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Evidence that Experimentally Induced Sleep Bruxism is a Consequence of Transient Arousal
1 Centre d’étude sur le Sommeil et des Rythmes Biologiques, Hôpital du Sacré-Coeur de Montréal; Correspondence: *corresponding author, gilles.lavigne{at}umontreal.ca
Spontaneous rhythmic masticatory muscle activity (RMMA) during sleep occurs more frequently following spontaneous transient micro-arousal in patients with sleep bruxism (SB) and normal controls. Here, we tested the hypothesis that an experimental arousal would be followed by an increase in RMMA. We identified RMMA on polygraphic recordings taken before and after sensory stimulation to induce experimental arousal in eight SB patients and eight matched normal subjects. The rate of experimental arousal and the level of resting electromyographic activity in masseter and suprahyoid muscles during sleep did not differ between the groups. In both, muscle tone and heart rate increased during the experimental arousal. Although post-arousal RMMA occurred in all SB patients, it was seen in only one normal subject. Moreover, tooth-grinding occurred during 71% of the evoked RMMA in SB patients. These results support the hypothesis that SB is an exaggerated form of oromotor activity associated with sleep micro-arousal.
Key Words: sleep bruxism • rhythmic masticatory muscle activity • sleep micro-arousal • sensory stimuli • arousal reactions
Sleep bruxism (SB) is the grinding or clenching of the teeth during sleep. It is reported by 8% of the adult population, and is classified as a parasomnia (Thorpy, 1997; Lavigne and Manzini, 2000; Kato et al., 2001b). Spontaneous rhythmic masticatory muscle activity (RMMA), in the absence of tooth-grinding, is observed in 60% of the normal population; in SB patients, it is found 3 times more frequently (Lavigne et al., 2001). Spontaneous micro-arousals occur about 15 times per hour of sleep in normal young adults (ASDA, 1992; Boselli et al., 1998; Sforza et al., 2000). These are defined as a sudden transient increase in electroencephalographic (EEG) and electromyographic (EMG) activity and in heart rate without full awakening (ASDA, 1992; Roehr et al., 2000). SB has been associated with sleep micro-arousal (Satoh and Harada, 1973; Macaluso et al., 1998; Kato et al., 2001a; Lavigne et al., 2001). Since micro-arousal can be triggered by sensory stimuli without disrupting sleep continuity (Morgan et al., 1996; Monstad and Guilleminault, 1999; Roehr et al., 2000), and based on evidence that tooth-grinding can be triggered by sensory stimulation in SB patients (Satoh and Harada, 1973), we decided to compare responses of SB patients and matched normals to test the following hypotheses: SB patients will (1) have a lower threshold of experimental arousal, (2) show more RMMA during arousal, and (3) have higher resting masticatory EMG levels during sleep.
Subjects Nine SB patients (5 M, 4 F; aged from 21 to 27 yrs old) and 10 normal subjects (5 M and 5 F; aged from 20 to 27 yrs old) were recruited. All gave informed consent. The protocol was reviewed and approved by a hospital research ethics board (Hôpital du Sacré-Coeur). SB patients had a history of tooth-grinding more than three times a week for the preceding 6 mos, orofacial jaw muscle fatigue or tenderness (but no pain) in the morning, tooth wear, and masseter muscle hypertrophy (Thorpy, 1997; Lavigne and Manzini, 2000; Kato et al., 2001b). The diagnosis of SB was confirmed in the sleep laboratory as described below. Normal subjects had none of these clinical findings. None of the participants had a history or showed signs of sleep disorders (e.g., snoring, apnea, periodic limb movement, insomnia) or medical disorders (e.g., psychiatric, neurological, movement disorders), and none was taking any medication. One SB patient and two normal subjects could not sleep well during the experimental night and were therefore excluded from the analysis. The final population was eight SB patients (5 M, 3 F; mean age = 22.8 yrs [range, 21 to 27]) and eight normal subjects (4 M, 4 F; mean age = 23.0 yrs [range, 20 to 26]).
SB Diagnosis and Study Procedures
Experimental Set-up The following measures were recorded on a computer (sampling rate: 200 Hz) equipped with commercial software (HARMONIE, Stellate, Montréal, PQ, Canada): EEG (C3A2, O2A1), electro-oculogram, electrocardiogram (EKG), chest respiratory movements, and EMG activity from the left masseter, suprahyoid, and tibialis muscles. EMG activity of the right masseter and suprahyoid muscles was recorded simultaneously on a second computer at a sampling rate of 1024 Hz for spectral analysis. Audio-video recording was performed for the identification of oromotor activity (Lavigne et al., 1996; Kato et al., 2001b).
Experimental Procedure
Off-line Data Analysis
Analysis of Masticatory Muscle Tone and Cardiac Activities in the Absence of RMMA
Statistics
On the second (baseline) night, SB patients had a mean of 7.1 ± 0.9 spontaneous RMMA episodes per hour of sleep, while normal subjects had 0.4 ± 0.2 episodes. Most sleep variables were no different between the two groups for the second baseline and third experimental nights (Table 1  ). The amount of time spent in sleep stage 2 increased slightly from the baseline to the experimental night (p = 0.024, ANOVA), and decreased in sleep stage 4 (p < 0.001, ANOVA). Seven out of eight SB patients and all normal subjects reported good sleep quality during the experimental night.
Experimental Arousal in Trials In total, 1624 stimuli (827 in SB patients; 797 in normal subjects) were delivered: 727 stimuli were given in sleep stage 2, 355 in stages 3 and 4, and 542 in REM. The number of each stimulus given to each group was similar between VT+AD and AD in each sleep stage (SB patients, 51 ± 1.4 stimuli [VT+AD] and 52 ± 1.4 [AD]; and normals, 50 ± 1.1 [VT+AD] and 50 ± 1.1 [AD]). Experimental arousal occurred with 295 stimuli in SB patients and with 347 in normal subjects. Although there were significant effects for sleep stage, stimulus type, and stimulus intensity (p < 0.001 for all effects, ANOVA), no significant group effects were found for the rate of experimental arousal in any sleep stages (Fig. 1A ). The number of stimuli that participants remembered during sleep was not different between groups (SB patients, 1.6 ± 0.5%; normals, 2.9 ± 0.5%, p > 0.05; t test).
Experimentally Induced RMMA Episodes Thirty-one RMMA episodes occurred following experimental arousal in SB patients (Fig. 1B  ). These occurred in all eight SB patients. One normal subject had 5 episodes; the other had none. Evoked RMMA episodes were 7 times more frequent in SB patients (SB patients, 10.9 ± 1.8%; normals, 1.5 ± 1.5%, p = 0.003, Mann-Whitney test, Fig. 1C). Similarly to Satoh and Harada (1973), the mean latency of RMMA after stimulation was 8.0 ± 0.84 sec (range, 2 to 18). In the SB patients, 27 experimentally induced RMMA episodes (87%) occurred during sleep stage 2, 3 episodes (9.7%) in stages 3 and 4, and 2 (6.5%) in REM. In the normal subject, four episodes were in stage 2 and one in REM. In SB patients, the evoked RMMA response rate differed significantly across sleep stages (stage 2, 14.9% [4.8 to 37.5]; stages 3 and 4, 0% [0 to 66.7]; REM, 0% [0 to 7.7], p = 0.025, Friedman test). Post hoc analysis revealed a significant difference between stages 2 and REM (p = 0.012, Wilcoxon test). Audible tooth-grinding occurred during 71% (22/31) of the evoked episodes in the SB patients only (7.5% of overall experimental arousals [22/295]), and most of these (19/22) occurred in sleep stage 2.
Masticatory Muscle Tone and Heart Rate
During experimental arousals, in the absence of evoked RMMA, the EMG activity of both muscles increased significantly in sleep stage 2 (p < 0.001 for all, ANOVA, Fig. 2A ). There were no differences between the two groups in any of the sleep stages. There was also no difference in change in heart rate between the groups for any sleep stage (Fig. 2B).
This study provides clear evidence that experimentally induced arousal is more frequently followed by RMMA in SB patients than in normal subjects, and that many of these episodes are accompanied by tooth-grinding. These results suggest that SB could be caused by a heightened responsiveness during ongoing transient sleep arousal. Sleep micro-arousal is usually characterized by a transient change in cortical EEG activity, an increase in heart rate, and, occasionally, in muscle activity, and is thought to be a physiological adjustment to endogenous and environmental influences (ASDA, 1992; Monstad and Guilleminault, 1999; Roehr et al., 2000; Sforza et al., 2000). The frequency of spontaneous sleep micro-arousal is normal in young SB patients (Boselli et al., 1998; Sforza et al., 2000; Kato et al., 2001b; Lavigne et al., 2001, 2002). Our results confirm that sleep in SB patients is normal and lead us to reject the first hypothesis, that SB patients have a lower threshold for sleep arousal to environmental stimuli than do normals. More importantly, our results showed that RMMA episodes could be induced, following experimental arousal, seven times more frequently in SB patients than in normal subjects. In addition, tooth-grinding was triggered in SB patients only. These results support the suggestion that SB is a consequence of sleep micro-arousal (Satoh and Harada, 1973; Macaluso et al., 1998; Kato et al., 2001a), and confirm the hypothesis that the RMMA follows experimental arousal more frequently in SB patients than in normal subjects. This study also documented that it was easier to trigger RMMA in sleep stage 2, where 60 to 80% of spontaneous SB episodes occur (Satoh and Harada, 1973; Lavigne et al., 1996; Macaluso et al., 1998). A previous non-controlled study of SB patients showed that visual, tactile, and auditory arousal stimuli induced tooth-grinding in 7.9% of experimental arousals (Satoh and Harada, 1973), which is almost the same value as the 7.5% that we observed. The same authors reported that 65% of evoked tooth-grinding episodes occurred during sleep stage 2 (Satoh and Harada, 1973), which is somewhat less than the 86% seen in our SB population. The increase in RMMA frequency in SB patients was probably not due to a change in motoneuron excitability during sleep, since the resting masticatory muscle EMG was similar in the two groups. Furthermore, the slow rise in masticatory muscle EMG levels during experimental arousal in trials in which no RMMA occurred was similar in the two groups, as was the change in heart rate. These results allow us to reject the third hypothesis, that SB is associated with higher motor excitability. Nonetheless, under the influence of experimental arousal, the frequency with which oromotor events are triggered is higher in SB patients. Although the nature of the link between micro-arousal and RMMA is not known, sleep micro-arousal has been suggested to result from the activation of subcortical and reticular systems which control autonomic, thalamo-cortical, and motor activity (Steriade, 1996; Garcia-Rill, 1997; Lund et al., 1998; Lavigne et al., 2003). Recent evidence indicates the importance of neurochemicals (e.g., orexin, monoamine, dopamine) in the arousal-reticular system and in the pathophysiology of sleep-related periodic motor activity (Mignot et al., 2002; Zhang and Luo, 2002). It is therefore possible that SB is associated with a shift in the balance from sleep-maintaining influences toward a transient increase in activity induced by the arousal-reticular system.
The authors thank B. Adam, P. Rompré, S. Rompré, and L. Tenbokum for their technical support. This study was supported by the Canadian Institute of Health Research and Fonds de la Recherche en Santé du Québec (FRSQ). T. Kato’s fellowship was supported by FRSQ, J.A. DeSève foundation, and FCAR-Central Nervous System Research Group at Université de Montréal. B.J. Sessle is the holder of a Canada Research Chair. Received for publication June 28, 2002. Revision received December 10, 2002. Accepted for publication January 27, 2003.
Journal of Dental Research, Vol. 82, No. 4,
284-288 (2003) This article has been cited by other articles:
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