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Ictal bruxism treated with temporal lobectomy
Sleep Medicine 16 (2015) 1429–1431
Contents lists available at ScienceDirect
Sleep Medicine j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / s l e e p
Video-Clinical Corners
Ictal bruxism treated with temporal lobectomy Marc Guaita a,b, Cecile van Eendenburg c, Antonio Donaire b,d,e, Javier Aparicio b,d,e, Xavier Setoain b,d,f, Núria Bargalló b,d,g, Jordi Rumià d,h, Albert Molins c, Mar Carreño b,d,e,* a
Multidisciplinary Sleep Disorders Unit, Department of Neurology, Hospital Clinic, Villarroel 170, Barcelona, Spain Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain Department of Neurology, Hospital Universitari Dr. Josep Trueta, Carretera de Francia s/n, Girona, Spain d Epilepsy Unit, Department of Neurology, Hospital Clinic, Villarroel 170, Barcelona, Spain e Department of Neurology, Hospital Clinic, Villarroel 170, Barcelona, Spain f Department of Nuclear Medicine, Hospital Clinic, Villarroel 170, Barcelona, Spain g Department of Radiology, Hospital Clinic, Villarroel 170, Barcelona, Spain h Department of Neurosurgery, Hospital Clinic, Villarroel 170, Barcelona, Spain b c
A R T I C L E
I N F O
Article history: Received 9 February 2015 Received in revised form 24 April 2015 Accepted 29 May 2015 Available online 6 August 2015 Keywords: Teeth grinding Epilepsy Sleep bruxism Oromandibular automatism
1. Introduction Teeth grinding (TG) is the main sign of sleep bruxism (SB) [1,2], although occasionally it may be seen as a rhythmic motor event (automatism) during epileptic seizures [3]. We report a patient with drug-resistant right temporal lobe epilepsy with prominent TG during his seizures, which occurred mainly during sleep but occasionally also during wakefulness. After presurgical evaluation, the patient underwent right anterior mesial temporal resection, which has rendered him free of seizures and TG episodes, as shown by polysomnography (PSG). The case illustrates the unusual occurrence of TG associated with epileptic seizures. 2. Case description The patient is a 37-year-old, right-handed man with a history of repeated febrile seizures from the age of three months. He later developed drug-resistant epilepsy with seizures occurring mainly during sleep; these consisted of prominent episodes of TG associated with loss of awareness, followed by disorganized movements
* Corresponding author. Epilepsy Unit, Department of Neurology, Hospital Clinic, C/ Villarroel 170, 08036 Barcelona, Spain. Tel.: +34 932275414; fax: +34 932275783. E-mail address: [email protected] (M. Carreño). http://dx.doi.org/10.1016/j.sleep.2015.05.024 1389-9457/© 2015 Elsevier B.V. All rights reserved.
of the arms and legs and occasional secondary generalization. Seizures during wakefulness were preceded by an epigastric aura. Seizure frequency when he was seen at our unit was two to three seizures per month. Physical examination revealed severe tooth wear accompanied by cheek bitings, which were treated with an occlusal splint. A presurgical evaluation was performed during one week of hospitalization and included continuous video electroencephalography (EEG) monitoring, 3T magnetic resonance imaging (MRI), interictal and ictal single photon emission computed tomography (SPECT), and positron emission tomography (PET) with 18fluorodeoxyglucose. Interictal EEG showed continuous slowing and sharp waves over the anterior part of the right temporal lobe, whereas ictal EEG showed rhythmic theta (θ) at the right anterior temporal electrodes (maximal at F8-T8) (Fig. 1A,B), very early obscured by the muscle artifact produced by movement and TG. 3T brain MRI showed blurring of the gray–white matter junction in the right temporal pole without obvious alterations in size or signal of the hippocampus. No alterations in cerebral perfusion were seen in the interictal SPECT; however, ictal SPECT showed a marked increase in perfusion in the anterior and lateral parts of the right temporal lobe, which was confirmed by subtraction ictal SPECT coregistered with MRI (SISCOM) (Fig. 1C). Brain PET showed a concordant region of hypometabolism in the pole and lateral cortex of the right temporal lobe (Fig. 1C).
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M. Guaita et al./Sleep Medicine 16 (2015) 1429–1431
Fig. 1. (A and B) Interictal and ictal electroencephalography (EEG) recordings during sleep. A longitudinal “double banana” montage shows an interictal EEG with continuous slowing and sharp waves over the anterior part of the right temporal lobe (*), whereas ictal EEG shows a rhythmic theta (θ) at the same region. Both recordings were captured during stage N2 sleep. The EEG trace is shown at an amplification of 5 μV/mm. (C) Neuroimaging. On top, coronal subtraction ictal single photon emission computed tomography coregistered with magnetic resonance imaging, showing ictal hyperperfusion in the right temporal lobe, maximal at the pole. On the bottom, coronal positron emission tomogram showing hypometabolism in the right temporal lobe, mainly at the pole and over the mesial structures.
The patient underwent right anterior temporal resection in 2010, and pathology confirmed mesial temporal sclerosis. He has had no more seizures since surgery. An antiepileptic drug regimen has been progressively simplified, and he is now on oxcarbazepine 900 mg per day. Teeth grinding episodes have also disappeared during both sleep and wakefulness, according to his wife. In 2014, nocturnal PSG performed with an expanded EEG montage and surface electromyography (EMG) of masticatory muscles demonstrated occasional bursts of right fronto-temporal epileptiform activity that were not associated with any clinical manifestations. A total of 51 isolated jaw jerks occurred during nonrapid eye movement sleep but were not preceded by any epileptiform activity. Teeth grinding was not seen during the PSG study.
they were associated with rhythmic right temporal discharges and disappeared when the seizures were controlled after surgery. Moreover, they were accompanied by limb automatisms, and occurred during both sleep and awake seizures [3]. Other differences with idiopathic SB are the number of TG episodes per night (one episode vs repetitive TG episodes), the duration of the episode, which lasted much longer than in SB (50 seconds vs 9 seconds), and maybe the presence of eyes open during the motor event [2,4]. In our patient, assessment of heart rate was not possible because of the movement artifact, so we have not been able to confirm the increased heart rate associated with TG that has been observed by other authors [3,5,6]. Table 1 summarizes the key factors for differentiating ictal from primary sleep bruxism.
3. Video analysis The video shows one seizure occurring during sleep (Video S1). The patient woke up from stage N2 sleep with disorganized movements of the arms, trunk, and legs, and 13 seconds later he displayed severe TG (see the muscular artifacts related to movements and TG superimposed on EEG traces in Fig. 2). The episode lasted 50 seconds and consisted of 53 EMG bursts firing at a frequency of 1.06 Hz, with visible jaw lateral movements. During the episode, he had his eyes open and the automatisms in his arms and legs continued. Then, TG stopped and the patient had head and eye deviation to the left, followed by tonic contraction of the left hemiface and generalized clonic jerks. 4. Discussion In this report, we highlight the uncommon ictal origin of episodes of TG in a patient with drug-resistant right temporal lobe epilepsy. These episodes seem to represent a special type of epilepsyrelated oromandibular automatism more than a benign SB because
Table 1 Comparison between ictal bruxism and primary sleep bruxism.
Etiology Clinical presentation
Characteristics of TG episodes No. of episodes Episode duration (s) Number of bursts per episode Increased heart rate Management
Ictal bruxisma (Ref. [3])
Primary sleep bruxism (Ref. [4])
Temporal epileptic discharges Wakefulness and sleep TG accompanied by limb automatisms
Micro-arousals
1/night 50a/47.6 ± 9.1 (Ref. [3]) 53a/60.7 ± 15.3 (Ref. [3])
5.8/h 9.4 ± 0.7 8.3 ± 0.6
Yes (Ref. [3]) Antiepileptic drugs ± surgery
Yes Occlusal splint
Sleep TG accompanying body movements
Ictal bruxism is described based on two different patients with drug-resistant temporal lobe epilepsy: the patient in this study and the patient described by Meletti et al. [3]. Ref., reference; TG, teeth grinding. a The patient in this study.
M. Guaita et al./Sleep Medicine 16 (2015) 1429–1431
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Fig. 2. Epileptic seizure occurring during sleep. This epoch of two minutes represents the polygraphic recording of the seizure shown in the video. Note the muscular artifacts related to movements and teeth grinding activity that are superimposed on electroencephalographic traces. The EEG traces have been modified to emphasized teeth grinding EMG activity, using amplification at 75 μV/mm, low-frequency filter at 16 Hz and high-frequency filter at 70 Hz, and referring each EEG channel to both ears (ref = TP9 + TP10).
In accordance with Meletti et al., who reported the occurrence of ictal TG in another patient with left temporal lobe epilepsy [3], we confirm that rhythmic jaw muscle activity of TG can be set in motion by sleep-related mechanisms [5] or pathological conditions such as epileptic seizures. Independently from the nature of the trigger, some authors have suggested that the activation of the same motor trigeminal neurons or interneurons of the central pattern generator (CPG) network underlies the common motor and autonomic phenomena. Although in idiopathic SB an abnormal stimulation of the ascending reticular activating system may be involved in the activation of the masticatory CPG [5–7], in limbic seizures this could be due to a “release” mechanism produced by functional inactivation of inhibitory neocortical areas such as the frontobasal and cingulated regions [8].
Conflict of interest The ICMJE Uniform Disclosure Form for Potential Conflicts of Interest associated with this article can be viewed by clicking on the following link: http://dx.doi.org/10.1016/j.sleep.2015.05.024.
Appendix: Supplementary material Supplementary data to this article can be found online at doi:10.1016/j.sleep.2015.05.024. References [1] American Academy of Sleep Medicine. International classification of sleep disorders. 3rd ed. Darien, IL: American Academy of Sleep Medicine; 2014. [2] Lavigne GJ, Rompré PH, Montplaisir JY. Sleep bruxism: validity of clinical research diagnostic criteria in a controlled polysomnographic study. J Dent Res 1996;75:546–52. [3] Meletti S, Cantalupo G, Volpi L, et al. Rhythmic teeth grinding induced by temporal lobe seizures. Neurology 2004;62:2306–9. [4] Lavigne GJ, Rompre PH, Poirier G, et al. Rhythmic masticatory muscle activity during sleep in humans. J Dent Res 2001;80:443–8. [5] Lavigne GJ, Huynh N, Kato T, et al. Genesis of sleep bruxism: motor and autonomic-cardiac interactions. Arch Oral Biol 2007;52:381–4. [6] Kato T, Montplaisir JY, Guitard F, et al. Evidence that experimentally induced sleep bruxism is a consequence of transient arousal. J Dent Res 2003;82:284–8. [7] Macaluso GM, Guerra P, Di Giovanni G, et al. Sleep bruxism is a disorder related to periodic arousals during sleep. J Dent Res 1998;77:565–73. [8] Tassinari CA, Rubboli G, Gardella E, et al. Central pattern generators for a common semiology in fronto-limbic seizures and in parasomnias. A neuroethologic approach. Neurol Sci 2005;26:s225–32.
Contents lists available at ScienceDirect
Sleep Medicine j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / s l e e p
Video-Clinical Corners
Ictal bruxism treated with temporal lobectomy Marc Guaita a,b, Cecile van Eendenburg c, Antonio Donaire b,d,e, Javier Aparicio b,d,e, Xavier Setoain b,d,f, Núria Bargalló b,d,g, Jordi Rumià d,h, Albert Molins c, Mar Carreño b,d,e,* a
Multidisciplinary Sleep Disorders Unit, Department of Neurology, Hospital Clinic, Villarroel 170, Barcelona, Spain Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain Department of Neurology, Hospital Universitari Dr. Josep Trueta, Carretera de Francia s/n, Girona, Spain d Epilepsy Unit, Department of Neurology, Hospital Clinic, Villarroel 170, Barcelona, Spain e Department of Neurology, Hospital Clinic, Villarroel 170, Barcelona, Spain f Department of Nuclear Medicine, Hospital Clinic, Villarroel 170, Barcelona, Spain g Department of Radiology, Hospital Clinic, Villarroel 170, Barcelona, Spain h Department of Neurosurgery, Hospital Clinic, Villarroel 170, Barcelona, Spain b c
A R T I C L E
I N F O
Article history: Received 9 February 2015 Received in revised form 24 April 2015 Accepted 29 May 2015 Available online 6 August 2015 Keywords: Teeth grinding Epilepsy Sleep bruxism Oromandibular automatism
1. Introduction Teeth grinding (TG) is the main sign of sleep bruxism (SB) [1,2], although occasionally it may be seen as a rhythmic motor event (automatism) during epileptic seizures [3]. We report a patient with drug-resistant right temporal lobe epilepsy with prominent TG during his seizures, which occurred mainly during sleep but occasionally also during wakefulness. After presurgical evaluation, the patient underwent right anterior mesial temporal resection, which has rendered him free of seizures and TG episodes, as shown by polysomnography (PSG). The case illustrates the unusual occurrence of TG associated with epileptic seizures. 2. Case description The patient is a 37-year-old, right-handed man with a history of repeated febrile seizures from the age of three months. He later developed drug-resistant epilepsy with seizures occurring mainly during sleep; these consisted of prominent episodes of TG associated with loss of awareness, followed by disorganized movements
* Corresponding author. Epilepsy Unit, Department of Neurology, Hospital Clinic, C/ Villarroel 170, 08036 Barcelona, Spain. Tel.: +34 932275414; fax: +34 932275783. E-mail address: [email protected] (M. Carreño). http://dx.doi.org/10.1016/j.sleep.2015.05.024 1389-9457/© 2015 Elsevier B.V. All rights reserved.
of the arms and legs and occasional secondary generalization. Seizures during wakefulness were preceded by an epigastric aura. Seizure frequency when he was seen at our unit was two to three seizures per month. Physical examination revealed severe tooth wear accompanied by cheek bitings, which were treated with an occlusal splint. A presurgical evaluation was performed during one week of hospitalization and included continuous video electroencephalography (EEG) monitoring, 3T magnetic resonance imaging (MRI), interictal and ictal single photon emission computed tomography (SPECT), and positron emission tomography (PET) with 18fluorodeoxyglucose. Interictal EEG showed continuous slowing and sharp waves over the anterior part of the right temporal lobe, whereas ictal EEG showed rhythmic theta (θ) at the right anterior temporal electrodes (maximal at F8-T8) (Fig. 1A,B), very early obscured by the muscle artifact produced by movement and TG. 3T brain MRI showed blurring of the gray–white matter junction in the right temporal pole without obvious alterations in size or signal of the hippocampus. No alterations in cerebral perfusion were seen in the interictal SPECT; however, ictal SPECT showed a marked increase in perfusion in the anterior and lateral parts of the right temporal lobe, which was confirmed by subtraction ictal SPECT coregistered with MRI (SISCOM) (Fig. 1C). Brain PET showed a concordant region of hypometabolism in the pole and lateral cortex of the right temporal lobe (Fig. 1C).
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Fig. 1. (A and B) Interictal and ictal electroencephalography (EEG) recordings during sleep. A longitudinal “double banana” montage shows an interictal EEG with continuous slowing and sharp waves over the anterior part of the right temporal lobe (*), whereas ictal EEG shows a rhythmic theta (θ) at the same region. Both recordings were captured during stage N2 sleep. The EEG trace is shown at an amplification of 5 μV/mm. (C) Neuroimaging. On top, coronal subtraction ictal single photon emission computed tomography coregistered with magnetic resonance imaging, showing ictal hyperperfusion in the right temporal lobe, maximal at the pole. On the bottom, coronal positron emission tomogram showing hypometabolism in the right temporal lobe, mainly at the pole and over the mesial structures.
The patient underwent right anterior temporal resection in 2010, and pathology confirmed mesial temporal sclerosis. He has had no more seizures since surgery. An antiepileptic drug regimen has been progressively simplified, and he is now on oxcarbazepine 900 mg per day. Teeth grinding episodes have also disappeared during both sleep and wakefulness, according to his wife. In 2014, nocturnal PSG performed with an expanded EEG montage and surface electromyography (EMG) of masticatory muscles demonstrated occasional bursts of right fronto-temporal epileptiform activity that were not associated with any clinical manifestations. A total of 51 isolated jaw jerks occurred during nonrapid eye movement sleep but were not preceded by any epileptiform activity. Teeth grinding was not seen during the PSG study.
they were associated with rhythmic right temporal discharges and disappeared when the seizures were controlled after surgery. Moreover, they were accompanied by limb automatisms, and occurred during both sleep and awake seizures [3]. Other differences with idiopathic SB are the number of TG episodes per night (one episode vs repetitive TG episodes), the duration of the episode, which lasted much longer than in SB (50 seconds vs 9 seconds), and maybe the presence of eyes open during the motor event [2,4]. In our patient, assessment of heart rate was not possible because of the movement artifact, so we have not been able to confirm the increased heart rate associated with TG that has been observed by other authors [3,5,6]. Table 1 summarizes the key factors for differentiating ictal from primary sleep bruxism.
3. Video analysis The video shows one seizure occurring during sleep (Video S1). The patient woke up from stage N2 sleep with disorganized movements of the arms, trunk, and legs, and 13 seconds later he displayed severe TG (see the muscular artifacts related to movements and TG superimposed on EEG traces in Fig. 2). The episode lasted 50 seconds and consisted of 53 EMG bursts firing at a frequency of 1.06 Hz, with visible jaw lateral movements. During the episode, he had his eyes open and the automatisms in his arms and legs continued. Then, TG stopped and the patient had head and eye deviation to the left, followed by tonic contraction of the left hemiface and generalized clonic jerks. 4. Discussion In this report, we highlight the uncommon ictal origin of episodes of TG in a patient with drug-resistant right temporal lobe epilepsy. These episodes seem to represent a special type of epilepsyrelated oromandibular automatism more than a benign SB because
Table 1 Comparison between ictal bruxism and primary sleep bruxism.
Etiology Clinical presentation
Characteristics of TG episodes No. of episodes Episode duration (s) Number of bursts per episode Increased heart rate Management
Ictal bruxisma (Ref. [3])
Primary sleep bruxism (Ref. [4])
Temporal epileptic discharges Wakefulness and sleep TG accompanied by limb automatisms
Micro-arousals
1/night 50a/47.6 ± 9.1 (Ref. [3]) 53a/60.7 ± 15.3 (Ref. [3])
5.8/h 9.4 ± 0.7 8.3 ± 0.6
Yes (Ref. [3]) Antiepileptic drugs ± surgery
Yes Occlusal splint
Sleep TG accompanying body movements
Ictal bruxism is described based on two different patients with drug-resistant temporal lobe epilepsy: the patient in this study and the patient described by Meletti et al. [3]. Ref., reference; TG, teeth grinding. a The patient in this study.
M. Guaita et al./Sleep Medicine 16 (2015) 1429–1431
1431
Fig. 2. Epileptic seizure occurring during sleep. This epoch of two minutes represents the polygraphic recording of the seizure shown in the video. Note the muscular artifacts related to movements and teeth grinding activity that are superimposed on electroencephalographic traces. The EEG traces have been modified to emphasized teeth grinding EMG activity, using amplification at 75 μV/mm, low-frequency filter at 16 Hz and high-frequency filter at 70 Hz, and referring each EEG channel to both ears (ref = TP9 + TP10).
In accordance with Meletti et al., who reported the occurrence of ictal TG in another patient with left temporal lobe epilepsy [3], we confirm that rhythmic jaw muscle activity of TG can be set in motion by sleep-related mechanisms [5] or pathological conditions such as epileptic seizures. Independently from the nature of the trigger, some authors have suggested that the activation of the same motor trigeminal neurons or interneurons of the central pattern generator (CPG) network underlies the common motor and autonomic phenomena. Although in idiopathic SB an abnormal stimulation of the ascending reticular activating system may be involved in the activation of the masticatory CPG [5–7], in limbic seizures this could be due to a “release” mechanism produced by functional inactivation of inhibitory neocortical areas such as the frontobasal and cingulated regions [8].
Conflict of interest The ICMJE Uniform Disclosure Form for Potential Conflicts of Interest associated with this article can be viewed by clicking on the following link: http://dx.doi.org/10.1016/j.sleep.2015.05.024.
Appendix: Supplementary material Supplementary data to this article can be found online at doi:10.1016/j.sleep.2015.05.024. References [1] American Academy of Sleep Medicine. International classification of sleep disorders. 3rd ed. Darien, IL: American Academy of Sleep Medicine; 2014. [2] Lavigne GJ, Rompré PH, Montplaisir JY. Sleep bruxism: validity of clinical research diagnostic criteria in a controlled polysomnographic study. J Dent Res 1996;75:546–52. [3] Meletti S, Cantalupo G, Volpi L, et al. Rhythmic teeth grinding induced by temporal lobe seizures. Neurology 2004;62:2306–9. [4] Lavigne GJ, Rompre PH, Poirier G, et al. Rhythmic masticatory muscle activity during sleep in humans. J Dent Res 2001;80:443–8. [5] Lavigne GJ, Huynh N, Kato T, et al. Genesis of sleep bruxism: motor and autonomic-cardiac interactions. Arch Oral Biol 2007;52:381–4. [6] Kato T, Montplaisir JY, Guitard F, et al. Evidence that experimentally induced sleep bruxism is a consequence of transient arousal. J Dent Res 2003;82:284–8. [7] Macaluso GM, Guerra P, Di Giovanni G, et al. Sleep bruxism is a disorder related to periodic arousals during sleep. J Dent Res 1998;77:565–73. [8] Tassinari CA, Rubboli G, Gardella E, et al. Central pattern generators for a common semiology in fronto-limbic seizures and in parasomnias. A neuroethologic approach. Neurol Sci 2005;26:s225–32.