Dysembryoplastic neuroepithelial tumors, F: frontal, FC: frontocentral, GA: genital automatism, HS: hippocampal sclerosis, Lat: lateralized, MA: manual automatism, MTLE: mesial temporal lobe epilepsy, Nl: normal, NP: not performed, OA: oral automatism, O: occipital, T: temporal)

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Sex/age

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Fig. 1. (A–B): The patient's (N4) ictal scalp EEG was nonlateralized; however, cranial MRI showed left hippocampal sclerosis, and he had genital automatisms of the left hand.

this automatism suggested that the perisylvian, cingulate gyrus, and paracentral lobe were the source of these automatisms [15,16]. There are limited data about sexual/genital auras. Somatosensory sensations in the genitals, reported with parietal lobe epilepsy, could be defined as genital/sexual auras [6]. None of our patients reported genital/sexual sensations. Leutmezer et al. defined genital automatisms as repeated fondling or grabbing of the genitals; and sexual automatisms as hypermotoric pelvic and truncal movements. They suggested the adjective “sexual” refers to the symptoms/signs with erotic content and the term “genital” refers to signs involving genitals without erotic components. Leutmezer et al. reported five patients with GAs who were treated with temporal lobe surgery [6]. On the other hand, some authors asserted that the source of sexual automatisms was the frontal lobe [17]. Spencer et al. demonstrated using deep electrodes that the epileptogenic foci of sexual automatisms was in the frontal lobe in 3 of 4 patients. Williamson et al. identified sexual automatisms with deep electrodes in 6 of 10 patients with FLE [18]. The most prominent clinical signs associated with orbitofrontal onset are hypermotor automatisms and thrashing movements [19]. Hypermotor movements and pelvic thrusting can be seen in psychogenic nonepileptic seizures (PNES). Psychogenic nonepileptic seizures and focal seizure discrimination can be achieved using accompanying findings such as rhythm of movements and head or eye deviation. Video-EEG monitoring is the

gold standard for the diagnosis of PNES. We detected no hypermotor sexual automatisms in our study. All GAs were identified as subtle (e.g., grabbing, fondling). Mascia et al. indicated that GAs were not beneficial signs for separating temporal or frontal lobe seizures [20]. Leutmezer et al. speculated that genital automatisms, such as grabbing or fondling the genitals, which are related to a temporal lobe seizure onset, and hypermotoric sexual automatisms such as pelvic or truncal thrusting, eventually combine with manipulations of the genitals; these automatisms are common in frontal lobe seizures [6]. On the other hand, Currier et al. [21] reported two patients with sexual automatisms like pelvic thrusting, and indicated temporal lobe origin of their seizures. Our results suggest that GAs are more common in temporal lobe seizures than frontal lobe seizures (9/3). Three of our patients (N9, N10, and N11) had FLE, 9 had TLE, and all had hippocampal sclerosis. Genital automatisms were 88.9% ipsilateral in temporal lobe epilepsy (TLE). Hand automatisms are one of the main characteristics of focal seizures, occurring in N80%, [4,20] and they occur in only one hand in 9–40% of patients [23,24]. Unilateral manipulative hand automatisms, including postictal nose wiping, usually indicate ipsilateral focus, whereas unilateral dystonia almost always indicates a contralateral hemisphere focus. If a unilateral hand automatism was accompanied by contralateral hand dystonia, it had a high lateralizing value to the

Fig. 2. The evaluation lateralization and localization value of GAs.

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Fig. 3. A–B. (N 7): Rhythmic 7 Hz sharp waves were seen in the left temporal region at the beginning of the seizure. Synchronously, he had genital automatisms in the left hand and a dystonic posture in the right hand (Fig. 3A). The EEG showed subsequently irregular slow waves and spikes in the right temporal lobe (switch phenomenon) accompanying genital automatisms in the right hand (Fig. 3B).

ipsilateral epileptic focus; it was ipsilateral in 85% of patients [1]. Rhythmic ictal nonclonic hand motions were contralateral to the seizure onset in 83.3% of patients and 91.7% of seizures [25]. Postictal nose wiping was seen in almost 60% of patients with TLE, and the lateralizing ipsilateral seizure focus was approximately 90% [26]. Fogarasi et al. reported the hand used for GA was more frequently (88.9%) ipsilateral to the seizure onset zone [22]. However, Mascia et al. disclosed no lateralizing value for genital automatisms [20]. We found that GAs indicated the ipsilateral hemisphere in 80% of patients. This ratio increased to 88.9% in patients with TLE. Automatisms indicated the ipsilateral hemisphere in all our patients with FLE. We demonstrated the correlation of GAs with ‘other hand’ automatisms. Nose wiping and manual automatisms associated with ipsilateral GAs were seen in 84.6% of our patients. Unilateral dystonia was contralateral with GAs in all patients. It is unclear whether ictal automatisms are caused by spreading ictal epileptic activity or whether they are a release phenomenon [27,28].

The origin of ictal manual automatisms is controversial. Hand automatisms can occur by stimulating the anterior gyrus cinguli and mesiotemporal structures. Automatisms may be caused by spreading ictal activity [28]. Others suggest that automatisms may be a release phenomenon during partially disturbed consciousness. Another hypothesis for GAs is that they may occur as a nonspecific reaction to an internal stimulus, such as urinary urge [29]]. None of our patients had any of these symptoms. We identified GAs in seizures that originated from both the dominant and nondominant hemisphere. Genital automatisms can be seen at any time of the ictal or postictal period [22]. We generally detected GAs during the seizure and there was no relation with the period of GAs and lateralization. These findings suggest that GAs are important but underestimated semiologic characteristics, which strongly correlate with an ipsilateral epileptic focus. Awareness of the increasing number of patients showing this special phenomenon will provide more valuable knowledge on semiology.

Fig. 4. The ictal invasive EEG showed rhythmic sharp waves in the left anterior temporal region at the beginning of the seizure. At the same time, he had genital automatisms in the left hand.

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