Epilepsy & Behavior 44 (2015) 253–257
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Ictal body turning in focal epilepsy Metin Mercan a,⁎, İrem Yıldırım a, Özgür Akdemir b, Erhan Bilir a a b
Gazi University Faculty of Medicine, Department of Neurology, Ankara, Turkey Gazi University Faculty of Medicine, Department of Nuclear Medicine, Ankara, Turkey
a r t i c l e
i n f o
Article history: Received 29 July 2014 Revised 6 November 2014 Accepted 8 November 2014 Available online 10 March 2015 Keywords: Body turning Head turning Temporal lobe epilepsy
a b s t r a c t Despite the explanations of many lateralization findings, body turning in focal epilepsy has been rarely investigated. One of the aims of this study was to evaluate the role of ictal body turning in the lateralization of focal epilepsies. The records of 263 patients with focal epilepsy (temporal lobe epilepsy (TLE), n = 178; extratemporal lobe epilepsy (ETLE), n = 85) who underwent prolonged video-EEG monitoring during presurgical epilepsy evaluation were reviewed. Preoperative findings (TLE, n = 16; ETLE, n = 6) and postoperative outcomes (TLE, n = 7) of patients with focal epilepsy with ictal body turning were assessed. For the evaluation of ictal body turning, two definitions were proposed. Nonversive body turning (NVBT) was used to denote at least a 90° nonforced (without tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Versive body turning (VBT) was used to denote at least a 90° forced (with tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Nonversive body turning was observed in 6% (n = 11) of patients with TLE and 2% (n = 2) of patients with ETLE. For VBT, these ratios were 5% (n = 8) and 7% (n = 6) for patients with TLE and ETLE, respectively. Nonversive body turning was frequently oriented to the same side as the epileptogenic zone (EZ) in TLE and ETLE seizures (76% and 80%, respectively). If the amount of NVBT was greater than 180°, then it was 80% to the same side in TLE seizures. Versive body turning was observed in 86% of the TLE seizures, and 55% of the ETLE seizures were found to be contralateral to the EZ. When present with head turning, NVBT ipsilateral to the EZ and VBT contralateral to the EZ were more valuable for lateralization. In TLE seizures, a significant correlation was found between the head turning and body turning onsets and durations. Our study demonstrated that ictal body turning is a rarely observed but reliable lateralization finding in TLE and ETLE seizures, which also probably has the same pathophysiological mechanism as head turning in TLE seizures. © 2014 Elsevier Inc. All rights reserved.
1. Introduction The most important phase of surgical treatment decisions in focal epilepsies is the detection of the epileptogenic zone (EZ). Therefore, many semiologic and neuroimaging studies have focused on the detection of the EZ. Investigating different clinical symptoms and electroencephalography (EEG) recordings of the cortical areas activated by the EZ has revealed relationships between these behaviors and localization and lateralization of the EZ [1,2]. However, there are not enough data on the occurrence of body turning during seizures of patients with focal epilepsy, and only a few studies have investigated the role of EZ detection in ictal body turning [3–5]. Seizures containing ictal body turning are known as rotatory, volvular, circling, and gyratory seizures in the literature. Most of the data were collected from case reports, and there is no consensus about the definition [6–8]. These seizures were observed by ⁎ Corresponding author at: Gazi University Faculty of Medicine, Department of Neurology, Beşevler, 06560 Ankara, Turkey. Tel.: +90 312 202 53 28, +90 506 909 36 63 (GSM); fax: +90 312 212 90 16. E-mail address: [email protected] (M. Mercan).
http://dx.doi.org/10.1016/j.yebeh.2014.11.005 1525-5050/© 2014 Elsevier Inc. All rights reserved.
Gastaut et al. in primarily generalized epilepsy and were defined as turning of half of the body. However, some authors have stated that these seizures can also occur in focal epilepsy and defined them as at least a 180° rotation around the body axis [3,9]. The goals of this study were to 1) investigate the role of ictal body turning in focal epilepsies during the localization and lateralization of the EZ, 2) report the results of the presurgical and postsurgical evaluations, and 3) form an opinion on the pathophysiological mechanism of these seizures. 2. Methods 2.1. Patient data Two hundred and sixty-three patients with focal epilepsy were admitted to the Gazi University Faculty of Medicine (GUFOM) between 2009 and 2014 for three to seven days, on whom video-EEG monitoring was performed and who were included in the study (temporal lobe epilepsy (TLE), n = 178; extratemporal lobe epilepsy (ETLE), n = 85). After all of the videos were examined, patients with ictal body turning
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(n = 22) were evaluated for their clinical history, video-EEG monitoring, magnetic resonance imaging (MRI), [18F]-fluorodeoxyglucose (FDG) positron emission tomography (PET), pathology findings, and postoperative outcomes. The study was approved by the local ethics committee of the GUFOM. 2.2. Epileptic syndrome classification and seizure analysis Seizures and epileptic syndromes were classified according to the International League Against Epilepsy (ILAE) diagnostic criteria [10]. The video-EEG results and clinical symptoms were reassessed by at least two experienced epileptologists at the same time. Epileptogenic zone localization was determined based on their epilepsy surgery council decisions. Patients with focal epilepsy with ictal body turning were separated into two groups: TLE (n = 16) and ETLE (n = 6). Ictal body turning was present during complex partial seizures (CPSs) (n = 39) and/or secondarily generalized tonic–clonic seizures (sGTCSs) (n = 23). 2.2.1. Body turning terminology and inclusion–exclusion criteria Because there are insufficient data on the definition of ictal body turning in the literature, two definitions, nonversive body turning (NVBT) and versive body turning (VBT), were proposed in our study. Nonversive body turning was used to denote at least a 90° nonforced (without tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Versive body turning was used to denote at least a 90° forced (with tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Each of the patients who turned to their side to notify others of the seizure turned from the side to lie on her/his back during their aura, and those with partial consciousness who turned while watching a relative or when she/he heard a sound were excluded. The start of the rotation in the shoulder in NVBT and VBT was accepted as the onset of ictal body turning, and the end of the movement acceleration or the start of the movement to the opposite side was accepted as the ending of ictal body turning. All onsets and durations of the ictal body turning were calculated for each NVBT and VBT seizure. 2.2.2. Lateralizing motor signs Nonversive head turning (NVHT) is defined as at least a 30° involuntary head rotation lasting longer than 2 s without a forced deviation within the first 60 s of the seizure, whereas versive head turning (VHT) is defined as an involuntary and forced head rotation lasting longer than 5 s accompanied with clonic or tonic activity [11–14]. In this study, an involuntary head rotation of at least 45° from the midline (chin and sternum line) for a minimum of 3 s was regarded as NVHT. Versive head turning was assessed based on the definition in the literature. The inclusion and exclusion criteria of body turning were also applied for head turning. The onsets and durations of NVHT and VHT were calculated in the same manner as those of NVBT and VBT. Other lateralization symptoms from focal seizures that occurred besides ictal body turning, such as unilateral tonic posturing, unilateral hand automatisms, postictal nose wiping, figure-of-4 sign, and asymmetric ending of clonic jerks, were also assessed [15]. 2.3. Video-EEG and neuroimaging Continuous scalp video-EEG monitoring using 32 channels was performed with surface electrodes (with additional temporal electrodes) placed according to the international 10–20 system. Not only ictal EEG recordings during body turning but also interictal and postictal EEG changes were assessed in patients with TLE and ETLE [16]. Possible etiologic diagnoses of patients without pathology results were made using imaging. For all patients (n = 22), radiologic assessment was performed via high-resolution magnetic resonance imaging (MRI) at 3 T using a standardized epilepsy protocol. For mesial temporal
sclerosis (MTS), diagnosis of hippocampal atrophy, loss of distinction between gray matter and white matter, and a hippocampal signal increase were considered major findings [17]. The MTS diagnosis was further supported using magnetic resonance spectroscopy (MRS) findings, such as the reduction of the NAA peak and/or reduced NAA/ Cho + Cr ratio. The blood flow in the parahippocampal regions were virtually assessed using perfusion MRI and regional brain hypometabolism with 18F-FDG PET (n = 19). The dominant hemisphere for language was determined using functional MRI (n = 10). Surgical outcomes of the patients who underwent lesionectomy or anterior temporal lobectomy were assessed by Engel's classification [18]. 2.4. Statistical analyses The data were analyzed using SPSS version 15.0 for Windows. The chi-square test or Fisher's exact test, where appropriate, was used to compare the clinical or video-EEG monitoring data of patients with TLE and ETLE. The Mann–Whitney U test was performed in comparison of unequally distributed parametric variables including age, age at seizures onset, duration of epilepsy, and the body turning characteristics between both groups. Spearman's correlation was used to assess the correlation between NVBT and NVHT and VBT and VHT. p values of less than 0.05 are reported as statistically significant. 3. Results 3.1. Demographic data Sixteen patients with TLE (9%) and six patients with ETLE (7%) had at least one 90° ictal body turning in their CPSs and/or sGTCSs. Seven patients with TLE (4%) and two patients with ETLE (2%) had greater than 180° ictal body turning during at least one seizure (180°–540°). Fiftynine percent of the patients had seizures starting from the left hemisphere; this rate was 89% for patients (TLE, n = 6; ETLE, n = 2) with greater than 180° of body turning. No significant difference was observed between patients with TLE and ETLE regarding age, age at seizure onset, epilepsy duration, and risk factors (p N 0.05). The history of febrile convulsion and aura was more frequent in patients with TLE compared to patients with ETLE; however, this difference was not statistically significant (p N 0.05). Patients with TLE had autonomic (n = 7), psychic (n = 4), and vertiginous (n = 1) auras, while patients with ETLE had visual (n = 2) auras. In patients with ETLE, sGTCSs were more frequent, although this observation just missed statistical significance (p = 0.056) (Table 1). While Table 1 Clinical data of the patients. TLE (n = 16) ETLE (n = 6) p value Gender (female/male) Agea Age at seizure onset, yearsa Duration of epilepsy, yearsa Focal epilepsy with left hemisphere onset Risk factors History of febrile convulsions History of perinatal complications History of head trauma History of CNS infections Family history of epilepsy Consanguinity among parents Aura Seizure type frequency N4/month (CPSs) N1/year (sGTCSs)
10/6 26,5 (17–42) 10,5 (2–23) 15 (8–31) 11 (69%)
1/5 24 (22–42) 7,8 (4–13) 16,5 (11–35) 2 (33%)
0.740 0.630 0.297 0.711 0.178
11 (69%) 2 (13%) 3 (19%) 0 4 (25%) 3 (19%) 12 (75%)
1 (17%) 1 (17%) 3 (50%) 0 3 (50%) 2 (33%) 2 (33%)
0.560 1.000 0.283 0.334 0.585 0.137
11 (69%) 5 (31%)
5 (83%) 5 (83%)
0.634 0.560
TLE, temporal lobe epilepsy; ETLE, extratemporal lobe epilepsy; sGTCSs, secondarily generalized tonic–clonic seizures; CPSs, complex partial seizures; CNS, central nervous system. a Median (IQR).
M. Mercan et al. / Epilepsy & Behavior 44 (2015) 253–257
50% of patients with TLE had no history of sGTCSs, this rate was 17% for patients with ETLE.
3.2. Seizure semiology on video-EEG recording In the video-EEG monitoring data, the CPSs of patients with ETLE turned into sGTCSs with a statistically significantly higher rate compared to patients with TLE (p = 0.006). Nonversive body turning was only observed in CPSs. In addition, NVBT started in the first one-third part of the seizure in 91% (n = 31) of TLE seizures. This rate was 80% (n = 4) in ETLE seizures. Versive body turning was observed right before or during the tonic phase of sGTCSs. Temporal lobe onset CPSs (45% of 76 seizures) had NVBT more frequently than ETLE onset CPSs (14% of 37 seizures), which was found to be statistically significant (p = 0.002). No significant difference between TLE and ETLE seizures was found regarding the VBT frequency (p = 0.456). Additionally, no significant difference between TLE and ETLE seizures was found regarding the NVBT and VBT onsets and durations (p N 0.05) (Table 2). Nonversive body turning was observed in 6% (n = 11) of patients with TLE and 2% (n = 2) of patients with ETLE. In 76% (n = 26) of the seizures with NVBT in patients with TLE, the body rotated to the EZ's side. This rate increased to 88% when NVHT was also present with NVBT. In nearly all of the seizures, NVHT and NVBT were to the same side (except in one seizure in which NVHT and NVBT were opposite). A significant correlation between the NVHT and NVBT onsets and durations was found (rho = 0.470, p = 0.016; rho = 0.702, p = 0.000). The NVBT to the EZ's side was 80% (n = 4) in the ETLE seizures, and in only two of the five seizures, both NVHT and NVBT were present together. In 80% of the 15 TLE seizures with greater than 180° NVBT, the body rotated to the EZ's side. Versive body turning was observed in 5% (n = 8) of patients with TLE and 7% (n = 6) of patients with ETLE. In 86% (n = 12) of the seizures, VBT in patients with TLE was to the opposite side of the EZ, whereas this rate was 56% (n = 5) in the ETLE seizures. This rate increased to 92% when VHT was also present with VBT (92% in TLE seizures and 71% in ETLE seizures). Versive body turning greater than 180° occurred only in one seizure. In TLE seizures, a significant correlation was found between the VHT and VBT onsets and durations (rho = 0.826, p = 0.000; rho = 0.683, p = 0.01), whereas in ETLE seizures, the correlation between the VHT and VBT onsets and durations was
Table 2 Video-EEG monitoring data.
Total CPSs Total sGTCSs NVBT VBT NVBT onset (s)a NVBT duration (s)a VBT onset (s)a VBT duration (s)a Interictal EEG Unilateral temporal Unilateral hemispheric Ictal EEG during NVBT Unilateral T or FT Unilateral hemispheric Nonfocal and nonlateralized Postictal EEG Unilateral temporal Unilateral hemispheric
TLE (n = 16)
ETLE (n = 6)
76 27 (36%) 34 (45%) 14 (52%) 10 (0–48) 13 (3–57) 30 (14–150) 9 (4–26) n = 16 12 (75%) 4 (25%) n = 34 20 (59%) 4 (12%) 10 (29%) n = 40 14 (33%) 9 (22%)
37 24 (65%) 5 (14%) 9 (38%) 7 (1–25) 5 (3–23) 28 (17–42) 6 (4–22) n=6 0 6 (100%) n=5 0 2 (40%) 3 (60%) n = 13 0 8 (62%)
p value 0.006 0.002 0.456 0.817 0.178 0.777 0.590
TLE, temporal lobe epilepsy; ETLE, extratemporal lobe epilepsy; sGTCSs, secondarily generalized tonic–clonic seizures; CPSs, complex partial seizures; NVBT, nonversive body turning; VBT, versive body turning; T, temporal; FT, frontotemporal. Significance was assigned for all tests at p N 0.05 (bold figures). a Median (IQR).
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not statistically significant (rho = 0.643, p = 0.119; rho = 0.057, p = 0.904). The most common lateralization findings accompanying NVBT in TLE seizures were manual automatism (n = 29; 85%), NVHT (n = 24; 71%), dystonic posture (n = 19; 56%), and postictal nose wiping (n = 4; 12%). Nonversive body turning was the only lateralization sign in 12% (n = 4) of the TLE seizures. In ETLE seizures, the lateralization findings were manual automatism (n = 1) and bilateral dystonic posture (n = 1). Versive head turning was the most common lateralization finding and was observed in the sGTCSs of patients with TLE and ETLE (93% and 78%, respectively). Asymmetric clonic ending was the second most common lateralization finding in sGTCSs with ictal body turning (TLE, 36%; ETLE, 44%), and it was always on the same side with the EZ. Lateralization signs of TLE and ETLE seizures were shown in Table 3. 3.3. EEG, imaging findings, and surgery outcomes During NVBT, rhythmical activity between 5 and 12 Hz was observed in the ictal EEG. This activity was localized in the unilateral temporal and frontotemporal regions in 59% of the TLE seizures and was lateralized to the unilateral hemisphere in 40% of the ETLE seizures (Table 2). Fifty-six percent of the patients with TLE had mesial temporal sclerosis (MTS), consistent with the MRI results (two patients' pathology results indicated MTS), and ipsilateral anterior temporal hypometabolism was the most frequent finding in 18F-FDG PET. However, in almost all other etiologic cases, except for MTS, the lesion was located in the parahippocampal region in the anterior temporal lobe. In patients with ETLE, multilobar abnormalities (e.g., frontotemporal cystic lesion and occipitoparietal DNET) were more frequently observed. It was revealed with fMRI that one patient with TLE with right NVBT had a right hemisphere dominance for language. Three patients underwent lesionectomies, and four underwent anterior temporal lobectomies (ATL); in 66% of the patients, the surgical outcome was consistent with Engel 1 (Table 4). One patient who underwent ATL was lost in follow-up. 4. Discussion In our study, ictal body turning was present in patients with both TLE and ETLE. Nonversive body turning was seen only during CPSs; however, VBT was observed right before or during the tonic phase of sGTCSs. Our study revealed that NVBT and VBT are reliable lateralization findings in TLE seizures. During most of the seizures, NVBT was ipsilateral to the EZ whereas VBT was contralateral. Moreover, NVBT was more reliable in EZ lateralization when accompanied with NVHT. A similar Table 3 Lateralization findings in complex partial seizures and secondarily generalized tonic– clonic seizures with ictal body turning. Lateralization findings
Nonversive body turning Versive body turning Nonversive head turning Versive head turning Unilateral manual automatisms Unilateral dystonic posturing Nose wiping Asymmetric ending of clonic jerks Figure-of-4 sign
Number of TLE seizures (n = 48)
Number of ETLE seizures (n = 14)
Ipsilateral
Contralateral
Ipsilateral
Contralateral
26 2 21 0 25
8 12 3 13 4
4 4 1 2 1
1 5 1 5 0
1
18
0
0
3 5
1 0
0 4
0 0
0
3
1
2
TLE, temporal lobe epilepsy; ETLE, extratemporal lobe epilepsy.
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Table 4 Diagnostic information. TLE (n = 16)
ETLE (n = 6)
MRI diagnosis Mesial temporal sclerosis Neuronal migration defect Tumor Vascular pathology Encephalomalacia Dual pathology Normal
9 (56%) 1 (6%) 3 (19%) 1 (6%) 0 1 (6%) 1 (6%)
0 2 (33%) 2 (33%) 0 1 (17%) 0 1 (17%)
MRS (n = 13) Lateralization Normal
9 (70%) 4 (30%)
Perfusion MRI (n = 9) Lateralization Normal
7 (77%) 2 (13%)
PET Ipsilateral AT hypometabolism Multilobar hypometabolism Normal
12 (80%) 3 (20%) 0
Functional MRI (n = 10) Left dominant hemisphere Right dominant hemisphere
9 (90%) 1 (10%)
Histopathological findings (n = 7) Hippocampal sclerosis Dysplasia Tumor Vascular pathology
3 (43%) 1 (14%) 2 (29%) 1 (14%)
Surgical outcomes (n = 6) Engel I Engel II Engel III Engel IV
4 (66%) 1 (17%) 1 (17%) 0
1 (25%) 3 (75%) 0
MRI, magnetic resonance imaging; MRS, magnetic resonance spectroscopy; PET, perfusion emission tomography; and AT; anterior temporal.
situation was found for VBT in TLE seizures. According to our results, NVBT on its own is a reliable lateralization finding in ETLE seizures whereas VBT is not. This may be caused by the lower number of ETLE seizures or rapid spreading of seizure activity over both hemispheres in ETLE seizures. Data on turning during seizures are mostly based on patient statements and are defined in primarily generalized epilepsies and focal epilepsies caused by brain tumors, Wilson's disease, or tuberous sclerosis [6,7,9,19,20]. There are only a few studies conducted using video-EEG monitoring. It was stated in a study with patients with epilepsy who had 180° and greater amounts of body turning during seizures that ictal body turning was frequently present in frontal lobe epilepsies (17%) and rarely occurs in temporal lobe epilepsies (2%). It was also stated in the same study that if VHT was present before body turning, the EZ was contralateral to the body's rotation side, and if body turning did not have VHT, then it was ipsilateral to the body's rotation side [3]. A study on patients who exhibited trunk rotation of over 90° and longer than 10 s revealed that the EZ was 92% contralateral to the rotation side [4]. There is a study claiming that ictal body turning may be present in mesial frontal lobe epilepsy [5]. However, these studies used different turning definitions and are not entirely clear about the turning characteristics. Therefore, to identify ictal body turning, we recommended two definitions as NBVT and VBT according to the clinical characteristics of body movement. In the literature, NVHT was present in 70% of TLE seizures, with 87–94% being to the same side as the EZ. Nonversive head turning was usually present with dystonic extremity posture (71–96%), and it was noted that these two phenomena's pathophysiologic mechanisms may be related [11–13]. A few ictal SPECT studies indicated that during unilateral dystonia, there was hyperperfusion in the striatum and
dorsolateral thalamus ipsilateral to the EZ [21–23]. Interictal PET studies indicated that dystonic posture is related with striatal hypometabolism [24,25]. All of these studies indicate that NVHT and unilateral dystonia are associated with basal ganglia involvement. In our study, NVBT was frequently accompanied with NVHT and/or unilateral dystonia. Furthermore, a high correlation between the NVBT and NVHT characteristics was present in TLE seizures. As a result, our study suggests that TLE seizure ictal spread patterns during head and body turning may be similar. The cause of turning during seizures is not entirely understood, but there are a few hypotheses. One hypothesis suggests that the turning is due to imbalance in the striatum; imbalance in striatal dopamine due to activation in the nucleus accumbens may lead to postural asymmetry determining the rotation side. Neurochemistry studies in rats indicated that an asymmetrical increase in striatal dopamine metabolism leads to contralateral turning [26–28]. Löscher et al. state that turning is related to the decrease in ipsilateral dopamine metabolism [29]. It is also known that changes in cortical epileptiform activity or turning movements may occur with caudate nucleus stimulation [30,31]. It is claimed that in TLE seizures, when epileptic activity is spreading from the mesial structure to other zones in the hemisphere, 2- to 10-Hz frequency activity is observed in the basal ganglia, and thus, the basal ganglia prevent the spread of ictal activity to other zones in the hemisphere [32,33]. Feddersen et al. reported that unilateral dystonic posture prevents the generalization of the seizure in focal epilepsies [34]. The possible antiepileptic activity of the striatum is considered to be due to the substantia nigra pars reticulata's GABAergic modulation [35]. Jung et al. demonstrated in patients with mesial temporal lobe epilepsy that after seizure onset, a strong rhythmic 6- to 10-Hz theta to alpha activity in the ipsilateral medial temporal region was observed at the same time as a dipole cluster of the basal ganglia [36]. As a result, one may assume that altered basal ganglia activity results in turning movement during a seizure. Dystonic posture or excessive immobility in the contralateral extremity and a comparative movement increase in ipsilateral extremity (head, hand, and trunk) may lead to turning movement. In our study, we observed 5to 12-Hz rhythmic EEG activation and contralateral extremity dystonia accompanying NVHT during NVBT which support the relationship of NVBT with the activity in the basal ganglia. Versive head turning that is present in 35–45% of TLE and ETLE seizures and before sGTCSs is counted as a highly reliable lateralization finding (over 90% being contralateral to the EZ) [11,14,37]. Studies indicated that stimulation of the cortical eye field leads to contralateral head version in 58% of patients [38]; SPECT studies also support this view [23, 39]. In our study, VHT and VBT were present together in almost all of the TLE seizures and were significantly correlated. This finding supports the view that VBT occurs due to frontal eye field spreading to neighboring areas, such as VHT in TLE seizures. The reason why this correlation is not present in ELTE seizures may be the lower number of seizures, the zones being multifocal, or the differences in the ictal spread patterns. There are some limitations in our study. The lower number of ETLE seizures may affect the generalizability of the results. In addition, there is a lack of measurement tools for the calculation of the degree of body and head turnings (such as video-based software). Of the 22 patients, there were only six who underwent epilepsy surgery, and most of the patients were lost during follow-up, which makes the interpretation of the data more difficult regarding the identification of the epileptogenic zone. In conclusion, NVBT ipsilateral to the EZ and VBT contralateral to the EZ are valuable lateralization findings in TLE and ETLE seizures. When present with head turning, NVBT ipsilateral to the EZ and VBT contralateral to the EZ are more valuable for lateralization. In TLE seizures, both versive body turning and nonversive body turning are probably caused by two different pathophysiological mechanisms similarly to head turning. Whereas NVBT is more related with basal ganglia involvement, VBT seems to be related with cortical area spreading. Although a valuable lateralization finding, further studies are required to understand the pathophysiology of ictal body turning.
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Acknowledgments This study was not supported by government agencies or private foundations. Disclosure of conflicts of interest None of the authors has any conflicts of interest to disclose. We confirm that we have read the journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Ictal body turning in focal epilepsy Metin Mercan a,⁎, İrem Yıldırım a, Özgür Akdemir b, Erhan Bilir a a b
Gazi University Faculty of Medicine, Department of Neurology, Ankara, Turkey Gazi University Faculty of Medicine, Department of Nuclear Medicine, Ankara, Turkey
a r t i c l e
i n f o
Article history: Received 29 July 2014 Revised 6 November 2014 Accepted 8 November 2014 Available online 10 March 2015 Keywords: Body turning Head turning Temporal lobe epilepsy
a b s t r a c t Despite the explanations of many lateralization findings, body turning in focal epilepsy has been rarely investigated. One of the aims of this study was to evaluate the role of ictal body turning in the lateralization of focal epilepsies. The records of 263 patients with focal epilepsy (temporal lobe epilepsy (TLE), n = 178; extratemporal lobe epilepsy (ETLE), n = 85) who underwent prolonged video-EEG monitoring during presurgical epilepsy evaluation were reviewed. Preoperative findings (TLE, n = 16; ETLE, n = 6) and postoperative outcomes (TLE, n = 7) of patients with focal epilepsy with ictal body turning were assessed. For the evaluation of ictal body turning, two definitions were proposed. Nonversive body turning (NVBT) was used to denote at least a 90° nonforced (without tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Versive body turning (VBT) was used to denote at least a 90° forced (with tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Nonversive body turning was observed in 6% (n = 11) of patients with TLE and 2% (n = 2) of patients with ETLE. For VBT, these ratios were 5% (n = 8) and 7% (n = 6) for patients with TLE and ETLE, respectively. Nonversive body turning was frequently oriented to the same side as the epileptogenic zone (EZ) in TLE and ETLE seizures (76% and 80%, respectively). If the amount of NVBT was greater than 180°, then it was 80% to the same side in TLE seizures. Versive body turning was observed in 86% of the TLE seizures, and 55% of the ETLE seizures were found to be contralateral to the EZ. When present with head turning, NVBT ipsilateral to the EZ and VBT contralateral to the EZ were more valuable for lateralization. In TLE seizures, a significant correlation was found between the head turning and body turning onsets and durations. Our study demonstrated that ictal body turning is a rarely observed but reliable lateralization finding in TLE and ETLE seizures, which also probably has the same pathophysiological mechanism as head turning in TLE seizures. © 2014 Elsevier Inc. All rights reserved.
1. Introduction The most important phase of surgical treatment decisions in focal epilepsies is the detection of the epileptogenic zone (EZ). Therefore, many semiologic and neuroimaging studies have focused on the detection of the EZ. Investigating different clinical symptoms and electroencephalography (EEG) recordings of the cortical areas activated by the EZ has revealed relationships between these behaviors and localization and lateralization of the EZ [1,2]. However, there are not enough data on the occurrence of body turning during seizures of patients with focal epilepsy, and only a few studies have investigated the role of EZ detection in ictal body turning [3–5]. Seizures containing ictal body turning are known as rotatory, volvular, circling, and gyratory seizures in the literature. Most of the data were collected from case reports, and there is no consensus about the definition [6–8]. These seizures were observed by ⁎ Corresponding author at: Gazi University Faculty of Medicine, Department of Neurology, Beşevler, 06560 Ankara, Turkey. Tel.: +90 312 202 53 28, +90 506 909 36 63 (GSM); fax: +90 312 212 90 16. E-mail address: [email protected] (M. Mercan).
http://dx.doi.org/10.1016/j.yebeh.2014.11.005 1525-5050/© 2014 Elsevier Inc. All rights reserved.
Gastaut et al. in primarily generalized epilepsy and were defined as turning of half of the body. However, some authors have stated that these seizures can also occur in focal epilepsy and defined them as at least a 180° rotation around the body axis [3,9]. The goals of this study were to 1) investigate the role of ictal body turning in focal epilepsies during the localization and lateralization of the EZ, 2) report the results of the presurgical and postsurgical evaluations, and 3) form an opinion on the pathophysiological mechanism of these seizures. 2. Methods 2.1. Patient data Two hundred and sixty-three patients with focal epilepsy were admitted to the Gazi University Faculty of Medicine (GUFOM) between 2009 and 2014 for three to seven days, on whom video-EEG monitoring was performed and who were included in the study (temporal lobe epilepsy (TLE), n = 178; extratemporal lobe epilepsy (ETLE), n = 85). After all of the videos were examined, patients with ictal body turning
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(n = 22) were evaluated for their clinical history, video-EEG monitoring, magnetic resonance imaging (MRI), [18F]-fluorodeoxyglucose (FDG) positron emission tomography (PET), pathology findings, and postoperative outcomes. The study was approved by the local ethics committee of the GUFOM. 2.2. Epileptic syndrome classification and seizure analysis Seizures and epileptic syndromes were classified according to the International League Against Epilepsy (ILAE) diagnostic criteria [10]. The video-EEG results and clinical symptoms were reassessed by at least two experienced epileptologists at the same time. Epileptogenic zone localization was determined based on their epilepsy surgery council decisions. Patients with focal epilepsy with ictal body turning were separated into two groups: TLE (n = 16) and ETLE (n = 6). Ictal body turning was present during complex partial seizures (CPSs) (n = 39) and/or secondarily generalized tonic–clonic seizures (sGTCSs) (n = 23). 2.2.1. Body turning terminology and inclusion–exclusion criteria Because there are insufficient data on the definition of ictal body turning in the literature, two definitions, nonversive body turning (NVBT) and versive body turning (VBT), were proposed in our study. Nonversive body turning was used to denote at least a 90° nonforced (without tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Versive body turning was used to denote at least a 90° forced (with tonic or clonic component) rotation of the upper (shoulder) and lower (hip) parts of the body around the body axis for a minimum of 3 s. Each of the patients who turned to their side to notify others of the seizure turned from the side to lie on her/his back during their aura, and those with partial consciousness who turned while watching a relative or when she/he heard a sound were excluded. The start of the rotation in the shoulder in NVBT and VBT was accepted as the onset of ictal body turning, and the end of the movement acceleration or the start of the movement to the opposite side was accepted as the ending of ictal body turning. All onsets and durations of the ictal body turning were calculated for each NVBT and VBT seizure. 2.2.2. Lateralizing motor signs Nonversive head turning (NVHT) is defined as at least a 30° involuntary head rotation lasting longer than 2 s without a forced deviation within the first 60 s of the seizure, whereas versive head turning (VHT) is defined as an involuntary and forced head rotation lasting longer than 5 s accompanied with clonic or tonic activity [11–14]. In this study, an involuntary head rotation of at least 45° from the midline (chin and sternum line) for a minimum of 3 s was regarded as NVHT. Versive head turning was assessed based on the definition in the literature. The inclusion and exclusion criteria of body turning were also applied for head turning. The onsets and durations of NVHT and VHT were calculated in the same manner as those of NVBT and VBT. Other lateralization symptoms from focal seizures that occurred besides ictal body turning, such as unilateral tonic posturing, unilateral hand automatisms, postictal nose wiping, figure-of-4 sign, and asymmetric ending of clonic jerks, were also assessed [15]. 2.3. Video-EEG and neuroimaging Continuous scalp video-EEG monitoring using 32 channels was performed with surface electrodes (with additional temporal electrodes) placed according to the international 10–20 system. Not only ictal EEG recordings during body turning but also interictal and postictal EEG changes were assessed in patients with TLE and ETLE [16]. Possible etiologic diagnoses of patients without pathology results were made using imaging. For all patients (n = 22), radiologic assessment was performed via high-resolution magnetic resonance imaging (MRI) at 3 T using a standardized epilepsy protocol. For mesial temporal
sclerosis (MTS), diagnosis of hippocampal atrophy, loss of distinction between gray matter and white matter, and a hippocampal signal increase were considered major findings [17]. The MTS diagnosis was further supported using magnetic resonance spectroscopy (MRS) findings, such as the reduction of the NAA peak and/or reduced NAA/ Cho + Cr ratio. The blood flow in the parahippocampal regions were virtually assessed using perfusion MRI and regional brain hypometabolism with 18F-FDG PET (n = 19). The dominant hemisphere for language was determined using functional MRI (n = 10). Surgical outcomes of the patients who underwent lesionectomy or anterior temporal lobectomy were assessed by Engel's classification [18]. 2.4. Statistical analyses The data were analyzed using SPSS version 15.0 for Windows. The chi-square test or Fisher's exact test, where appropriate, was used to compare the clinical or video-EEG monitoring data of patients with TLE and ETLE. The Mann–Whitney U test was performed in comparison of unequally distributed parametric variables including age, age at seizures onset, duration of epilepsy, and the body turning characteristics between both groups. Spearman's correlation was used to assess the correlation between NVBT and NVHT and VBT and VHT. p values of less than 0.05 are reported as statistically significant. 3. Results 3.1. Demographic data Sixteen patients with TLE (9%) and six patients with ETLE (7%) had at least one 90° ictal body turning in their CPSs and/or sGTCSs. Seven patients with TLE (4%) and two patients with ETLE (2%) had greater than 180° ictal body turning during at least one seizure (180°–540°). Fiftynine percent of the patients had seizures starting from the left hemisphere; this rate was 89% for patients (TLE, n = 6; ETLE, n = 2) with greater than 180° of body turning. No significant difference was observed between patients with TLE and ETLE regarding age, age at seizure onset, epilepsy duration, and risk factors (p N 0.05). The history of febrile convulsion and aura was more frequent in patients with TLE compared to patients with ETLE; however, this difference was not statistically significant (p N 0.05). Patients with TLE had autonomic (n = 7), psychic (n = 4), and vertiginous (n = 1) auras, while patients with ETLE had visual (n = 2) auras. In patients with ETLE, sGTCSs were more frequent, although this observation just missed statistical significance (p = 0.056) (Table 1). While Table 1 Clinical data of the patients. TLE (n = 16) ETLE (n = 6) p value Gender (female/male) Agea Age at seizure onset, yearsa Duration of epilepsy, yearsa Focal epilepsy with left hemisphere onset Risk factors History of febrile convulsions History of perinatal complications History of head trauma History of CNS infections Family history of epilepsy Consanguinity among parents Aura Seizure type frequency N4/month (CPSs) N1/year (sGTCSs)
10/6 26,5 (17–42) 10,5 (2–23) 15 (8–31) 11 (69%)
1/5 24 (22–42) 7,8 (4–13) 16,5 (11–35) 2 (33%)
0.740 0.630 0.297 0.711 0.178
11 (69%) 2 (13%) 3 (19%) 0 4 (25%) 3 (19%) 12 (75%)
1 (17%) 1 (17%) 3 (50%) 0 3 (50%) 2 (33%) 2 (33%)
0.560 1.000 0.283 0.334 0.585 0.137
11 (69%) 5 (31%)
5 (83%) 5 (83%)
0.634 0.560
TLE, temporal lobe epilepsy; ETLE, extratemporal lobe epilepsy; sGTCSs, secondarily generalized tonic–clonic seizures; CPSs, complex partial seizures; CNS, central nervous system. a Median (IQR).
M. Mercan et al. / Epilepsy & Behavior 44 (2015) 253–257
50% of patients with TLE had no history of sGTCSs, this rate was 17% for patients with ETLE.
3.2. Seizure semiology on video-EEG recording In the video-EEG monitoring data, the CPSs of patients with ETLE turned into sGTCSs with a statistically significantly higher rate compared to patients with TLE (p = 0.006). Nonversive body turning was only observed in CPSs. In addition, NVBT started in the first one-third part of the seizure in 91% (n = 31) of TLE seizures. This rate was 80% (n = 4) in ETLE seizures. Versive body turning was observed right before or during the tonic phase of sGTCSs. Temporal lobe onset CPSs (45% of 76 seizures) had NVBT more frequently than ETLE onset CPSs (14% of 37 seizures), which was found to be statistically significant (p = 0.002). No significant difference between TLE and ETLE seizures was found regarding the VBT frequency (p = 0.456). Additionally, no significant difference between TLE and ETLE seizures was found regarding the NVBT and VBT onsets and durations (p N 0.05) (Table 2). Nonversive body turning was observed in 6% (n = 11) of patients with TLE and 2% (n = 2) of patients with ETLE. In 76% (n = 26) of the seizures with NVBT in patients with TLE, the body rotated to the EZ's side. This rate increased to 88% when NVHT was also present with NVBT. In nearly all of the seizures, NVHT and NVBT were to the same side (except in one seizure in which NVHT and NVBT were opposite). A significant correlation between the NVHT and NVBT onsets and durations was found (rho = 0.470, p = 0.016; rho = 0.702, p = 0.000). The NVBT to the EZ's side was 80% (n = 4) in the ETLE seizures, and in only two of the five seizures, both NVHT and NVBT were present together. In 80% of the 15 TLE seizures with greater than 180° NVBT, the body rotated to the EZ's side. Versive body turning was observed in 5% (n = 8) of patients with TLE and 7% (n = 6) of patients with ETLE. In 86% (n = 12) of the seizures, VBT in patients with TLE was to the opposite side of the EZ, whereas this rate was 56% (n = 5) in the ETLE seizures. This rate increased to 92% when VHT was also present with VBT (92% in TLE seizures and 71% in ETLE seizures). Versive body turning greater than 180° occurred only in one seizure. In TLE seizures, a significant correlation was found between the VHT and VBT onsets and durations (rho = 0.826, p = 0.000; rho = 0.683, p = 0.01), whereas in ETLE seizures, the correlation between the VHT and VBT onsets and durations was
Table 2 Video-EEG monitoring data.
Total CPSs Total sGTCSs NVBT VBT NVBT onset (s)a NVBT duration (s)a VBT onset (s)a VBT duration (s)a Interictal EEG Unilateral temporal Unilateral hemispheric Ictal EEG during NVBT Unilateral T or FT Unilateral hemispheric Nonfocal and nonlateralized Postictal EEG Unilateral temporal Unilateral hemispheric
TLE (n = 16)
ETLE (n = 6)
76 27 (36%) 34 (45%) 14 (52%) 10 (0–48) 13 (3–57) 30 (14–150) 9 (4–26) n = 16 12 (75%) 4 (25%) n = 34 20 (59%) 4 (12%) 10 (29%) n = 40 14 (33%) 9 (22%)
37 24 (65%) 5 (14%) 9 (38%) 7 (1–25) 5 (3–23) 28 (17–42) 6 (4–22) n=6 0 6 (100%) n=5 0 2 (40%) 3 (60%) n = 13 0 8 (62%)
p value 0.006 0.002 0.456 0.817 0.178 0.777 0.590
TLE, temporal lobe epilepsy; ETLE, extratemporal lobe epilepsy; sGTCSs, secondarily generalized tonic–clonic seizures; CPSs, complex partial seizures; NVBT, nonversive body turning; VBT, versive body turning; T, temporal; FT, frontotemporal. Significance was assigned for all tests at p N 0.05 (bold figures). a Median (IQR).
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not statistically significant (rho = 0.643, p = 0.119; rho = 0.057, p = 0.904). The most common lateralization findings accompanying NVBT in TLE seizures were manual automatism (n = 29; 85%), NVHT (n = 24; 71%), dystonic posture (n = 19; 56%), and postictal nose wiping (n = 4; 12%). Nonversive body turning was the only lateralization sign in 12% (n = 4) of the TLE seizures. In ETLE seizures, the lateralization findings were manual automatism (n = 1) and bilateral dystonic posture (n = 1). Versive head turning was the most common lateralization finding and was observed in the sGTCSs of patients with TLE and ETLE (93% and 78%, respectively). Asymmetric clonic ending was the second most common lateralization finding in sGTCSs with ictal body turning (TLE, 36%; ETLE, 44%), and it was always on the same side with the EZ. Lateralization signs of TLE and ETLE seizures were shown in Table 3. 3.3. EEG, imaging findings, and surgery outcomes During NVBT, rhythmical activity between 5 and 12 Hz was observed in the ictal EEG. This activity was localized in the unilateral temporal and frontotemporal regions in 59% of the TLE seizures and was lateralized to the unilateral hemisphere in 40% of the ETLE seizures (Table 2). Fifty-six percent of the patients with TLE had mesial temporal sclerosis (MTS), consistent with the MRI results (two patients' pathology results indicated MTS), and ipsilateral anterior temporal hypometabolism was the most frequent finding in 18F-FDG PET. However, in almost all other etiologic cases, except for MTS, the lesion was located in the parahippocampal region in the anterior temporal lobe. In patients with ETLE, multilobar abnormalities (e.g., frontotemporal cystic lesion and occipitoparietal DNET) were more frequently observed. It was revealed with fMRI that one patient with TLE with right NVBT had a right hemisphere dominance for language. Three patients underwent lesionectomies, and four underwent anterior temporal lobectomies (ATL); in 66% of the patients, the surgical outcome was consistent with Engel 1 (Table 4). One patient who underwent ATL was lost in follow-up. 4. Discussion In our study, ictal body turning was present in patients with both TLE and ETLE. Nonversive body turning was seen only during CPSs; however, VBT was observed right before or during the tonic phase of sGTCSs. Our study revealed that NVBT and VBT are reliable lateralization findings in TLE seizures. During most of the seizures, NVBT was ipsilateral to the EZ whereas VBT was contralateral. Moreover, NVBT was more reliable in EZ lateralization when accompanied with NVHT. A similar Table 3 Lateralization findings in complex partial seizures and secondarily generalized tonic– clonic seizures with ictal body turning. Lateralization findings
Nonversive body turning Versive body turning Nonversive head turning Versive head turning Unilateral manual automatisms Unilateral dystonic posturing Nose wiping Asymmetric ending of clonic jerks Figure-of-4 sign
Number of TLE seizures (n = 48)
Number of ETLE seizures (n = 14)
Ipsilateral
Contralateral
Ipsilateral
Contralateral
26 2 21 0 25
8 12 3 13 4
4 4 1 2 1
1 5 1 5 0
1
18
0
0
3 5
1 0
0 4
0 0
0
3
1
2
TLE, temporal lobe epilepsy; ETLE, extratemporal lobe epilepsy.
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Table 4 Diagnostic information. TLE (n = 16)
ETLE (n = 6)
MRI diagnosis Mesial temporal sclerosis Neuronal migration defect Tumor Vascular pathology Encephalomalacia Dual pathology Normal
9 (56%) 1 (6%) 3 (19%) 1 (6%) 0 1 (6%) 1 (6%)
0 2 (33%) 2 (33%) 0 1 (17%) 0 1 (17%)
MRS (n = 13) Lateralization Normal
9 (70%) 4 (30%)
Perfusion MRI (n = 9) Lateralization Normal
7 (77%) 2 (13%)
PET Ipsilateral AT hypometabolism Multilobar hypometabolism Normal
12 (80%) 3 (20%) 0
Functional MRI (n = 10) Left dominant hemisphere Right dominant hemisphere
9 (90%) 1 (10%)
Histopathological findings (n = 7) Hippocampal sclerosis Dysplasia Tumor Vascular pathology
3 (43%) 1 (14%) 2 (29%) 1 (14%)
Surgical outcomes (n = 6) Engel I Engel II Engel III Engel IV
4 (66%) 1 (17%) 1 (17%) 0
1 (25%) 3 (75%) 0
MRI, magnetic resonance imaging; MRS, magnetic resonance spectroscopy; PET, perfusion emission tomography; and AT; anterior temporal.
situation was found for VBT in TLE seizures. According to our results, NVBT on its own is a reliable lateralization finding in ETLE seizures whereas VBT is not. This may be caused by the lower number of ETLE seizures or rapid spreading of seizure activity over both hemispheres in ETLE seizures. Data on turning during seizures are mostly based on patient statements and are defined in primarily generalized epilepsies and focal epilepsies caused by brain tumors, Wilson's disease, or tuberous sclerosis [6,7,9,19,20]. There are only a few studies conducted using video-EEG monitoring. It was stated in a study with patients with epilepsy who had 180° and greater amounts of body turning during seizures that ictal body turning was frequently present in frontal lobe epilepsies (17%) and rarely occurs in temporal lobe epilepsies (2%). It was also stated in the same study that if VHT was present before body turning, the EZ was contralateral to the body's rotation side, and if body turning did not have VHT, then it was ipsilateral to the body's rotation side [3]. A study on patients who exhibited trunk rotation of over 90° and longer than 10 s revealed that the EZ was 92% contralateral to the rotation side [4]. There is a study claiming that ictal body turning may be present in mesial frontal lobe epilepsy [5]. However, these studies used different turning definitions and are not entirely clear about the turning characteristics. Therefore, to identify ictal body turning, we recommended two definitions as NBVT and VBT according to the clinical characteristics of body movement. In the literature, NVHT was present in 70% of TLE seizures, with 87–94% being to the same side as the EZ. Nonversive head turning was usually present with dystonic extremity posture (71–96%), and it was noted that these two phenomena's pathophysiologic mechanisms may be related [11–13]. A few ictal SPECT studies indicated that during unilateral dystonia, there was hyperperfusion in the striatum and
dorsolateral thalamus ipsilateral to the EZ [21–23]. Interictal PET studies indicated that dystonic posture is related with striatal hypometabolism [24,25]. All of these studies indicate that NVHT and unilateral dystonia are associated with basal ganglia involvement. In our study, NVBT was frequently accompanied with NVHT and/or unilateral dystonia. Furthermore, a high correlation between the NVBT and NVHT characteristics was present in TLE seizures. As a result, our study suggests that TLE seizure ictal spread patterns during head and body turning may be similar. The cause of turning during seizures is not entirely understood, but there are a few hypotheses. One hypothesis suggests that the turning is due to imbalance in the striatum; imbalance in striatal dopamine due to activation in the nucleus accumbens may lead to postural asymmetry determining the rotation side. Neurochemistry studies in rats indicated that an asymmetrical increase in striatal dopamine metabolism leads to contralateral turning [26–28]. Löscher et al. state that turning is related to the decrease in ipsilateral dopamine metabolism [29]. It is also known that changes in cortical epileptiform activity or turning movements may occur with caudate nucleus stimulation [30,31]. It is claimed that in TLE seizures, when epileptic activity is spreading from the mesial structure to other zones in the hemisphere, 2- to 10-Hz frequency activity is observed in the basal ganglia, and thus, the basal ganglia prevent the spread of ictal activity to other zones in the hemisphere [32,33]. Feddersen et al. reported that unilateral dystonic posture prevents the generalization of the seizure in focal epilepsies [34]. The possible antiepileptic activity of the striatum is considered to be due to the substantia nigra pars reticulata's GABAergic modulation [35]. Jung et al. demonstrated in patients with mesial temporal lobe epilepsy that after seizure onset, a strong rhythmic 6- to 10-Hz theta to alpha activity in the ipsilateral medial temporal region was observed at the same time as a dipole cluster of the basal ganglia [36]. As a result, one may assume that altered basal ganglia activity results in turning movement during a seizure. Dystonic posture or excessive immobility in the contralateral extremity and a comparative movement increase in ipsilateral extremity (head, hand, and trunk) may lead to turning movement. In our study, we observed 5to 12-Hz rhythmic EEG activation and contralateral extremity dystonia accompanying NVHT during NVBT which support the relationship of NVBT with the activity in the basal ganglia. Versive head turning that is present in 35–45% of TLE and ETLE seizures and before sGTCSs is counted as a highly reliable lateralization finding (over 90% being contralateral to the EZ) [11,14,37]. Studies indicated that stimulation of the cortical eye field leads to contralateral head version in 58% of patients [38]; SPECT studies also support this view [23, 39]. In our study, VHT and VBT were present together in almost all of the TLE seizures and were significantly correlated. This finding supports the view that VBT occurs due to frontal eye field spreading to neighboring areas, such as VHT in TLE seizures. The reason why this correlation is not present in ELTE seizures may be the lower number of seizures, the zones being multifocal, or the differences in the ictal spread patterns. There are some limitations in our study. The lower number of ETLE seizures may affect the generalizability of the results. In addition, there is a lack of measurement tools for the calculation of the degree of body and head turnings (such as video-based software). Of the 22 patients, there were only six who underwent epilepsy surgery, and most of the patients were lost during follow-up, which makes the interpretation of the data more difficult regarding the identification of the epileptogenic zone. In conclusion, NVBT ipsilateral to the EZ and VBT contralateral to the EZ are valuable lateralization findings in TLE and ETLE seizures. When present with head turning, NVBT ipsilateral to the EZ and VBT contralateral to the EZ are more valuable for lateralization. In TLE seizures, both versive body turning and nonversive body turning are probably caused by two different pathophysiological mechanisms similarly to head turning. Whereas NVBT is more related with basal ganglia involvement, VBT seems to be related with cortical area spreading. Although a valuable lateralization finding, further studies are required to understand the pathophysiology of ictal body turning.
M. Mercan et al. / Epilepsy & Behavior 44 (2015) 253–257
Acknowledgments This study was not supported by government agencies or private foundations. Disclosure of conflicts of interest None of the authors has any conflicts of interest to disclose. We confirm that we have read the journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.
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