Headache Medicine 2021, 12(1) p-ISSN 2178-7468, e-ISSN 2763-6178
35
ASAA
DOI: 10.48208/HeadacheMed.2021.7
Headache Medicine
© Copyright 2021
Original
Association between sleep and awake bruxism in patients with migraine
Keryn Sporh Godk
1
Maria Luiza dos Santos
1
Marco Antonio Takashi Utiumi
2,3,4
João Guilherme
Bochnia Küster
1
Luiz Carlos Canalli Filho
1
Nikolai José Eustátios Kotsifas
1
Bin Cheng Tan
1
Eldislei Mioto
1
Gabriel Eduardo Faria Colombani
1
Elcio Juliato Piovesan
2,3
1
Federal University of Paraná, Health Sciences Sector, Curitiba PR, Brazil.
2
Federal University of Paraná General Hospital, Department of Internal Medicine, Curitiba PR, Brazil.
3
São José Neurology Clinic, São José dos Pinhais PR, Brazil.
4
Marcelino Champagnat Hospital, Neurology Service, Curitiba PR, Brazil.
Abstract
Introduction
When migraine undergoes transformation from episodic to chronic form it becomes more disabling due
to the refractoriness in treatment and the emergence of comorbidities, with the establishment of a bidi-
rectional relationship between sleep bruxism and chronic migraine. This study aimed to assess whether
sleep and awake bruxism are more prevalent in chronic migraine when compared to episodic migraine
and also to establish possible clinical correlations with the process of chronication.
Methods
210 patients were allocated to the study, 97 with episodic migraine and 113 with chronic migraine,
who underwent face-to-face interviews with the completion of the scales: specic questionnaire for the
diagnosis of sleep and awake bruxism, PHQ-9 (depression), GAD-7 (anxiety), Epworth Scale (daytime
sleepiness), MIDAS (migraine incapacity) and HIT-6 (impact of headache).
Results
The prevalence of sleep and awake bruxism was similar in patients with episodic versus chronic migraine
(p=0.300 and p=0.238). The correlation of patients with concomitant awake and sleep bruxism and with
high scores on the migraine incapacity (MIDAS) and headache impact (HIT-6) scales was higher among
patients with chronic migraine than in patients with episodic migraine. (p<0.001 and p<0.001).
Conclusion
Sleep and awake bruxism alone are not more prevalent in chronic migraine when compared to epi-
sodic migraine, although bruxism causes greater impact and disability on individuals with chronic
migraine.
Elcio Juliato Piovesan
Rua General Carneiro, 180,
Alto da Glória, Curitiba, Paraná,
Brazil
Federal University of Paraná
General Hospital
Zip-Code: 80060-900
Phone number: +55 41
33601866
piovesan1@hotmail.com
Edited by:
Marcelo Moraes Valença
Keywords:
Sleep bruxism
Awake bruxism
Migraine Disorders
Impact prole of the disease
Depression
Comorbidity
Received: June 28, 2021
Accepted: August 11, 2021
36
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
Introduction
M
igraine is considered one of the most debilitating pa-
thologies with roughly half of the patients losing func-
tional capacity during migraine attacks in addition to being
associated with a wide spectrum of comorbidities.
1
In Brazil,
migraine has a prevalence of 15.2% reaching its peak in
the third decade of life and in the female sex (27.1%).
2
According to its frequency, it can be classied as episodic
(<15 days a month) or chronic (≥15 days a month for at
least 3 months a year).
3
Migraine is clinically characterized
by a headache with a duration of 4 to 72 hours if left un-
treated, with a unilateral, pulsatile pain pattern of moderate
to severe intensity, aggravated by routine physical activity
and usually associated with nausea, vomiting, photophobia,
phonophobia and allodynia.
4
The prevalence of the chronic
form of migraine in Brazil is 5.12% being characterized
by a greater impact on the quality of life, more refractori-
ness to prophylactic treatments, greater predisposition to
comorbidities, disability and loss of productivity, and an
increased demand for medical services and hospitalizations
that consequently generate a high socioeconomic cost.
5,6
Bruxism is a frequent disorder with 85% to 90% of the
general population reporting at least one episode of
grinding or clenching their teeth throughout their lives.
7
Bruxism is dened as a repetitive activity of the masticatory
muscles that is characterized by squeezing or grinding
the teeth and/or pushing or holding the jaw, being
classied according to its circadian phenotype in sleep
bruxism or awake bruxism.
8
More recently, sleep bruxism
was dened as masticatory muscle activity during sleep,
formed by a rhythmic phase (Phasic Phase) and a non-
rhythmic phase (Tonic Phase). Awake Bruxism is an activity
of the masticatory muscles that occurs during wakefulness,
being characterized by repetitive and prolonged tooth
contact and/or locking or protrusion of the jaw. Both are
not considered movement disorders in healthy individuals.
9
Self-reported sleep bruxism is 13% in the adult population
and for awake bruxism the prevalence is 22% in adults
and 31% in women and young people.
10
It is estimated
that one in ve people in the general population have a
clinical overlap between sleep and awake bruxism.
11
The
presence of bruxism can be associated with environmental
and genetic factors, stress, anxiety, depression, alterations
in the autonomic system, sleep structure, and use of drugs
or medications, and those are in line with the factors and
comorbidities related to migraine.
12,13
The association between migraine and bruxism in adults
has been documented by several studies, although the
causality has not yet been completely elucidated.
14
A
study carried out in Brazil in 2013 showed that 74.6% of
participants with chronic migraine also had sleep bruxism.
15
Canto et al. in 2014 demonstrated that the risk for patients
with the chronic form of migraine to develop sleep bruxism
is 3.12-3.8 times higher thus demonstrating a bidirectional
relationship between those two pathologies. Regarding
episodic migraine no statistically signicant results were
evidenced.
16
The inuence of sleep or awake bruxism in the evolution
process of episodic to chronic migraine is not well reported
in the literature. This study aimed to assess whether sleep
and awake bruxism are more prevalent in chronic migraine
when compared to episodic migraine and also to establish
possible clinical correlations with chronication.
Methods
Study design
A comparative cross-sectional observational study between
episodic migraine (EM) and chronic migraine (CM) was
carried out, and individuals of both sexes aged between
18 and 64 years participated. Diagnosis of EM and CM
was dened according to the criteria of the International
Classication of Headache Disorders 3rd edition (ICHD-3).
3
Patients were allocated into groups based on consultations
carried out between 2018 and 2020 and three Brazilian
healthcare centers participated in this research: a tertiary-
level healthcare center that exclusively serves the public
health system (Federal University of Paraná General
Hospital) and two headache outpatient clinics (São Jo
Neurology Clinic and Marcelino Champagnat Hospital).
Ethical aspects
This study was approved by the Ethics Committee of the
Federal University of Paraná General Hospital (registration
2.732.610, CAAE number: 87998518.8.0000.0096)
and was registered in the Brazilian Registry of Clinical
Trials (RBR-9wgwnj). Written Informed Consent was
obtained from all the patients prior to data collection.
Study design and population characteristics
Subjects allocated to study participation should meet the
following criteria: (1) Present a denitive diagnosis of EM
or CM (with or without analgesic abuse) in accordance
with the ICHD-3 criteria; (2) Had migraine attacks within
a minimum period of six months at the beginning of the
37
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
study; (3) Had no limitations in information retrieval (e.g.,
severe aphasia, severe hearing loss, or other situations that
could limit the understanding of the questionnaire applied);
(4) Had no associated conditions that could promote
diagnostic confusion (e.g., HIV infections, active cancer,
use of immunosuppressive drugs); (5) Completed all
medical questionnaires; and (6) Agreed to participate in
the study by signing the Written Informed Consent form. All
subjects included in the study received a clinical diagnosis
of EM or CM after a face-to-face medical consultation with
a neurologist with experience in the area of headache
(authors MATU and EJP). The exclusion criteria were: (1)
Withdrawal by the participant of the consent to participate
in the study; and (2) The development of any other type of
headache during the research interval.
Weekly alcohol consumption was classied as: (1) Present;
or (2) Absent. The aerobic physical activity classication
was in accordance with the World Health Organization
recommendations: (1) ≥150 minutes of moderate intensity
or (2) ≥75 minutes of vigorous intensity per week were
considerated as adequate physical activity and the rest
was considered as (3) sedentary.
17
Monthly income was
calculated to assess the socioeconomic inuence on the
results. The monthly earnings of all family members were
added and divided by the number of individuals residing
in the family group. For years with migraine disease, the
period between the rst migraine attack and the time of
study evaluation was considered.
Data collection, instruments and methods used
To assess depression, anxiety and daytime sleepiness, the
following scales were respectively used: PHQ-9 (Patient
Health Questionnaire-9)
18
; GAD-7 (Generalized Anxiety
Disorder-7)
19
and Epworth scale.
20
MIDAS (Migraine
Disability Assessment Test)
21
and HIT-6 (Headache Impact
Test)
22
scales were also included to assess, respectively,
migraine disability and headache impact in study subjects.
Identification of awake and sleep bruxism
To establish the diagnosis of sleep bruxism, a questionnaire
consisting of seven questions prepared by the American
Academy for Sleep Disorders was used
23
: (1) “Do you
grind or clench your teeth during sleep?”; (2) “When you
wake up, do you feel pain or fatigue in the muscles of the
face?”; (3) “When you wake up and move your mouth, do
you notice stiffness or blockage in your joint?”; (4) “You feel
discomfort in your teeth when you wake up?”; (5) “Do you
feel a headache in your temples when you wake up?”; (6)
“Has a relative or roommate ever reported that you make
creaking noises while sleeping?”; (7) “In the past three
months, have you had fractured teeth or llings, except
for cavities or leaks?”. Using those questions patients were
evaluated in the last 30 days prior to treatment using a
Likert scale consisting of ve possible answers: never; less
than once a month; between one and three days a month;
between one and three days a week; more than four
days a week. Frequent bruxism was considered when the
individual reported a frequency equal to or greater than
once a week for questions 1 or 6. When the frequency
was less than once a week, but occurring at least once a
month, it was considered as eventual bruxism.
To characterize awake bruxism four questions were applied
following the Oral Behavior Checklist
24
: (1) “Do you grind
or clench your teeth when you are awake?”; (2) “Do you
press, touch or hold your teeth when not chewing?”; (3)
“Do you hold or tense the muscles without chewing?”; (4)
“Do you press, touch or hold your teeth when you are not
chewing?”. The Likert scale was also applied to quantify
awake bruxism. Awake bruxism was considered as present
when the patient answered questions 1, 2 and/or 3 with
the statement “sometime”.
Directed acyclic graphs
Prior to data analysis, directed acyclic graphs were used to
demonstrate each of our assumptions and for statistical adjustment
(Figures 1A, 1B and 1C). The structured model, based on
information from the literature regarding possible relationships
between bruxism and migraine, included variables considered
relevant for predicting sleep bruxism and CM
25,26
(Figure 1A).
The second model considered anxiety and depression symptoms
as part of a confounding pathway between sleep bruxism and
migraine chronicity (Figure 1B). The third model shows our
assumptions for the effect of wakefulness bruxism as a factor in
the chronicity of migraine (Figure 1C). The directed acyclic graphs
were developed in DAGitty software.
38
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
Figure 1. Figures 1A and 1B: Model 1 and 2 (adjusted) for sleep
bruxism. Figure 1C: Model 3 for awake bruxism. Circles: green
- antecedent factors of bruxism; blue - antecedents of migraine
chronicity; red - factors needing adjustment; light gray: factors
not measured in this study; green with triangle - bruxism; blue
marked with I - chronic migraine; white - selection bias. Arrows:
black - causal relationship; green - effects of bruxism on migraine
chronication; red - confounding pathway that needs adjustment.
Statistical analysis
All statistical analyzes were conducted using R version
4.0.2.16. Shapiro-Wilk test and quantile-quantile graphs
were used to verify normality. Thus, sample data were
summarized as mean ± standard deviation, median
(interquartile range) and count (percentage ratio). A
multivariate logistic regression model was tted according
to each model assumption with the presence of CM as the
dependent variable to calculate the prole's odds ratio
(OR) and likelihood ratio ranges. To assess the model's
t, residual analysis, the ratio between residual deviation
and residual degrees of freedom, the Hosmer and
Lemeshow test, the Osius-Rojek test, the Stukel test and the
inuence analysis were used. Tests were performed with a
signicance level of 0.05 and the listwise exclusion method
was used to deal with missing data.
Results
254 individuals were invited to participate in the study, of
which 212 (83%) agreed. After the interview, two patients
were excluded after presenting a recent headache pattern
different from migraine. Thus, 97 patients (46%) with a
diagnosis of EM and 113 patients (54%) with CM were
included. Of the group of patients with EM, 76 did not
have aura (78%) and 21 had aura (22%). In the CM group
78 patients (69%) had analgesic abuse.
The EM and CM groups did not differ with regards to
age (p=0.187), sex (p=0.746), marital status (p=0.451),
race (p=0.167), routine physical activity (p=0.480), body
mass index (p=0.446), family income (p=0.131) and
smoking (p=0.191). Patients with EM had higher alcohol
consumption than patients with CM (p=0.020). Patients
with CM had a slightly longer duration of disease, but not
signicant (p=0.093). Analgesic abuse was higher in the
CM group (p<0.001). The degree of disability was also
higher in the CM group (MIDAS score) (p<0.001) (Table
1).
Table 1. Descriptive and comparative analysis of general clinical aspects
in the episodic and chronic migraine groups.
Variable Episodic migraine (n=97) Chronic migraine (n=113) p-value
Age (years) 38.21±12.54 40.54±12.67 0.187
Gender: female 88 (91%) 101 (89%) 0.746
Marital status: married 56 (58%) 71 (63%) 0.451
Skin color: white 79 (81%) 83 (73%) 0.167
MIDAS score 20 (39) 57 (73)
<0.001***
Migraine duration (years) 10 (14.75) 13 (18) 0.093
Analgesic abuse 24 (25%) 78 (69%)
<0.001***
Adequate physical
activity†
20 (21%) 19 (17%) 0.480
BMI (kg/m²) 25.32 (6.73) 25.49 (7.43) 0.446
Monthly household income
per resident
(Brazilian real)
2500 (2500) 1500 (1500) 0.131
Current or former smoker 3 (3%) 9 (8%) 0.191
Weekly alcohol
consumption
24 (25%) 14 (12%) 0.02*
All data are summarized as mean ± standard deviation, count (frequency,
%) or median (interquartile ratio) according to the variable type and
distribution. * p<0.050; ** p<0.010; *** p<0.001. † At least 150 minutes
of moderate-intensity or 75 minutes of vigorous-intensity aerobic physical
activity. MIDAS: Migraine Disability Assessment.
The frequency of sleep and awake bruxism was similar
in the EM and CM groups (p=0.300 and p=0.238).
Anxiety and depression scores were higher in the CM
group (p=0.012 and p=0.003, respectively). The daytime
sleepiness score was similar in the EM and CM groups
39
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
(Table 2). There was no signicant difference when
comparing the effect of the presence of isolated sleep or
awake bruxism with the absence of bruxism in patients with
CM on the MIDAS and HIT-6 scores (Table 3).
Table 2. Descriptive and comparative analysis of sleep and awake bruxism
in the episodic and chronic migraine groups.
Variable Episodic migraine (n=97) Chronic migraine (n=113) p-value
Sleep bruxism: absent 30 (31%) 29 (26%) 0.300
Sleep bruxism: eventual 25 (26%) 23 (20%) -
Sleep bruxism: frequent 42 (43%) 61 (54%) -
Awake bruxism: absent 33 (34%) 39 (35%) 0.238
Awake bruxism: eventual 46 (47%) 43 (38%)
-
Awake bruxism: frequent 18 (19%) 31 (27%) -
GAD-7 (anxiety) 8 (8) 11 (9)
0.012*
PHQ-9 (depression) 7 (7) 10 (8)
0.003**
Epworth Scale (daytime
sleepiness)
6 (7) 6 (8) 0.807
All data are summarized as count (frequency, %) or median (interquartile
ratio) according to the variable type and distribution. * p<0.050; **
p<0.010; *** p<0.001. GAD-7: Generalized Anxiety Disorder-7. PHQ-9:
Patient Health Questionnaire-9.
When compared with patients with CM without bruxism,
those with both sleep and awake bruxism had a worse
disability measured by MIDAS (p=0.003), whereas the
impact of headache by the HIT-6 scale was similar with or
without bruxism (p=0.210). However, when the HIT-6 scale
was measured at different degrees of impact, a statistically
signicant difference was found (p=0.007).
Among patients with both types of bruxism, 92.4% had
a severe headache impact score, while patients without
bruxism had a percentage of 72.7% (Table 3). For EM the
difference between the MIDAS and HIT-6 scores regarding
the absence and presence of the two types of bruxism
alone or together was not signicant.
When comparing the EM versus CM groups, regarding
the effect of sleep bruxism on MIDAS and HIT-6, no
statistical differences were found (p=0.126 and p=0.310,
respectively). Regarding the effect of awake bruxism
on MIDAS and HIT-6 the results obtained were also not
statistically different (p=0.930 and p=0.220, respectively).
In the association of both bruxisms, it was observed that the
difference was signicant regarding the effect of bruxism
on the MIDAS and HIT-6 scores being more pronounced in
the CM group (p<0.001 and p<0.001) (Table 4).
Table 3. Relationship between MIDAS and HIT-6 scores and sleep bruxism,
awake bruxism and both in the chronic migraine group.
Chronic migraine
With sleep bruxism
Without sleep
bruxism
p-value
MIDAS Grade 1 4 (25%) 5 (22.7%)
0.800
Grade 2 0 2 (9.1%)
Grade 3 2 (12.5%) 2 (9.1%)
Grade 4 10 (62.5%) 13 (59.1%)
Midas score 32,5 (8.75; 122.5) 30 (6.750; 66.5) 0.600
HIT-6 Little or no impact 0 1 (4.5%)
0.740
Moderate impact 1 (6.3%) 4 (18.2%)
Substantial impact 1 (6.3%) 1 (4.5%)
Severe impact 14 (87.5%) 16 (72.7%)
HIT-6 score 66,5 (60.75; 72) 65 (57.25; 68.75) 0.520
With awake bruxism
Without awake
bruxism
MIDAS Grade 1 1 (20%) 5 (22.7%)
0.400
Grade 2 0 2 (9.1%)
Grade 3 2 (40%) 2 (9.1%)
Grade 4 2 (40%) 13 (59.1%)
Midas score 15 (11; 76) 30 (6.75; 66.5) 0.970
HIT-6 Little or no impact 0 1 (4.5%)
1
Moderate impact 1 (20%) 4 (18.2%)
Substantial impact 0 1 (4.5%)
Severe impact 4 (80%) 16 (72.7%)
HIT-6 score 66 (66; 66) 65 (57.25; 68.75) 1
Both sleep and awake
bruxism
Without bruxism
MIDAS Grade 1 5 (7.6%) 5 (22.7%)
0.060
Grade 2 2 (3%) 2 (9.1%)
Grade 3 4 (6.1%) 2 (9.1%)
Grade 4 55 (83.3%) 13 (59.1%)
Midas score 69 (35; 101) 30 (6.75; 66.5) 0.003**
HIT-6 Little or no impact 0 1 (4.5%)
0.007**
Moderate impact 1 (1.5%) 4 (18.2%)
Substantial impact 4 (6.1%) 1 (4.5%)
Severe impact 61 (92,4%) 16 (72.7%)
HIT-6 score 66 (64; 70) 65 (57.25; 68.75) 0.210
All data are summarized as count (frequency, %) or median (interquartile
ratio) according to the variable type and distribution. * p<0.050; **
p<0.010; *** p<0.001. MIDAS: Migraine Disability Assessment. HIT-6:
Headache Impact Test.
40
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
Table 4. Relationship between MIDAS and HIT-6 scores and sleep bruxism,
awake bruxism and both in episodic migraine versus chronic migraine.
Episodic migraine Chronic migraine
p-value
With sleep bruxism With sleep bruxism
MIDAS
Grade 1 3 (33.3%) 4 (25%)
0.048*
Grade 2 3 (33.3%) 0
Grade 3 1 (11.1%) 2 (12.5%)
Grade 4 2 (22.2%) 10 (62.5%)
Midas score 7 (5; 17) 32,5 (8.75; 122.5) 0.126
HIT-6
Little or no impact 0 0
0.460
Moderate impact 2 (22.2%) 1 (6.3%)
Substantial impact 1 (11.1%) 1 (6.3%)
Severe impact 6 (66.7%) 14 (87.5%)
HIT-6 score 66 (59; 67) 66,5 (60.75; 72) 0.310
With awake bruxism
With awake
bruxism
MIDAS
Grade 1 2 (28.6%) 1 (20%)
1
Grade 2 1 (14.3%) 0
Grade 3 1 (14.3%) 2 (40%)
Grade 4 3 (42.9%) 2 (40%)
Midas score 15 (6; 37) 15 (11; 76) 0.930
HIT-6
Little or no impact 0 0
2
Moderate impact 2 (28.6%) 1 (20%)
Substantial impact 1 (14.3%) 0
Severe impact 4 (57.1%) 4 (80%)
HIT-6 score 62 (55; 64) 66 (66; 66) 0.220
Both sleep and awake
bruxism
Both sleep and
awake bruxism
MIDAS
Grade 1 9 (16.7%) 5 (7.6%)
0.002**
Grade 2 7 (13%) 2 (3%)
Grade 3 10 (18.5%) 4 (6.1%)
Grade 4 28 (51.9%) 55 (83.3%)
Midas score 22,5 (10; 58) 69 (35; 101) <0.001***
HIT-6
Little or no impact 3 (5.6%) 0
0.020*
Moderate impact 5 (9.3%) 1 (1.5%)
Substantial impact 6 (11.1%) 4 (6.1%)
Severe impact 40 (74.1%) 61 (92.4%)
HIT-6 score 63 (59.25; 66.75) 66 (64; 70) <0.001***
All data are summarized as count (frequency, %) or median (interquartile
ratio) according to the variable type and distribution. * p<0.050; **
p<0.010; *** p<0.001. MIDAS: Migraine Disability Assessment. HIT-6:
Headache Impact Test.
For patients with both types of bruxism, a difference was
found in the MIDAS classications between patients in
the two groups (EM and CM), and for patients with CM,
83.3% were classied as 4, while for EM this proportion
was of 51.9% (p=0.002). A statistical difference was also
found between the categories of the HIT-6 questionnaire,
with the CM group having 92.4% of patients classied as
severe impact, while for patients with EM this proportion
was 74.1% (p=0.020) (Table 4).
Using multivariate logistic regression to estimate the effect
of bruxism on migraine, four scenarios were separated,
according to the adjustment of the variables, but there was
no difference in the prevalence of bruxism between the EM
and CM groups (Table 5).
Table 5. Multivariate logistic regression models for estimating the effect
of bruxism on migraine.
Model Comparison OR 95% CI
Not adjusted Sleep bruxism: absent Ref. -
Sleep bruxism: eventual 0.95 0.440-2.040
Sleep bruxism: frequent 1.50 0.790-2.870
Model 1 Sleep bruxism: absent Ref. -
Sleep bruxism: eventual 1.17 0.520-2.680
Sleep bruxism: frequent 1.50 0.750-3.000
Model 2 Sleep bruxism: absent Ref. -
Sleep bruxism: eventual 1.15 0.500-2.650
Sleep bruxism: frequent 1.35 0.660-2.750
Model 3 Awake bruxism: absent Ref. -
Awake bruxism: eventual 0.77 0.390-1.520
Awake bruxism: frequent 1.33 0.580-3.060
Odds ratio for chronic migraine to cause more bruxism in different models
for those with sleep bruxism (models 1 and 2) and awake bruxism (model
3). Model 1 was adjusted for age, use of preventive medication for migraine
and selection method. Model 2 added adjustments for anxiety and
depression symptoms. Model 3 was adjusted for age, anxiety symptoms,
use of preventive medication for migraine and selection method. OR: Odds
ratio. CI: Condence interval. Ref.: reference level.
Discussion
We have observed in the literature that patients with EM
and CM have an increased prevalence of sleep bruxism
and awake bruxism.
14,16
No previous study aimed to assess
the risk that sleep and/or awake bruxism could cause
in the process of chronication of migraine. However, a
study carried out in Brazil showed that the association of
sleep bruxism with migraine was signicant although only
in the chronic form, with no signicant association in the
episodic form of the disease.
15
However, data from our
study did not support sleep or awake bruxism as being
more prevalent in CM when compared to EM, which could
indicate that there is no relationship between bruxism
and migraine chronicity. However when sleep and awake
bruxism presented concomitally we observed greater
impact and disability on individuals with CM.
As demonstrated by the results of this study, CM is a
disease with greater debilitating power than the episodic
form. This disease brings together patients from different
groups of individuals, as it has in common a headache
pattern typical of migraine, but at the same time they have
41
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
symptoms that are not related to headache and that can
identied as comorbidities. The CaMEO study was perhaps
one of the most important efforts to identify and classify
patients with CM into different groups based on their other
associated clinical characteristics (comorbidities).
27
In this
study, according to the group of symptoms (comorbidities),
patients were subdivided into eight classes: Class 1 –
Multimorbidities (several associated comorbidities); Class
2 – Respiratory and Psychiatric Comorbidities; Class 3 –
Respiratory and other pains (eg bromyalgia); Class 4
Respiratory; Class 5 – Psychiatric; Class 6 – Cardiovascular;
Class 7 – Pain; Class 8 – Few Comorbidities.
This classication allowed a risk stratication for the
evolution of EM to CM. Thus, patients with Class 1 have
an annual risk of 5.34 times higher to undergo migraine
chronication. On the other hand, patients with only one
comorbidity have a 1.53 times greater risk of suffering
this transformation than migraine individuals without
comorbidities.
28
In these studies, awake and/or sleep
bruxism were not evaluated as a factor in the evolution of
EM to CM.
Another fact from these studies was that the assessment
of the impact of migraine using the MIDAS scales proved
to be effective as a prognostic factor of chronication,
which when high inuences any of the reported classes of
comorbidities.
27,28
In the present study, it was observed that
individuals with sleep and awake bruxism at the same time
have a higher degree of migraine disability. Given these
data, we can assume that bruxism could collaborate with
the degree of disability in CM.
The disability caused by migraine does not fully explain the
association between the comorbidity classes and the risk of
progression to the chronic form, demonstrating that multiple
comorbidities may play a role in this transformation process
but only a higher degree of disability alone would not justify
the transformation from EM to CM.
28
There is, therefore,
the need for an aggregating factor of transformation, as
may have been the case with the presence of both types
of bruxism. A 10-point increase in disability (MIDAS) is
believed to have the power to transform EM in CM by 1.11
times, 20 points 1.22 times, and 40 points 1.49 times.
28
An European study evaluated the correlation of the impact
of headache (HIT-6) with sleep bruxism diagnosed by
polysomnography. It has been shown that the relationship
between sleep bruxism and the impact of headache on the
patient's life is only modest, being altered only in patients
with phasic bruxism and is associated with the moment
of awakening.
29
In our study, however, we did not nd
signicant relevance of the effect of isolated sleep bruxism
on the degree of impact of headache in patients with EM
and CM. However, there was a positive association of a
higher headache impact score in patients with CM who
had both sleep and awake bruxism. In the literature, there
are no reports of similar studies that trace the relationship
of the impact of headache (HIT-6) with the chronicity of
migraine, as well as whether bruxism would have any
inuence on it. In other words, analyzing these data
together, it is possible to show that patients affected by
both forms of bruxism could have repercussions on the
severity of CM when assessed by the degree of impact of
the headache.
A limitation found in our study was that the diagnosis of
bruxism is only classied as possible, as it was based on
self-report, without clinical evaluation and complementary
tests which are necessary for a probable and denitive
diagnosis.
8
A healthy control group was also not formed
to be used in the comparisons. Future studies using
longitudinal and controlled methodology would be useful
to elucidate the inuences of sleep and awake bruxism on
both forms of migraine.
Conclusion
In conclusion, sleep or awake bruxism alone are not more
prevalent in CM when compared to EM. We observed,
however, that bruxism causes greater impact and disability
on individuals with CM and thus could participate as a
cofactor in the process of migraine chronication.
Conflict of Interest: There is no conict of interest to declare.
Funding: This study was nanced in part by the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) – Finance
Code 001 (grant number 88887.465414/2019-00). This work was
sponsored by Allergan (grant number PG-2020-10985). The funders had
no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Authors’ contributions: All authors contributed equally to this work.
Keryn Sporh Godk
https://orcid.org/0000-0003-3231-6061
Maria Luiza dos Santos
https://orcid.org/0000-0001-7745-8739
Marco Antonio Takashi Utiumi
https://orcid.org/0000-0001-5273-6798
João Guilherme Bochnia Küster
https://orcid.org/0000-0002-1828-2726
Luiz Carlos Canalli Filho
https://orcid.org/0000-0001-5438-2823
42
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
Nikolai José Eustátios Kotsifas
https://orcid.org/0000-0003-4735-1812
Bin Cheng Tan
https://orcid.org/0000-0003-0812-7906
Eldislei Mioto
https://orcid.org/0000-0001-5376-9292
Gabriel Eduardo Faria Colombani
https://orcid.org/0000-0003-2774-5152
Elcio Juliato Piovesan
https://orcid.org/0000-0002-0915-0430
References
1. Brandes JL. Migraine and functional impairment.
CNS Drugs
2009;23(12):1039-1045 Doi:
10.2165/11530030-000000000-00000
2. Queiroz LP, Peres MF, Piovesan EJ, Kowacs F, Ciciarelli
MC, Souza JA and Zukerman E. A nationwide population-
based study of migraine in Brazil.
Cephalalgia
2009;29(6):642-649 Doi: 10.1111/j.1468-
2982.2008.01782.x
3. Headache Classication Committee of the International
Headache Society (IHS) The International Classification
of Headache Disorders, 3rd edition.
Cephalalgia
2018;38(1):1-211 Doi: 10.1177/0333102417738202
4. Ribeiro FAM, Anderle F, Grassi V, Barea LM, Stelzer FG
and Reppold CRJRBdNeP. Avaliação Neuropsicológica
em Pacientes com Enxaqueca Episódica e Enxaqueca
Crônica/Cefaleia Associada ao uso Excessivo de
Analgésicos. 2017;21(1):17-32
5. Giacomozzi AR, Vindas AP, Silva AA, Jr., Bordini
CA, Buonanotte CF, Roesler CA, . . . Filho PF. Latin
American consensus on guidelines for chronic migraine
treatment.
Arq Neuropsiquiatr
2013;71(7):478-486
Doi: 10.1590/0004-282x20130066
6. Lantéri-Minet M, Duru G, Mudge M and Cottrell S.
Quality of life impairment, disability and economic
burden associated with chronic daily headache, focusing
on chronic migraine with or without medication overuse:
a systematic review.
Cephalalgia
2011;31(7):837-850
Doi: 10.1177/0333102411398400
7. Sateia MJ. International Classification of Sleep Disorders-
Third Edition.
Chest
2014;146(5):1387-1394 Doi:
10.1378/chest.14-0970
8. Lobbezoo F, Ahlberg J, Raphael KG, Wetselaar P, Glaros
AG, Kato T, . . . Manfredini D. International consensus on
the assessment of bruxism: Report of a work in progress.
J Oral Rehabil
2018;45(11):837-844 Doi: 10.1111/
joor.12663
9. Lobbezoo F, Ahlberg J, Glaros AG, Kato T, Koyano K,
Lavigne GJ, . . . Winocur E. Bruxism defined and graded:
an international consensus.
J Oral Rehabil
2013;40(1):2-
4 Doi: 10.1111/joor.12011
10. Ella B, Ghorayeb I, Burbaud P and Guehl D. Bruxism
in Movement Disorders: A Comprehensive Review.
J Prosthodont
2017;26(7):599-605 Doi: 10.1111/
jopr.12479
11. Lavigne GJ, Khoury S, Abe S, Yamaguchi T and Raphael
K. Bruxism physiology and pathology: an overview
for clinicians.
J Oral Rehabil
2008;35(7):476-494 Doi:
10.1111/j.1365-2842.2008.01881.x
12. Wieckiewicz M, Paradowska-Stolarz A and Wieckiewicz
W. Psychosocial aspects of bruxism: the most paramount
factor influencing teeth grinding.
Biomed Res Int
2014;469187 Doi: 10.1155/2014/469187
13. Manfredini D. The Triangle Bruxism, Pain, and
Psychosocial Factors.
Academic Centre for Dentistry
Amsterdam (ACTA)
, Amsterdam, The Netherlands; 2021
14. Costa AL, D'Abreu A and Cendes F. Temporomandibular
joint internal derangement: association with headache,
joint effusion, bruxism, and joint pain.
J Contemp Dent
Pract
2008;9(6):9-16
15. Fernandes G, Franco AL, Gonçalves DA, Speciali JG,
Bigal ME and Camparis CM. Temporomandibular
disorders, sleep bruxism, and primary headaches are
mutually associated.
J Orofac Pain
2013;27(1):14-20
Doi: 10.11607/jop.921
16. De Luca Canto G, Singh V, Bigal ME, Major PW and
Flores-Mir C. Association between tension-type headache
and migraine with sleep bruxism: a systematic review.
Headache
2014;54(9):1460-1469 Doi: 10.1111/
head.12446
17. Organization WH. Global Recommendations on
Physical Activity for Health. 2010;60p
18. Kroenke K, Spitzer RL and Williams JB. The PHQ-9:
validity of a brief depression severity measure.
J Gen
Intern Med
2001;16(9):606-613 Doi: 10.1046/j.1525-
1497.2001.016009606.x
19. Spitzer RL, Kroenke K, Williams JB and Löwe B. A brief
measure for assessing generalized anxiety disorder: the
GAD-7.
Arch Intern Med
2006;166(10):1092-1097 Doi:
https://www.doi.org/10.1001/archinte.166.10.1092
20. Bertolazi AN, Fagondes SC, Hoff LS, Pedro VD, Menna
Barreto SS and Johns MW. Portuguese-language
version of the Epworth sleepiness scale: validation for
use in Brazil.
J Bras Pneumol
2009;35(9):877-883 Doi:
10.1590/s1806-37132009000900009
21. Fragoso YD. MIDAS (Migraine Disability Assessment): a
valuable tool for work-site identification of migraine in
workers in Brazil.
Sao Paulo Med J
2002;120(4):118-
121 Doi: 10.1590/s1516-31802002000400006
22. Martin M, Blaisdell B, Kwong JW and Bjorner JB.
The Short-Form Headache Impact Test (HIT-6) was
43
ASAA
Godk KS, Santos ML, Utiumi MAT, Küster JGB, Canalli Filho LC, Kotsifas NJE, Tan BC, Mioto E, Colombani GEF, Piovesan EJ
Association between sleep and awake bruxism in patients with migraine
psychometrically equivalent in nine languages.
J Clin
Epidemiol
2004;57(12):1271-1278 Doi: 10.1016/j.
jclinepi.2004.05.004
23. Sateia MJ. International classification of sleep disorders-
third edition: highlights and modifications.
Chest
2014;146(5):1387-1394 Doi: 10.1378/chest.14-0970
24. Markiewicz MR, Ohrbach R and McCall WD, Jr. Oral
behaviors checklist: reliability of performance in targeted
waking-state behaviors.
J Orofac Pain
2006;20(4):306-
316
25. Castroorio T, Bargellini A, Rossini G, Cugliari G
and Deregibus A. Sleep bruxism and related risk
factors in adults: A systematic literature review.
Arch Oral Biol
2017;83(1)25-32 Doi: 10.1016/j.
archoralbio.2017.07.002
26. Probyn K, Bowers H, Caldwell F, Mistry D, Underwood
M, Matharu M and Pincus T. Prognostic factors for chronic
headache: A systematic review.
Neurology
2017;89(3):291-
301 Doi: 10.1212/wnl.0000000000004112
27. Lipton RB, Fanning KM, Buse DC, Martin VT, Reed
ML, Manack Adams A and Goadsby PJ. Identifying
Natural Subgroups of Migraine Based on Comorbidity
and Concomitant Condition Profiles: Results of the
Chronic Migraine Epidemiology and Outcomes (CaMEO)
Study.
Headache
2018;58(7):933-947 Doi: 10.1111/
head.13342
28. Lipton RB, Fanning KM, Buse DC, Martin VT,
Hohaia LB, Adams AM, . . . Goadsby PJ. Migraine
progression in subgroups of migraine based on
comorbidities: Results of the CaMEO Study.
Neurology
2019;93(24):e2224-e2236 Doi: 10.1212/
wnl.0000000000008589
29. Martynowicz H, Smardz J, Michalek-Zrabkowska M,
Gac P, Poreba R, Wojakowska A, . . . Wieckiewicz
M. Evaluation of Relationship Between Sleep Bruxism
and Headache Impact Test-6 (HIT-6) Scores: A
Polysomnographic Study.
Front Neurol
2019;10(487
Doi: 10.3389/fneur.2019.00487