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Nocturnal sleep architecture is altered by sleep bruxism
Accepted Manuscript Title: Nocturnal sleep architecture is altered by sleep bruxism Author: Marcelo Palinkas Marisa Semprini Jo˜ao Espir Filho Graziela de Luca Canto Isabela Hallak Regalo C´esar Bataglion La´ıse Ang´elica Mendes Rodrigues Selma Si´essere Simone Cecilio Hallak Regalo PII: DOI: Reference:
S0003-9969(17)30135-8 http://dx.doi.org/doi:10.1016/j.archoralbio.2017.04.025 AOB 3869
To appear in:
Archives of Oral Biology
Received date: Revised date: Accepted date:
18-9-2016 9-3-2017 20-4-2017
Please cite this article as: Palinkas M, Semprini M, Filho JE, de Luca Canto G, Regalo IH, Bataglion C, Rodrigues LAM, Si´essere S, Regalo SCH, Nocturnal sleep architecture is altered by sleep bruxism, Archives of Oral Biology (2017), http://dx.doi.org/10.1016/j.archoralbio.2017.04.025 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Nocturnal sleep architecture is altered by sleep bruxism Marcelo Palinkasa,*, Marisa Semprinia, João Espir Filhoa, Graziela de Luca Canto
b,c
, Isabela Hallak
Regaloa, César Batagliond, Laíse Angélica Mendes Rodriguesa, Selma Siésserea, Simone Cecilio Hallak
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Regaloa
a
University of São Paulo, São Paulo, Brazil b
Department of Dentistry, Federal University of Santa Catarina, Florianopolis, Brazil
c
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Department of Dentistry, University of Alberta, Edmonton, Canada
d
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Department of Morphology, Physiology and Basic Pathology, Ribeirão Preto School of Dentistry,
Department of Restorative Dentistry, Ribeirão Preto School of Dentistry, University of São Paulo, São
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Paulo, Brazil
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Corresponding Author: Prof. Marcelo Palinkas. Faculdade de Odontologia de Ribeirão Preto, Universidade de São Paulo. Avenida do Café, s / n, 14040-904, Ribeirão Preto, São Paulo, Brazil.
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Highlights
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Phone: +55 16 3315-0281. E-mail: [email protected]
Sleep bruxism impact on sleep architecture. Evaluation mechanism of sleep parameters in sleep bruxism. The sleep is essential for maintaining the health.
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Abstract. Objective: Sleep is a complex behavior phenomenon essential for physical and mental health and for the body to restore itself. It can be affected by structural alterations caused by sleep bruxism. The aim of this study was verify the effects of sleep bruxism on the sleep architecture parameters
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proposed by the American Academy of Sleep Medicine. Design: The sample comprised ninety individuals, between the ages of 18 and 45 years, divided into two groups: with sleep bruxism (n=45)
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and without sleep bruxism (n=45). The individuals were paired by age, gender and body mass index: A
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polysomnography was performed at night. Results: Statistically significant differences were found between (P≤0.05) individuals with sleep bruxism and individuals without sleep bruxism during total
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sleep time (P=0.00), non-rapid eye movement (NREM) total sleep time (P=0.03), NREM sleep time stage 3 (P=0.03), NREM sleep latency (P=0.05), sleep efficiency (P=0.05) and index of microarousals
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(P=0.04). Conclusions: Sleep bruxism impairs the architecture of nocturnal sleep, interfering with total
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sleep time, NREM sleep latency, and sleep efficiency.
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1.Introduction A normal night sleep is defined as a vital physiological process (Harrington & Lee-Chiong, 2009). It is also described as a transient reversible state (the person can be awakened) (Gemignani, et
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al., 2015) with the purpose to restore the sensory perception and the neuromuscular function, and to regulate the hormonal rhythms (Consensus Conference Panel et al., 2015). Sleep has a complex
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architecture divided into stages. Each has unique characteristics, including physiological variations and
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a structure that regulates the sleep-awake cycle with the circadian rhythm (Yoshida, Shinohara, & Kodama, 2015).
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There are two types of sleep: non-rapid eye movement (NREM) sleep, characterized by nonrapid eye movements and muscle relaxation and rapid eye movement (REM) sleep , which is the most
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restorative part of sleep, with the presence of desynchronized brain wave activity, muscle tone, and
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bursts of rapid eye movements (Berry et al., 2015).
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When a quiet night sleep is disturbed by sleep bruxism, chronic insomnia, narcolepsy or obstructive sleep apnea (OSA) (American Academy of Sleep Medicine, 2014), the consequences of the
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possible functional changes in sleep architecture need to be investigated, as these disorders can negatively affect the quality of life, causing public health problems (Rao, Orpana, & Krewski, 2016), with substantial increases in hospitalizations (Malish, Arastu, & O'Brien, 2016) and health care costs. Previous studies on sleep bruxism reported a prevalence rate of about 8% in adult population (Carra et al., 2015), whose oral-motor movements of the stomatognathic system (American Academy of Sleep Medicine et al., 2005) are characterized by jaw clenching and tooth gnashing or grinding (Lobbezoo et al., 2013), causing a physio-pathological imbalance of the body (Minakuchi et al., 2016). Bibliographic reviews show that, although there are publications on this topic, further research is needed in the field of sleep medicine to help health professionals to better understand the architecture of sleep in individuals affected by sleep bruxism.
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Therefore, the present study aimed to evaluate the sleep architecture through the analysis of some standards set by the American Academy of Sleep Medicine (Berry et al., 2015), which characterize the micro-structure of the night sleep such as: registration period and total sleep time,
N1, N2, and N3, sleep efficiency and index of NREM micro-arousals.
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2. Material and methods
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NREM and REM sleep latency, total period of NREM and REM sleep, period of NREM sleep in stages
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2.1. Subjects recruitment
All subjects were informed about the experiment and agreed to participate by providing their
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free consent according to resolution 466/12 of the Brazilian Health National Council conducted by 1964 Declaration of Helsinki and its later amendments. This cross-sectional, observational study whose
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sample was random selection for the group with sleep bruxism and the selection of the control group
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was a convenience sample paired subject to subject with the group if, as provided for in the
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methodology of the study was approved by the Research Ethics Committee of the Ribeirão Preto School of Dentistry of the University of São Paulo (case n. 02735812.9.0000.5419).
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Among the 580 subjects, ages between 18 and 45 years and with normal occlusion, 150 participants were submitted a one single-night polysomnographic (De Siqueira et al., 2017). The participants were excluded if they presented with a history of neurological or degenerative disorders, chronic orofacial pain, awake bruxism, temporomandibular joint dysfunction, and any objection to take the polysomnography test (Palinkas et al., 2015). Polysomnographic recordings were obtained from 150 patients. Among these, 90 subjects were considered for the final sample. The subjects were divided into two groups paired by gender, age and body mass index: with sleep bruxism (29 men and 16 women with a mean age of 30.58 ± 6.78 yrs and a mean body mass index of 25.59 ± 0.57 Kg/m2) and without sleep bruxism (29 men and 16 women with a mean age of 29.44 ± 7.88 yrs and a mean body mass index 25.18 ± 0.64 kg/m2). A flowchart describing the process of identification, inclusion, and exclusion of subjects is shown in Fig. 1. The Page 4 of 18
anamneses provided data regarding the participants’ medical and dental history, any possible symptoms and signs of temporomandibular dysfunction (DC/TMD) (Schiffman et al., 2014), muscle fatigue and sleep-awake cycles.
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2.2. Polysomnography (gold standard)
Polysomnography (Stuginski-Barbosa et al., 2017) was analyzed using the Meditron-Sonolab
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620 device with 26 A/C programmable channels, six DC constant channels, low consumption and noise
obtain
the
bruxism-related
variables,
the
basic
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level, coupled to 5000v, multi-user software, Windows XP / 2000 / NT and 32-bit C++ compiler. To polysomnographic
measures
of
sleep,
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electroencephalography, electrooculography (bilateral), electromyography (masseter muscle (right and left), temporal muscle (right and left), mentalis muscle and tibialis anterior muscle), plethysmographic
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signals (respiratory effort of the chest and abdomen), body movements and legs, nasal airflow,
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electrocardiogram, bronchogram and visual analysis by video camera, were recorded to confirm sleep based on standards set by the
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bruxism diagnosis, and to characterize the sleep micro-structure
American Academy of Sleep Medicine (2005): registration period and total sleep time (min), NREM
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and REM sleep latency (min), total period of non-REM and REM sleep (min), period of NREM sleep in stages N1, N2, and N3 (min), sleep efficiency (%) and index of NREM micro-arousals (number of events). The bruxism sleep disorder was established when the registered polysomnography showed four or more episodes (phasic, tonic and mixed) during 8 hours of sleep or 25 or more bursts during sleep (Lavigne, Rompré, & Montplaisir, 1996). The subjects were informed that the polysomnography could be interrupted at any time, or ended in the morning of the next day to the examination. Comfort and well-being of the patients during the test were carefully taken into account, such as: type of pillow and bed, room temperature, sounds and noises and correct way to fix the electrodes on the body without causing discomfort. These electrodes were embedded in electrolyte medium and placed on the scalp, the face and leg, using a hypoallergenic tape (3M Micropore™) to record sleep data. Page 5 of 18
Before starting the sleep recordings, the subjects performed calibration tests to recognize the physiological signs like jaw movements, coughing, swallowing, maximum voluntary contraction (maximum force which a human subject can produce in a specific isometric exercise) and rhythmic
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contractions.
2.3. Statistical analysis
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Data were tabulated and it was found that they were normally distributed (Kolmogorov-
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Smirnov). A descriptive analysis was carried out for each variable. The Student’s t test was used for group comparison (significance level of 5%, 95% CI). The statistical analysis was performed using the
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SPSS software, version 22.0 for Windows (SPSS Inc., Chicago, IL, USA).
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3. Results
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Table 1 shows the sleep macro-structure patterns for individuals with sleep bruxism and
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individuals without sleep bruxism. Comparisons of the two groups showed that individuals with sleep bruxism presented a shorter total sleep period when compared to individuals without sleep bruxism.
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The level of statistical significance was set at P≤0.05. SBG revealed increased non-REM latency compared to individuals without sleep bruxism, with statistical significance level of P ≤ 0.05. The NREM and REM sleep periods lasted longer in individuals with sleep bruxism than in individuals without sleep bruxism, with statistical significance level of P ≤ 0.05 in NREM. Data on sleep efficiency showed that individuals with sleep bruxism had significantly higher sleep efficiency (P≤0.05) compared to controls. The results showed that the index of NREM micro-arousals, during the total sleep period, was significantly higher (P ≤ 0.05) in individuals with sleep bruxism when compared to individuals without sleep bruxism. Table 2 shows values during NREM sleep stages N1, N2 and N3 in both groups. The duration of stage 3 was statistically longer (P ≤ 0.05) in individuals with sleep bruxism compared to individuals
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without sleep bruxism. Although there were significant differences for the other stages when the groups were compared, those differences were not statistically significant.
4. Discussion
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It is known that there is a direct relationship between a normal night's sleep and a peaceful and productive day. A normal sleep follows predictable sleep architecture patterns that are used to recover
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energy that was recruited during sleep-awake cycles and to maintain functional and emotional balance
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(Louca & Short, 2014). In contrast, the regular sleep stages may be disturbed by some disorders, including sleep bruxism, with great impact on the sleep dynamics (Boutros et al, 1993).
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In our study, it was observed that the sleep parameters that included total monitoring time sleep latency sleep efficiency, and micro-arousal frequency presented significant differences between the study
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groups. These results were not in agreement with those found by Lavigne et al. (2002) who reported
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that individuals with sleep bruxism display normal sleep architecture in terms of total sleep time, sleep
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latency and percentage of the sleep stage distribution. Although our methodology is similar to the study of Lavigne et al. (2002), the number of individuals who participated in this study was 4 times larger
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and exclusion criteria were different, which may have influenced the difference of results. Sleep is essential for the maintenance of adaptive emotion regulation and reactivity. Sleep deprivation or shorter sleep periods may produce adverse changes in cognitive and physical performance (Palmer & Alfano, 2016). This statement corroborates the results obtained in the present study i.e. the total sleep period in individuals with sleep bruxism showed shorter duration when compared to individuals without sleep bruxism. Sleep bruxism in children causes significant problems of attention and behavior (Herrera et al., 2006). This study has not evaluated the cognitive performance of individuals. The NREM sleep cycle starts with stage N1, which corresponds to 5-10% of the total sleep time. After 1-10 minutes, a deep sleep stage starts (stage N2) with 45 to 55% of the total duration. Stage N3 typically starts 35-45 minutes after falling asleep; the brain waves slow down and become Page 7 of 18
larger. This stage corresponds to 15 to 25% of the total sleep time. After 90 minutes, a standard NREM-REM sleep cycle (25% of the total sleep time) is complete with a total of 4-6 different sleep stages (Consensus Conference Panel, 2015). The results obtained in our study showed that there were no significant differences in NREM
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stage N3. However, the mean percentage in individuals with sleep bruxism was higher compared to control (8.87% and 6.34%, respectively).
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The percentage values found in this stage are not in agreement with those presented in the
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literature, which correspond to 15 to 25% of the total sleep Consensus Conference Panel, 2015). These values are also inconsistent with those of Silva et al. (2012), who reported that sleep disorders reduced
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the time spent in stage N3.
NREM stage N3 is called “slow wave sleep” and is characterized by the presence of slow brain
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waves called “delta waves”. Growth hormones are secreted during this stage (Sprecher et al., 2016).
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Moreover, muscles are relaxed and energy is restored (De Gennaro et al., 2002). We believe that
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individuals with sleep bruxism require longer stage N3 to recover their muscle functions from a nonphysiological rhythmic masticatory muscle activity (RMMA) (Kato, Masuda, & Morimoto, 2007),
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which occurs more frequently and with a wide variation in masseter muscle activity. There is evidence in the literature that normal sleep efficiency is at least 85% (asleep 85% of the night) represented by the proportion of sleep in the episode potentially filled by sleep (i.e., the ratio of total sleep time to time in bed) (Silva, et al., 2012). Our findings revealed that both groups showed normal sleep efficiency, even individuals with sleep bruxism which presented higher percentage value when compared to individuals without sleep bruxism. However, this result does not mean that the night's sleep has affected the repair of neural functions (Raschke, 2004), in view of the shorter duration of the REM stage when compared to individuals without sleep bruxism. The NREM sleep latency is defined as the length of time that it takes to accomplish the transition from full wakefulness to sleep. The results of this study showed that the mean values found Page 8 of 18
for the latency period in individuals with sleep bruxism were higher when compared to individuals without sleep bruxism. This finding is in agreement with that described in the literature with regard to the increased latency, except the time, which was less than 30 minutes (Correa et al., 2014) for the normal sleep of the individual in contrast to our individuals without sleep bruxism, in which the time
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was 149.37±14.66. When some studies in the literature describe that the latency is high, the researchers are suggesting that individuals may have difficulties falling asleep, indicating initial or middle
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insomnia (Schutte-Rodin et al., 2008). Sleep disorders such as obstructive sleep apnea in adults and
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children are characterized by prolonged sleep latency and decrease in sleep time (Gurbani et al., 2017). Previous studies on normal sleep stages showed that micro-arousals are frequent and in NREM
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sleep may occur without a rise in muscle tone (Ramirez et al., 2013) with that in mind, we decided to verify the relationship between the number of microarousals during nocturnal sleep in sleep bruxism
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patients. It was observed that individuals with sleep bruxism presented a mean micro-arousal index of
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67.76, with statistical significance, compared to 54.49 in individuals without sleep bruxism. Sleep
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fragmentation is associated with poor mood, muscle fatigue, sleepiness, and negative effects on mental processes, hormone imbalance, reduced lung capacity and changes in metabolic rate (Ogawa, Nittono,
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& Hori, 2005). Huynh et al. (2006) reported that the microarousals in individuals with sleep bruxism were higher during the N2 and N3 with statistically significant. In this study, 83% of individuals with sleep bruxism that responded to the anamnesis questionnaire reported tiredness, sleepiness during the day and muscle discomfort upon awakening, which probably suggest that such manifestations are associated with rhythmic masticatory muscle activity involving the masticatory muscles. These results corroborate those by Mayer et al. (2016) and in contrast, Dumais et al.(2015) observed that those manifestations were related to microarousals during the total period of sleep. The association between the incidence of micro-arousals, muscle fatigue and initial sleepiness, were not included in the present study.
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The changes found in sleep architecture of individuals with bruxism may be attributed to the interaction of innumerous situations, and should be justified separately to demonstrate a single and total effect. For example, sleep efficiency in individuals with sleep bruxism could reflect on a normal sleep
opposite, considering that the incidence and the percentage remained higher.
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period; in contrast, the micro-arousals, the latency, and the period of non-REM sleep showed the
The results obtained encourage us to continue exploring this topic and to verify other
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parameters, namely the behavior and the social interaction of the individual with sleep bruxism, muscle
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fatigue and emotional changes caused by stress, irritability, anxiety and depression. The assessment of sleep architecture requires detailed observation of those external or internal stimuli that can affect the
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sleep dynamics.
Despite the great interest of the health care community in Sleep Medicine that seek to
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understand what happens to sleep architecture associated with several disorders, there is lack of
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information regarding the effects of sleep bruxism.
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The results described in the present study aimed to provide health professionals with parameters to obtain a better understanding of the sleep structure in bruxers, and to prescribe adequate treatment
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for this sleep-related movement disorder.
Limitation of this study includes the fact that the participants were observed only during a single night at the sleep laboratory. Probably more time would be needed for the adaptation to the equipment, sleeping environment, or both. However, according to Hasegawa et al. (2013), one-night sleep recording may be sufficient for moderate-high frequency sleep bruxism individuals.
5. Conclusions Sleep bruxism impairs the night sleep architecture evidenced by the different parameters related to the total sleep time (TST), the NREM sleep latency (NREMSL), and the sleep efficiency (SE), which characterize adverse changes in the sleep macrostructure, affecting its quality. Based on the results obtained, it can be concluded that additional studies should focus on this topic. Page 10 of 18
Funding
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Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Brazil provided financial support
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(012/10228-6). The sponsor had no role in the design or conduct of this research.
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Competing interests
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None declared.
Ethical approval
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All procedures performed in studies involving human participants were in accordance with the ethical
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standards of the institutional and/or national research committee and with the 1964 Helsinki declaration
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and its later amendments or comparable ethical standards. . This research was approved by the Research Ethics Committee of the Ribeirão Preto School of Dentistry of the University of São Paulo
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(case N. 02735812.9.0000.5419).
Informed consent
Informed consent was obtained from all individual participants included in the study.
Acknowledgements We gratefully acknowledge the support of Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Brazil.
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Excluded OSA (n=6)
Research Participants (n=90)
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Control group (n=45)
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SB Group (n=45)
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Included
Excluded Not attended PSG (n=9)
Excluded Awake bruxism (n=15)
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Excluded TMD (n-30)
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SAMPLE (n=150)
Eligibility
Screening
Identification
Figure 1. Diagram of Selection Criteria
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Table 1. Means, standard error (±) and statistical significance (P≤0.05)* of sleep macro-structure: sleep time period (STP), total sleep time (TST), NREM sleep latency (NREMSL), REM sleep latency (REMSL), NREM sleep time (NREMST), REM sleep time (REMST), sleep efficiency (SE) and NREM microarousal index (MI) for individuals with sleep bruxism (SBG) and individuals without
SBG
CG
P value
STP (min)
455.22 ± 4.55
464.02 ± 4.79
TST (min)
400.54 ± 5.51
420.52 ± 4.50
cr
NREMSL (min)
35.23 ± 3.18
26.57 ± 3.27
0.05*
REMSL (min)
156.81±14.19
149.37±14.66
0.71
NREMST (min)
390.20 ± 6.19
372.70 ± 5.09
0.03*
TREM (min)
27.84 ± 3.08
30.33 ± 3.65
0.60
SE (%)
90.80 ± 0.75
88.38 ± 0.99
0.05*
MI (n. events TST)
67.76 ± 4.48
54.49 ± 4.89
0.04*
0.18
M
an
us
0.00*
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te
d
Varibles
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sleep bruxism (CG).
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Table 2. Means, standard error (±) and statistical significance (P≤0.05)* of NREM sleep (min) stage N1, stage N2 and stage N3 for individuals with sleep bruxism (SBG) and individuals without sleep bruxism (CG).
CG
P value
N1
91.35 ± 4.19
96.79 ± 5.58
0.43
N2
265.73 ± 4.70
250.35 ± 8.54
0.11
N3
35.64 ± 3.29
25.40 ± 3.31
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SBG
cr
Stages
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te
d
M
an
us
0.03*
Page 18 of 18
S0003-9969(17)30135-8 http://dx.doi.org/doi:10.1016/j.archoralbio.2017.04.025 AOB 3869
To appear in:
Archives of Oral Biology
Received date: Revised date: Accepted date:
18-9-2016 9-3-2017 20-4-2017
Please cite this article as: Palinkas M, Semprini M, Filho JE, de Luca Canto G, Regalo IH, Bataglion C, Rodrigues LAM, Si´essere S, Regalo SCH, Nocturnal sleep architecture is altered by sleep bruxism, Archives of Oral Biology (2017), http://dx.doi.org/10.1016/j.archoralbio.2017.04.025 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Nocturnal sleep architecture is altered by sleep bruxism Marcelo Palinkasa,*, Marisa Semprinia, João Espir Filhoa, Graziela de Luca Canto
b,c
, Isabela Hallak
Regaloa, César Batagliond, Laíse Angélica Mendes Rodriguesa, Selma Siésserea, Simone Cecilio Hallak
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Regaloa
a
University of São Paulo, São Paulo, Brazil b
Department of Dentistry, Federal University of Santa Catarina, Florianopolis, Brazil
c
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Department of Dentistry, University of Alberta, Edmonton, Canada
d
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Department of Morphology, Physiology and Basic Pathology, Ribeirão Preto School of Dentistry,
Department of Restorative Dentistry, Ribeirão Preto School of Dentistry, University of São Paulo, São
an
Paulo, Brazil
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Corresponding Author: Prof. Marcelo Palinkas. Faculdade de Odontologia de Ribeirão Preto, Universidade de São Paulo. Avenida do Café, s / n, 14040-904, Ribeirão Preto, São Paulo, Brazil.
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Highlights
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Phone: +55 16 3315-0281. E-mail: [email protected]
Sleep bruxism impact on sleep architecture. Evaluation mechanism of sleep parameters in sleep bruxism. The sleep is essential for maintaining the health.
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Abstract. Objective: Sleep is a complex behavior phenomenon essential for physical and mental health and for the body to restore itself. It can be affected by structural alterations caused by sleep bruxism. The aim of this study was verify the effects of sleep bruxism on the sleep architecture parameters
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proposed by the American Academy of Sleep Medicine. Design: The sample comprised ninety individuals, between the ages of 18 and 45 years, divided into two groups: with sleep bruxism (n=45)
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and without sleep bruxism (n=45). The individuals were paired by age, gender and body mass index: A
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polysomnography was performed at night. Results: Statistically significant differences were found between (P≤0.05) individuals with sleep bruxism and individuals without sleep bruxism during total
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sleep time (P=0.00), non-rapid eye movement (NREM) total sleep time (P=0.03), NREM sleep time stage 3 (P=0.03), NREM sleep latency (P=0.05), sleep efficiency (P=0.05) and index of microarousals
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(P=0.04). Conclusions: Sleep bruxism impairs the architecture of nocturnal sleep, interfering with total
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sleep time, NREM sleep latency, and sleep efficiency.
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1.Introduction A normal night sleep is defined as a vital physiological process (Harrington & Lee-Chiong, 2009). It is also described as a transient reversible state (the person can be awakened) (Gemignani, et
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al., 2015) with the purpose to restore the sensory perception and the neuromuscular function, and to regulate the hormonal rhythms (Consensus Conference Panel et al., 2015). Sleep has a complex
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architecture divided into stages. Each has unique characteristics, including physiological variations and
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a structure that regulates the sleep-awake cycle with the circadian rhythm (Yoshida, Shinohara, & Kodama, 2015).
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There are two types of sleep: non-rapid eye movement (NREM) sleep, characterized by nonrapid eye movements and muscle relaxation and rapid eye movement (REM) sleep , which is the most
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restorative part of sleep, with the presence of desynchronized brain wave activity, muscle tone, and
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bursts of rapid eye movements (Berry et al., 2015).
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When a quiet night sleep is disturbed by sleep bruxism, chronic insomnia, narcolepsy or obstructive sleep apnea (OSA) (American Academy of Sleep Medicine, 2014), the consequences of the
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possible functional changes in sleep architecture need to be investigated, as these disorders can negatively affect the quality of life, causing public health problems (Rao, Orpana, & Krewski, 2016), with substantial increases in hospitalizations (Malish, Arastu, & O'Brien, 2016) and health care costs. Previous studies on sleep bruxism reported a prevalence rate of about 8% in adult population (Carra et al., 2015), whose oral-motor movements of the stomatognathic system (American Academy of Sleep Medicine et al., 2005) are characterized by jaw clenching and tooth gnashing or grinding (Lobbezoo et al., 2013), causing a physio-pathological imbalance of the body (Minakuchi et al., 2016). Bibliographic reviews show that, although there are publications on this topic, further research is needed in the field of sleep medicine to help health professionals to better understand the architecture of sleep in individuals affected by sleep bruxism.
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Therefore, the present study aimed to evaluate the sleep architecture through the analysis of some standards set by the American Academy of Sleep Medicine (Berry et al., 2015), which characterize the micro-structure of the night sleep such as: registration period and total sleep time,
N1, N2, and N3, sleep efficiency and index of NREM micro-arousals.
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2. Material and methods
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NREM and REM sleep latency, total period of NREM and REM sleep, period of NREM sleep in stages
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2.1. Subjects recruitment
All subjects were informed about the experiment and agreed to participate by providing their
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free consent according to resolution 466/12 of the Brazilian Health National Council conducted by 1964 Declaration of Helsinki and its later amendments. This cross-sectional, observational study whose
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sample was random selection for the group with sleep bruxism and the selection of the control group
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was a convenience sample paired subject to subject with the group if, as provided for in the
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methodology of the study was approved by the Research Ethics Committee of the Ribeirão Preto School of Dentistry of the University of São Paulo (case n. 02735812.9.0000.5419).
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Among the 580 subjects, ages between 18 and 45 years and with normal occlusion, 150 participants were submitted a one single-night polysomnographic (De Siqueira et al., 2017). The participants were excluded if they presented with a history of neurological or degenerative disorders, chronic orofacial pain, awake bruxism, temporomandibular joint dysfunction, and any objection to take the polysomnography test (Palinkas et al., 2015). Polysomnographic recordings were obtained from 150 patients. Among these, 90 subjects were considered for the final sample. The subjects were divided into two groups paired by gender, age and body mass index: with sleep bruxism (29 men and 16 women with a mean age of 30.58 ± 6.78 yrs and a mean body mass index of 25.59 ± 0.57 Kg/m2) and without sleep bruxism (29 men and 16 women with a mean age of 29.44 ± 7.88 yrs and a mean body mass index 25.18 ± 0.64 kg/m2). A flowchart describing the process of identification, inclusion, and exclusion of subjects is shown in Fig. 1. The Page 4 of 18
anamneses provided data regarding the participants’ medical and dental history, any possible symptoms and signs of temporomandibular dysfunction (DC/TMD) (Schiffman et al., 2014), muscle fatigue and sleep-awake cycles.
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2.2. Polysomnography (gold standard)
Polysomnography (Stuginski-Barbosa et al., 2017) was analyzed using the Meditron-Sonolab
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620 device with 26 A/C programmable channels, six DC constant channels, low consumption and noise
obtain
the
bruxism-related
variables,
the
basic
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level, coupled to 5000v, multi-user software, Windows XP / 2000 / NT and 32-bit C++ compiler. To polysomnographic
measures
of
sleep,
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electroencephalography, electrooculography (bilateral), electromyography (masseter muscle (right and left), temporal muscle (right and left), mentalis muscle and tibialis anterior muscle), plethysmographic
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signals (respiratory effort of the chest and abdomen), body movements and legs, nasal airflow,
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electrocardiogram, bronchogram and visual analysis by video camera, were recorded to confirm sleep based on standards set by the
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bruxism diagnosis, and to characterize the sleep micro-structure
American Academy of Sleep Medicine (2005): registration period and total sleep time (min), NREM
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and REM sleep latency (min), total period of non-REM and REM sleep (min), period of NREM sleep in stages N1, N2, and N3 (min), sleep efficiency (%) and index of NREM micro-arousals (number of events). The bruxism sleep disorder was established when the registered polysomnography showed four or more episodes (phasic, tonic and mixed) during 8 hours of sleep or 25 or more bursts during sleep (Lavigne, Rompré, & Montplaisir, 1996). The subjects were informed that the polysomnography could be interrupted at any time, or ended in the morning of the next day to the examination. Comfort and well-being of the patients during the test were carefully taken into account, such as: type of pillow and bed, room temperature, sounds and noises and correct way to fix the electrodes on the body without causing discomfort. These electrodes were embedded in electrolyte medium and placed on the scalp, the face and leg, using a hypoallergenic tape (3M Micropore™) to record sleep data. Page 5 of 18
Before starting the sleep recordings, the subjects performed calibration tests to recognize the physiological signs like jaw movements, coughing, swallowing, maximum voluntary contraction (maximum force which a human subject can produce in a specific isometric exercise) and rhythmic
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contractions.
2.3. Statistical analysis
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Data were tabulated and it was found that they were normally distributed (Kolmogorov-
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Smirnov). A descriptive analysis was carried out for each variable. The Student’s t test was used for group comparison (significance level of 5%, 95% CI). The statistical analysis was performed using the
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SPSS software, version 22.0 for Windows (SPSS Inc., Chicago, IL, USA).
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3. Results
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Table 1 shows the sleep macro-structure patterns for individuals with sleep bruxism and
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individuals without sleep bruxism. Comparisons of the two groups showed that individuals with sleep bruxism presented a shorter total sleep period when compared to individuals without sleep bruxism.
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The level of statistical significance was set at P≤0.05. SBG revealed increased non-REM latency compared to individuals without sleep bruxism, with statistical significance level of P ≤ 0.05. The NREM and REM sleep periods lasted longer in individuals with sleep bruxism than in individuals without sleep bruxism, with statistical significance level of P ≤ 0.05 in NREM. Data on sleep efficiency showed that individuals with sleep bruxism had significantly higher sleep efficiency (P≤0.05) compared to controls. The results showed that the index of NREM micro-arousals, during the total sleep period, was significantly higher (P ≤ 0.05) in individuals with sleep bruxism when compared to individuals without sleep bruxism. Table 2 shows values during NREM sleep stages N1, N2 and N3 in both groups. The duration of stage 3 was statistically longer (P ≤ 0.05) in individuals with sleep bruxism compared to individuals
Page 6 of 18
without sleep bruxism. Although there were significant differences for the other stages when the groups were compared, those differences were not statistically significant.
4. Discussion
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It is known that there is a direct relationship between a normal night's sleep and a peaceful and productive day. A normal sleep follows predictable sleep architecture patterns that are used to recover
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energy that was recruited during sleep-awake cycles and to maintain functional and emotional balance
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(Louca & Short, 2014). In contrast, the regular sleep stages may be disturbed by some disorders, including sleep bruxism, with great impact on the sleep dynamics (Boutros et al, 1993).
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In our study, it was observed that the sleep parameters that included total monitoring time sleep latency sleep efficiency, and micro-arousal frequency presented significant differences between the study
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groups. These results were not in agreement with those found by Lavigne et al. (2002) who reported
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that individuals with sleep bruxism display normal sleep architecture in terms of total sleep time, sleep
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latency and percentage of the sleep stage distribution. Although our methodology is similar to the study of Lavigne et al. (2002), the number of individuals who participated in this study was 4 times larger
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and exclusion criteria were different, which may have influenced the difference of results. Sleep is essential for the maintenance of adaptive emotion regulation and reactivity. Sleep deprivation or shorter sleep periods may produce adverse changes in cognitive and physical performance (Palmer & Alfano, 2016). This statement corroborates the results obtained in the present study i.e. the total sleep period in individuals with sleep bruxism showed shorter duration when compared to individuals without sleep bruxism. Sleep bruxism in children causes significant problems of attention and behavior (Herrera et al., 2006). This study has not evaluated the cognitive performance of individuals. The NREM sleep cycle starts with stage N1, which corresponds to 5-10% of the total sleep time. After 1-10 minutes, a deep sleep stage starts (stage N2) with 45 to 55% of the total duration. Stage N3 typically starts 35-45 minutes after falling asleep; the brain waves slow down and become Page 7 of 18
larger. This stage corresponds to 15 to 25% of the total sleep time. After 90 minutes, a standard NREM-REM sleep cycle (25% of the total sleep time) is complete with a total of 4-6 different sleep stages (Consensus Conference Panel, 2015). The results obtained in our study showed that there were no significant differences in NREM
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stage N3. However, the mean percentage in individuals with sleep bruxism was higher compared to control (8.87% and 6.34%, respectively).
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The percentage values found in this stage are not in agreement with those presented in the
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literature, which correspond to 15 to 25% of the total sleep Consensus Conference Panel, 2015). These values are also inconsistent with those of Silva et al. (2012), who reported that sleep disorders reduced
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the time spent in stage N3.
NREM stage N3 is called “slow wave sleep” and is characterized by the presence of slow brain
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waves called “delta waves”. Growth hormones are secreted during this stage (Sprecher et al., 2016).
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Moreover, muscles are relaxed and energy is restored (De Gennaro et al., 2002). We believe that
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individuals with sleep bruxism require longer stage N3 to recover their muscle functions from a nonphysiological rhythmic masticatory muscle activity (RMMA) (Kato, Masuda, & Morimoto, 2007),
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which occurs more frequently and with a wide variation in masseter muscle activity. There is evidence in the literature that normal sleep efficiency is at least 85% (asleep 85% of the night) represented by the proportion of sleep in the episode potentially filled by sleep (i.e., the ratio of total sleep time to time in bed) (Silva, et al., 2012). Our findings revealed that both groups showed normal sleep efficiency, even individuals with sleep bruxism which presented higher percentage value when compared to individuals without sleep bruxism. However, this result does not mean that the night's sleep has affected the repair of neural functions (Raschke, 2004), in view of the shorter duration of the REM stage when compared to individuals without sleep bruxism. The NREM sleep latency is defined as the length of time that it takes to accomplish the transition from full wakefulness to sleep. The results of this study showed that the mean values found Page 8 of 18
for the latency period in individuals with sleep bruxism were higher when compared to individuals without sleep bruxism. This finding is in agreement with that described in the literature with regard to the increased latency, except the time, which was less than 30 minutes (Correa et al., 2014) for the normal sleep of the individual in contrast to our individuals without sleep bruxism, in which the time
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was 149.37±14.66. When some studies in the literature describe that the latency is high, the researchers are suggesting that individuals may have difficulties falling asleep, indicating initial or middle
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insomnia (Schutte-Rodin et al., 2008). Sleep disorders such as obstructive sleep apnea in adults and
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children are characterized by prolonged sleep latency and decrease in sleep time (Gurbani et al., 2017). Previous studies on normal sleep stages showed that micro-arousals are frequent and in NREM
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sleep may occur without a rise in muscle tone (Ramirez et al., 2013) with that in mind, we decided to verify the relationship between the number of microarousals during nocturnal sleep in sleep bruxism
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patients. It was observed that individuals with sleep bruxism presented a mean micro-arousal index of
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67.76, with statistical significance, compared to 54.49 in individuals without sleep bruxism. Sleep
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fragmentation is associated with poor mood, muscle fatigue, sleepiness, and negative effects on mental processes, hormone imbalance, reduced lung capacity and changes in metabolic rate (Ogawa, Nittono,
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& Hori, 2005). Huynh et al. (2006) reported that the microarousals in individuals with sleep bruxism were higher during the N2 and N3 with statistically significant. In this study, 83% of individuals with sleep bruxism that responded to the anamnesis questionnaire reported tiredness, sleepiness during the day and muscle discomfort upon awakening, which probably suggest that such manifestations are associated with rhythmic masticatory muscle activity involving the masticatory muscles. These results corroborate those by Mayer et al. (2016) and in contrast, Dumais et al.(2015) observed that those manifestations were related to microarousals during the total period of sleep. The association between the incidence of micro-arousals, muscle fatigue and initial sleepiness, were not included in the present study.
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The changes found in sleep architecture of individuals with bruxism may be attributed to the interaction of innumerous situations, and should be justified separately to demonstrate a single and total effect. For example, sleep efficiency in individuals with sleep bruxism could reflect on a normal sleep
opposite, considering that the incidence and the percentage remained higher.
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period; in contrast, the micro-arousals, the latency, and the period of non-REM sleep showed the
The results obtained encourage us to continue exploring this topic and to verify other
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parameters, namely the behavior and the social interaction of the individual with sleep bruxism, muscle
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fatigue and emotional changes caused by stress, irritability, anxiety and depression. The assessment of sleep architecture requires detailed observation of those external or internal stimuli that can affect the
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sleep dynamics.
Despite the great interest of the health care community in Sleep Medicine that seek to
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understand what happens to sleep architecture associated with several disorders, there is lack of
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information regarding the effects of sleep bruxism.
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The results described in the present study aimed to provide health professionals with parameters to obtain a better understanding of the sleep structure in bruxers, and to prescribe adequate treatment
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for this sleep-related movement disorder.
Limitation of this study includes the fact that the participants were observed only during a single night at the sleep laboratory. Probably more time would be needed for the adaptation to the equipment, sleeping environment, or both. However, according to Hasegawa et al. (2013), one-night sleep recording may be sufficient for moderate-high frequency sleep bruxism individuals.
5. Conclusions Sleep bruxism impairs the night sleep architecture evidenced by the different parameters related to the total sleep time (TST), the NREM sleep latency (NREMSL), and the sleep efficiency (SE), which characterize adverse changes in the sleep macrostructure, affecting its quality. Based on the results obtained, it can be concluded that additional studies should focus on this topic. Page 10 of 18
Funding
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Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Brazil provided financial support
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(012/10228-6). The sponsor had no role in the design or conduct of this research.
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Competing interests
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None declared.
Ethical approval
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All procedures performed in studies involving human participants were in accordance with the ethical
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standards of the institutional and/or national research committee and with the 1964 Helsinki declaration
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and its later amendments or comparable ethical standards. . This research was approved by the Research Ethics Committee of the Ribeirão Preto School of Dentistry of the University of São Paulo
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(case N. 02735812.9.0000.5419).
Informed consent
Informed consent was obtained from all individual participants included in the study.
Acknowledgements We gratefully acknowledge the support of Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Brazil.
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Electroencephalography. PLoS One, 11(2):e0149770.
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Stuginski-Barbosa, J., Porporatti, A.L., Costa, Y.M., Svensson, P., Conti, P.C. (2017). Agreement
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of the International Classification of Sleep Disorders Criteria with polysomnography for sleep bruxism diagnosis: A preliminary study. J Prosthet Dent, 117(1):61-66.
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Yoshida, M., Shinohara, H., Kodama, H.. Assessment of nocturnal sleep architecture by actigraphy and one-channel electroencephalography in early infancy. (2015). Early Hum Dev, 91(9):519-526.
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Excluded OSA (n=6)
Research Participants (n=90)
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Control group (n=45)
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SB Group (n=45)
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Included
Excluded Not attended PSG (n=9)
Excluded Awake bruxism (n=15)
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Excluded TMD (n-30)
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SAMPLE (n=150)
Eligibility
Screening
Identification
Figure 1. Diagram of Selection Criteria
Page 16 of 18
Table 1. Means, standard error (±) and statistical significance (P≤0.05)* of sleep macro-structure: sleep time period (STP), total sleep time (TST), NREM sleep latency (NREMSL), REM sleep latency (REMSL), NREM sleep time (NREMST), REM sleep time (REMST), sleep efficiency (SE) and NREM microarousal index (MI) for individuals with sleep bruxism (SBG) and individuals without
SBG
CG
P value
STP (min)
455.22 ± 4.55
464.02 ± 4.79
TST (min)
400.54 ± 5.51
420.52 ± 4.50
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NREMSL (min)
35.23 ± 3.18
26.57 ± 3.27
0.05*
REMSL (min)
156.81±14.19
149.37±14.66
0.71
NREMST (min)
390.20 ± 6.19
372.70 ± 5.09
0.03*
TREM (min)
27.84 ± 3.08
30.33 ± 3.65
0.60
SE (%)
90.80 ± 0.75
88.38 ± 0.99
0.05*
MI (n. events TST)
67.76 ± 4.48
54.49 ± 4.89
0.04*
0.18
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0.00*
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Varibles
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sleep bruxism (CG).
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Table 2. Means, standard error (±) and statistical significance (P≤0.05)* of NREM sleep (min) stage N1, stage N2 and stage N3 for individuals with sleep bruxism (SBG) and individuals without sleep bruxism (CG).
CG
P value
N1
91.35 ± 4.19
96.79 ± 5.58
0.43
N2
265.73 ± 4.70
250.35 ± 8.54
0.11
N3
35.64 ± 3.29
25.40 ± 3.31
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SBG
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Stages
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M
an
us
0.03*
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