Ictal Bruxism - A Sign of Temporal Lobe Ictal Localization: A Case Series

Abstract

Ictal bruxism (IB) is a rare oro-alimentary automatism in focal seizures. We report a series of six patients with IB in drug-resistant temporal lobe epilepsy (TLE) treated subsequently with temporal lobectomy. All patients had ictal teeth grinding with semiological features, suggestive of temporal lobe origin. Ictal electroencephalogram (EEG) onset showed artifacts corresponding to bruxism; one patient had a “checkerboard” pattern of EEG artifacts corresponding with lateral jaw movements. Five patients had a lesion in the mesial temporal lobe, while one patient had a neocortical temporal lobe lesion. Right temporal localization was observed in five, while one patient had left temporal localization. At the latest post-surgery follow-up of 3 to 14 years (mean 8.83 ± 3.53 years), all patients were seizure-free. IB is an under-recognized ictal phenomenon of TLE representing oro-mandibular automatisms involving the limbic networks. It is a sign of ictal localization to the temporal lobe but not a lateralizing sign.

Introduction

Temporal lobe epilepsy (TLE) is the most frequent type of focal epilepsy, and nearly two-thirds of these patients undergo surgery for drug-resistant epilepsy.[1] Oro-alimentary and manual automatisms are common and characteristics of TLE.[2] Bruxism is one of the rare oro-alimentary automatisms involving repetitive grinding or clenching of teeth.

Rhythmic teeth grinding induced by temporal lobe seizures was first reported by Meletti et al. in an adult patient with left hippocampal sclerosis in 2004.[3] Unlike sleep bruxism, ictal bruxism (IB) is associated with typical ictal electroencephalogram (EEG) patterns. Existing literature is limited to individual case studies classically localizing this phenomenon to temporal lobe seizures of either side.[4,5,6] We report the clinical, EEG, and imaging characteristics of six patients with drug-resistant TLE and IB treated with temporal lobectomy, who had remission or resolution of epilepsy.

Case Series

We screened Video EEG (VEEG) data of 1156 patients from 2003 to 2021. The inclusion criteria was patients with IB who underwent surgery irrespective of the post-surgery outcome. Six patients had drug-resistant TLE and IB and underwent temporal lobectomy; all were males. Clinical characteristics and semiology details were given in Table 1. IB was noted in all recorded seizures in three patients and in nearly 70% of seizures among the rest [Video 1]. Ictal EEG showed artifacts corresponding to bruxism intermixed with ictal rhythm in all patients [Figures 1 and 2]. Case 6 had a typical “checkerboard” pattern of EEG artifacts [Figure 3], corresponding with IB. Four cases had IB early (<10 s after the clinical onset of seizures), and two had later (>20 s after onset) [Table 1]. Case 2 had biphasic occurrence of IB early in the course of seizure followed by remission and re-occurrence late in the seizure. The duration of IB varied from 40% to almost the entire duration of seizures and occurred both during sleep and in the awake state. Five patients had mesial temporal involvement on Magnetic Resonance Imaging (MRI) brain [Table 2, Figure 4]. One patient (Case 3) had an aura of elementary auditory hallucinations followed by temporal semiology, suggestive of neocortical temporal lobe involvement at ictal onset; his MRI brain showed right lateral temporal focal cortical dysplasia (FCD), and histopathology was suggestive of FCD type 1b. Right temporal localization was observed in five patients, while one patient had left temporal localization. The surgery and post-surgery details were shown in Table 2. At the latest post-surgery follow-up of 3 to 14 years (mean 8.83 ± 3.53 years), all patients were seizure-free. Two patients had resolution of epilepsy, while four patients were seizure-free on antiseizure medication.

Table 1.

Clinical characteristics of patients with ictal bruxism

Patient	Age at evaluation, sex	Age of onset of epilepsy	Seizure type	Aura	Semiology	Baseline frequency	Frequency of BTCS
1	30, M	10	Focal motor onset with impaired awareness	None	Behavior arrest, bipedal automatisms	1–2/week	Rare
2	35, M	15	Focal motor onset with impaired awareness	None	Behavior arrest, OAA	3–4/week	1–2/year
3	30, M	23	Focal motor onset with preserved awareness	Elementary auditory hallucinations (rhythmic melody)	Behavior arrest, left UL dystonia followed by RINCH, right UL automatisms, with PPA	3–4/month	1–3/year
4	28, M	11	Focal motor onset with impaired awareness	None	Behavioral arrest, ictal vomiting	3–4/month with clustering	Rare
5	30, M	9	Focal motor onset with impaired awareness	Anxiety, palpitations	Behavioral arrest, OAA, right UL automatisms, late leaving behavior	3–4/week	Rare
6	49, M	6	Focal motor onset with impaired awareness	Epigastric discomfort	Behavioral arrest, OAA and right UL automatism	4–5/month	Never

BTCS: Bilateral tonic-clonic seizure; OAA: Oro alimentary automatism; PPA: Partially preserved awareness; RINCH: Rhythmic ictal nonclonic hand; M: Male, UL: Upper limb

Figure 1.

(a and b) Ictal EEG showing right anterior and mid-temporal rhythmic theta activity at ictal onset, later obscured by teeth grinding artifacts (arrows, Case 5). EEG: Electroencephalogram

Figure 2.

(a and b) Ictal EEG showing left frontal and anterior and mid-temporal rhythmic theta activity at ictal onset, later obscured by teeth grinding artifacts (arrows, Case 1). EEG: Electroencephalogram

Figure 3.

(a-d) Ictal EEG showing a “checkerboard” pattern during teeth grinding with continuous EMG activity in the bilateral masseter muscles and right temporal ictal EEG onset (arrows), (Case 6). EEG: Electroencephalogram, EMG: Electromyography

Table 2.

Inter-ictal, ictal EEG, MRI characteristics, and post-surgery outcome data of patients with ictal bruxism

Case	No. of seizures with IB/Total recorded seizures	Average seizure duration (s) Mean ± SD	Time of occurrence of bruxism	Average duration of teeth grinding (s) Mean ± SD	State during Seizures (Awake/Sleep)	Inter-ictal EEG spikes	Ictal EEG onset	MRI brain	Surgery	Histopathology	Acute post-operative seizures	Duration of FU (years)	Outcome at latest FU	Number of ASM at latest FU
1	4/4	116±17	Almost throughout	72±5	2/2	Left temporal	Left anterior and mid-temporal	Left HS with left temporo polar FCD	ATL with AH	FCD type IIIA	No	14	Seizure-free (had seizures on ASMW)	2
2	6/6	155±36	Biphasic	64±16	5/1	Right temporal	Right anterior and mid-temporal	Right HS	ATL with AH	FCD type IIIA	No	9	Seizure-free (had seizures on ASMW)	2
3	4/5	86±24	Mid to late	52±10	5/0	Right temporal and frontal	Right anterior temporal and frontal	Right lateral temporal (MTG) FCD	Lesionectomy	FCD type 1b	No	11	Seizure-free	none
4	2/2	100±5	Early to mid	27±4	2/0	Right temporal	Right anterior and mid-temporal	Right HS	ATL with AH	HS type I	No	10	Seizure-free	none
5	5/7	110±7	Early to mid	38±6	3/4	Right temporal	Right anterior and mid-temporal	Right temporal focal calcification	Lesionectomy	Calcification	No	6	Seizure-free	1 (not willing for ASMW)
6	4/5	93±13	Mid to late	43±7	5/0	Right temporal	Right anterior and mid-temporal	Right mesial temporal cavernoma involving hippocampus	ATL with AH	Cavernoma	No	3	Seizure free (had auras on ASMW)	1

ATL AH: Amygdalo hippocampectomy with anterior temporal lobectomy, ASM: Antiseizure medication, ASMW: Antiseizure medication withdrawal, EEG: Electroencephalogram, FCD: Focal cortical dysplasia, FU: Follow-up, HS: Hippocampal sclerosis, IB: Ictal bruxism, MRI: Magnetic resonance imaging, MTG: Middle temporal gyrus, SD: Standard deviation

Figure 4.

MRI brain in patients with ictal bruxism. Case 1: Left temporopolar focal cortical dysplasia (a). Case 2: Right hippocampal sclerosis (b). Case 3: Right lateral temporal focal cortical dysplasia (c) Case 4: Right hippocampal sclerosis (d) Case 5: Right temporal focal calcification (e). Case 6: Right mesial temporal cavernoma (f) (white arrows). MRI: Magnetic resonance imaging

Discussion

Bruxism as a constant and main manifestation of an epileptic seizure is a rare phenomenon. It is presumed to be part of oro-alimentary automatisms involving the limbic system.[3,5] In the current series, all except one patient had right temporal localization. Interestingly, IB has been reported from both right[4,5,6] and left[3] temporal lobe origins, similar to the present report. Five patients had a lesion in the mesial temporal lobe, while one patient had a neocortical temporal lobe lesion in the present case series. These findings suggest that IB is characteristically a phenomenon of TLE rather than representative of any particular pathology or lateralization. Coincidentally, all historical reports and our case series have shown IB in male patients. IB being a rare clinical phenomenon, this observation needs further validation.

Teeth grinding as a sleep-related phenomenon or as an ictal behavior has been described to result from activation of motor trigeminal neurons or from central pattern generator interneurons.[7] Primary sleep-related bruxism (SRB) may result from abnormal activation of the ascending reticular activating system stimulating the masticatory neurons. However, IB is likely a limbic release phenomenon due to loss of inhibitory frontal or cingulate neocortical networks.[7] IB can sometimes be mistaken as SRB, as the latter is a more common phenomena. Clinically, IB can occur in sleep as well as in the awake state, usually associated with open eyes and accompanied by other semiological features of TLE. The duration of episodes is longer in IB and has sparse episodes in one night compared to SRB. SRB is common in children and rare in adults.[4,5]

The ictal EEG shows characteristic muscle artifacts during bruxism intermixed with rhythmic seizure activity. Sometimes, a distinctive “checkerboard” pattern can be noted. This pattern of artifacts in EEG is produced by rhythmic lateral movements of the jaw.[8] The checkerboard pattern on EEG was described by Hirsch and Crispin in a case of SRB.[9] We report, for the first time, the occurrence of the checkerboard pattern in IB in the present case series.

Conclusions

IB is an under-recognized ictal phenomenon characteristically localizing to TLE, representing oro-mandibular automatisms involving limbic networks. It can occur in both mesial and lateral temporal epilepsy.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and that due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Conflicts of interest

There are no conflicts of interest.

Funding Statement

Nil.