Association between temporomandibular disorders and obesity

Association between temporomandibular disorders and obesity

Accepted Manuscript Association between temporomandibular disorders and obesity Eunmi Rhim, Kyungdo Han, Kyoung-In Yun PII: S1010-5182(16)30025-7 DO...

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Accepted Manuscript Association between temporomandibular disorders and obesity Eunmi Rhim, Kyungdo Han, Kyoung-In Yun PII:

S1010-5182(16)30025-7

DOI:

10.1016/j.jcms.2016.04.016

Reference:

YJCMS 2342

To appear in:

Journal of Cranio-Maxillo-Facial Surgery

Received Date: 13 January 2016 Revised Date:

8 March 2016

Accepted Date: 12 April 2016

Please cite this article as: Rhim E, Han K, Yun K-I, Association between temporomandibular disorders and obesity, Journal of Cranio-Maxillofacial Surgery (2016), doi: 10.1016/j.jcms.2016.04.016. 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.

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Association between temporomandibular disorders and obesity Eunmi Rhima, Kyungdo Hanb, Kyoung-In Yunc, * a

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Department of Conservative Dentistry and Endodontics, The Catholic University of Korea, Yeouido St. Mary’s Hospital, Seoul, Korea b Department of Biostatistics, The Catholic University of Korea, College of Medicine, Seoul, Korea c Department of Oral and Maxillofacial Surgery, The Catholic University of Korea, Yeouido St. Mary’s Hospital, Seoul, Korea *

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Corresponding Author. Department of Oral and Maxillofacial Surgery, The Catholic University of Korea, Yeouido St. Mary’s Hospital, Seoul, Korea. E-mail address: [email protected] (K.-I. Yun).

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Abstract Psychological stress can induce altered eating patterns, and studies have indicated that there is a correlation

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between temporomandibular disorder (TMD) and psychological stress. This study investigated the relationship between TMD and body mass index (BMI) in a large representative sample of the South Korean population using data from the Korea National Health and Nutrition Examination Survey (KNHANES). en and women with TMD showed decreased prevalence of abdominal obesity. Women with TMD had lower age, lower BMI,

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lower metabolic syndromic waist circumference, lower prevalence of metabolic syndrome, and lower prevalence of diabetes compared with the group without TMD. However, in male subjects, there was no

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statistically significant difference between BMI, metabolic syndromic waist circumference, or TMD, although there were similar tendencies in the male and female subject groups. Overall, TMD was associated with

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decreased BMI and abdominal obesity in women.

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Introduction Temporomandibular disorder (TMD) is defined as a set of clinical conditions characterized by pain and

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dysfunction of the masticatory muscles, TMJ, and associated hard and soft tissues [1]. Common symptoms include pain, limitation in jaw function, and clicking jaw sounds. Possible risk factors that contribute to TMJ are parafunction and psychological stress [2]. In comparison, TMD is also considered as a causative or intensifying factor in the development of anxiety and depression [2].

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Psychological stress induces altered eating patterns [3]. During stressful periods, some study subject ate highcalorie comfort foods and gained weight, whereas others ate less and lost weight [4, 5]. Body mass index (BMI)

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is used to identify possible weight problems, and previous studies have evaluated the effects of stress on eating behavior and BMI [5, 6]. However, there is little evidence on the relationship between TMD and BMI. The aim of this study were was to investigate the relationship between TMD and BMI in a large representative sample of the South Korean population using data from the Korea National Health and Nutrition Examination Survey (KNHANES).

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Survey Overview

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Materials and Methods

The present study was performed with data from the Fifth Korean National Health and Nutrition Examination Survey (KNHANES V), which was carried out from 2010 to 2012. The KNHANES was first performed as a

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nationwide survey in 1998 by the Division of Chronic Disease Surveillance at the Korean Center of Disease Control and Prevention [7]. It is a nationwide study of non-institutionalized civilians and uses a stratified and multistage probability sampling design with a rolling survey-sampling model. The sampling units were based on the population and housing consensus from the 2005 National Census Registry in Korea, which includes age, sex, and geographic area. A total of 25,533 KNHANES V participants had sufficient data available for inclusion in the present study. The KNHANES V was approved by the Institutional Review Board for Human Subjects of the Korea Center for Disease Control and Prevention. Each participant in the survey signed an informed consent form. Overall 2

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response rate was 81.9% in 2010, 80.4% in 2011, and 80.0% in 2012. There were 19,851 subjects who participated in the pain and/or discomfort questionnaire and 17,313 respondents for the TMD symptom questionnaire. Exclusion criteria were two-fold: (1) those aged < 12 years and (2) those with missing values in

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the health assessment or questionnaires. The final sample size for this study was 11,922 (5,120 males and 6,802 females, 46.7% of all participants in KNHANES V).

The survey was composed of three parts: a health interview survey, a health examination survey, and a nutrition survey. Trained interviewers conducted face-to-face interviews with a structured questionnaire.

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Physical examinations, blood sampling, and urine sampling were performed at a mobile examination center. All data used in the present study are available in public-use files provided by the Korea Centers for Disease

Demographic Variables

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Control and Prevention and the Ministry of Health and Welfare of Korea.

Demographic variables were sex, age, education level, alcohol intake, income, and smoking status according to author’s previous papers.

Education level was categorized into four groups: less than primary school, middle school, high school, and

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college or higher. The education level was classified as low if the respondent did not finish education beyond middle school.

Monthly household income was adjusted for the number of household members and was categorized into four

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groups: < 25%, 25% to 49%, 50% to 75%, and > 75% of the total equivalized income in the survey. Individuals with household incomes in the lowest quartile were classified as the low-income group. The amount of pure alcohol consumed (in grams per day) was calculated using the average number of

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alcoholic beverages consumed and the frequency of alcohol consumption. Alcohol consumption status was classified into three groups: nondrinker, mild-to-moderate drinker (< 30.0 g alcohol/day), and heavy drinker (≥ 30.0 g alcohol/day). High-risk drinker was designated as drinking > 60.0g alcohol/day for male and > 40.0g/day for female subjects.

Smoking status was categorized into three groups: non-smokers (i.e., those who had never smoked or who had smoked fewer than 100 cigarettes in their lifetime), current smokers (i.e., those who were currently smoking and who had smoked 100 or more cigarettes in their lifetime), and ex-smokers (i.e., those who had smoked in the past but had ceased smoking). 3

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Regular exercise was defined as strenuous physical activity performed for at least 20 minutes at a time at least three times a week [8].

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Descriptions of Metabolic Syndrome, Diabetes, and Hypertension Metabolic syndrome was defined according to the American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement criteria for Asians [9]. To be diagnosed with metabolic syndrome, ≥ 3 of the following criteria must be fulfilled: 1) waist circumference ≥ 90 cm in men or ≥ 80 cm in women; 2) fasting TG

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≥ 150 mg/dL or use of lipid-lowering medication; 3) HDL-C < 40 mg/dL in men or < 50 mg/dL in women or use of cholesterol-lowering medication; 4) blood pressure ≥ 130/85 mm Hg or use of antihypertensive

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medication; and 5) FBG ≥ 100 mg/dL or current use of anti-diabetic medication [10].

Diabetes was diagnosed when fasting blood sugar was > 126 mg/dL or when the individual was currently using anti-diabetic medication [11].

Hypertension was defined as systolic blood pressure > 160 mm Hg, diastolic blood pressure > 90 mmHg, or current use of systemic antihypertensive drugs [12].

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Anthropometric Measurements

Measurements were obtained by trained staff members in the Division of Chronic Disease Surveillance under the Korea Centers for Disease Control and Prevention and the Korean Ministry of Health and Welfare. Body

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weight and height were measured to the nearest 0.1 kg and 0.1 cm, respectively, with the participants in light indoor clothing without shoes [13].

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Waist circumference was measured at the narrowest point between the lower border of the rib cage and the iliac crest. The waist circumference cut-off point was defined as ≥ 90cm in men and ≥ 80cm in women. BMI was calculated as weight in kg divided by height in m2. The BMI cut-off point was 23 kg/m2 for overweight and 25 kg/m2 for obesity [14]. A standard mercury sphygmomanometer was used to measure systolic blood pressure and diastolic blood pressure on the right arm. Systolic blood pressure and diastolic blood pressure measurements were performed twice at 5-minute intervals; the average values were used for the analysis.

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TMD Assessment All TMD examinations were performed by dentists. To assess TMD, the following criteria of the World Health

(1) Clicking of one or both temporomandibular joints (TMJ),

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Organization (WHO) were used [15]:

(2) tenderness (on palpation) of the anterior temporalis and/or masseter muscles on one or both sides,

(3) reduced jaw mobility-opening of < 30 mm. Clicking was evaluated directly by an audible sharp sound or by palpation of the TMJ.

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Tenderness was evaluated by unilateral palpation with firm pressure of two fingers, exerted twice on the most voluminous part of the muscle. Tenderness was recorded only if the palpation spontaneously provoked an

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avoidance reflex.

Reduced jaw mobility was determined by measuring the distance between the incisal tips of the central maxillary and mandibular incisors. As a general guide, mobility was considered to be reduced if the subject was unable to open his or her jaw to the width of two fingers.

TMD was determined to be present if the subject reported having at least one of the following signs: clicking,

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tenderness (on palpation), or reduced jaw mobility (opening < 30 mm) once or more per week.

Statistical Analyses

All data are presented as mean ± SE or percentage (SE). If necessary, logarithmic transformation was performed

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to achieve a normal distribution. Statistical analyses were performed using the survey procedure of the statistical software package to account for the complex sampling design. P values < 0.05 were considered statistically

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significant. Student’s t-test or one-way analysis of variance was used to investigate the differences in presence of TMD, according to the variables. Univariate and multivariate logistic regression analyses were used to assess the associations of TMD with BMI and its individual components. Odds ratios (ORs) and 95% confidence intervals (CIs) were estimated after adjustment for potential confounders. In multivariate analyses of the prevalence of smoking, drinking, regular physical exercise, income, and education, adjustments were first made for age (model 1). Adjustments were then made for the same variables as model 1 plus smoking, drinking, regular physical exercise, income, and education (model 2). In addition, adjustments were made for the variables in model 2 plus mental stress, tooth brushing (times per day), and professional oral examination within 1 year 5

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(model 3). The SAS software package version 9.2 for Windows (SAS Institute Inc., Cary, NC, USA) was used to account for the complex sampling design and to provide approximations of the entire Korean population. P <

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0.05 was considered statistically significant.

Results

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A total of 11,922 subjects were included in this study. The males and females with TMD were found to have lower age, education, and metabolic syndrome but higher mental stress compared with the group without TMD (Table 1). Females with TMD had lower age, BMI, metabolic syndromic waist circumference, prevalence of

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metabolic syndrome, and prevalence of diabetes compared with the group without TMD (Table 1). Table 1 shows the higher prevalence of heavy drinking in females with TMD.

Table 2 shows adjusted ORs and their 95% CIs from multiple logistic regression analyses controlling for age in model 1; age, smoking, drinking, exercise, income, and education in model 2; and age, smoking, drinking, exercise, income, education, mental stress, number of times of tooth brushing per day, and professional oral

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examination within 1 year in model 3.

In females, BMI, metabolic syndromic waist circumference, and TMD showed statistically significant correlations after adjustment ( Table 2). Adjusted ORs and their 95% CIs in females were 1.477 (1.117 to 1.953), 1.438 (1.08 to 1.916), and 1.446 (1.085 to 1.926) for < 23 kg/m2 (models 1, 2, and 3, respectively). Adjusted

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ORs and their 95% CIs in females were 1.159 (0.808 to 1.661), 1.176 (0.810 to 1.707), and 1.199 (0.828 to 1.738) for 23 kg/m2 ≤ females < 25 kg/m2 (models 1, 2, and 3). Adjusted ORs and their 95% CIs in females were

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1.341 (1.037 to 1.735), 1.359 (1.047 to 1.764), and 1.350 (1.042 to 1.748) for metabolic syndromic waist circumference (models 1, 2, and 3). However, there were no significant relationships between BMI, metabolic syndromic waist circumference, or TMD in any of the male subject models.

Discussion

This study assessed the association between TMD and obesity in the nationally representative sample of the Korean population. The results of this study indicate that TMD is negatively correlated with BMI, metabolic syndromic waist circumference, and abdominal obesity in women. Men with TMD also showed lower BMI and 6

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metabolic syndromic waist circumference, although this result was not statistically significant. To the best of our knowledge, this is the first study to examine the relationship between TMD and obesity in the general population.

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The association between TMD and obesity remains controversial; some reports have indicated that there is a significant association between TMD and low body weight in institutionalized children 6 to 13 years old [16]. Those authors suggested that eating habits may influence BMI and contribute to development of TMD. Another author reported that TMD or muscular disorder was associated with subjects that were overweight in a twin

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study [17]. However, the relationship between TMD or muscular disorder and overweight subjects was no longer significant after adjusting for age, gender, and depression [17]. This study showed that TMD was

smoking, drinking, exercise, and mental stress.

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negatively correlated with BMI and metabolic syndromic waist circumference in women after adjusting for age,

There are several possible explanations for the association between obesity and TMD. The first possibility is abnormal eating behavior in obese subjects. A number of studies have reported that types of food affect the prevalence or severity of TMD. Obese subjects often show abnormal eating behavior such as avoiding hard food [18], high intake of soft fatty food [19, 20], and chewing less [19]. Dietary intake of hard food is negatively

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associated with increasing waist circumference [21]. A higher intake of fiber was seen in healthy adults [22]. Mean weight loss was greater in a low-fat and high-fiber diet group [23]. Decreased bite force may have contributed to lower BMI in the TMD group. It has been reported that bite force in the TMD group is significantly lower in the healthy group [24-26]. There was a four-fold increase in

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functional problems, such as chewing difficulty, compared with the non-pain population [27]. The patients with TMD reported difficulty eating some foods such as meat and apples because of pain [28].

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Mental stress may also be related to lower BMI in the TMD group. This study showed that the subjective mental stress rate was higher in the TMD group. Sucrose preference was reduced after chronic mild stress but reversed after anti-depressant treatment [29]. The stressor significantly delayed the glucose response in the normal-weight subjects but did not affect the glucose response in obese subjects [30, 31]. Psychological stress delays gastrointestinal transit time in normal-weight subjects, and the magnitude of the delay in gastrointestinal transit time is significantly correlated with the delay in peak glucose response [31]. The relationship among BMI, waist circumference, and TMD differed based on gender in the present study. Sex is an important factor related to sensitivity to stress and several mental disorders, such as depression and

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anxiety disorders [32-34]. Gender differences in stress reactivity may be caused by gender-specific neural activation underlying the central stress response [34]. Female sex hormones could lead to delayed cortisol feedback in the brain and reduced or delayed containment of the stress response [34]. Compromised cortisol

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feedback effects on hypothalamic-pituitary-adrenal (HPA) axis have been proposed as a major neurobiological pathway to the development of depression in females [35]. The HPA axis is also involved in cortisol secretion, and cortisol induces appetite. Subjective appetite (desire to eat) in women was lower than that in men because of reduced cortisol level in women compared to men, despite increased stress [36]. This study showed that women

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with TMD brushed their teeth more frequently and visited the dental hospital to check their oral health states compared with the non-TMD group. This result may reflect a higher anxiety level in the TMD group. There were some limitations to this study. First, this survey was conducted in only one Asian country.

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Therefore, it is hard to generalize this result. Second, this was a cross-sectional study. Therefore, it is impossible to show a causal relationship between obesity and TMD.

Despite these limitations, the main strength of the present study lies in the nationally representative sample of Koreans with sufficient power for investigation of these relationships. It also has important implications for the relationship between TMD and obesity.

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In conclusion, TMD was associated with decreased BMI and abdominal obesity in women. In contrast, BMI was not associated with TMD in male subjects. Further prospective studies are needed to determine the causal

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relationship and mechanism between TMD and obesity.

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Table 1. Characteristics of the Study Population (mean ± SE) Male TMD

Age (years)

(n=4,837) 45.1±0.4

(n=283) 34.6±0.8

BMI (kg/m2)

24.0±0.1

Waist circumference (cm) Eversmoker High-risk drinker

1

Non-TMD

TMD

<.0001*

(n=6,272) 47.4±0.3

(n=530) 36.8±0.8

<.0001*

23.9±0.3

0.569

23.3±0.1

22.1±0.2

<.0001*

84.3±0.2

83.2±0.7

0.115

78.2±0.2

74.4±0.5

<.0001*

73.9±0.9

66.6±3.7

0.047

8.60±0.5

11.7±1.8

0.054

18.8±0.8

23.0±3.0

0.153

1.70±0.2

4.00±1.3

0.021*

0.244

17.6±0.7

17.5±2.0

0.963

p

p

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Non-TMD

Female

27.7±3.4

14.8±0.7

11.5±2.4

0.206

19.8±0.7

10.6±1.6

<.0001*

Education (below high school)

76.1±0.9

90.4±1.9

<.0001*

62.0±1.1

82.6±2.0

<.0001*

Mental stress (yes, %)

24.4±0.8

37.8±3.6

<.0001*

Income (lower)

16.5±0.7

9.10±2.0

twice

50.3±1.0

52.1±3.8

33.2±0.9

three times or more Professional oral examination within 1 year (%) BMI level (%)

24.5±0.9

38.8±3.6

23.9±3.2

38.5±0.8

46.5±0.8

41.3±2.6

44.3±1.0

53.5±2.6

0.487

22.6±0.9

30.1±2.4

25.7±0.8

< 25

35.9±0.9

0.001* 0.001*

<.0001* <.0001*

43.9±3.5

50.4±0.8

66.7±2.4

23.1±3.1

21.0±0.6

15.5±1.9

33.0±3.5

28.6±0.7

17.8±1.9

26.2±0.9

20.8±3.0

0.100

41.0±0.9

24.3±2.2

<.0001*

27.3±0.8

17.7±2.8

0.004*

25.9±0.7

11.6±1.7

<.0001*

10.1±0.5

6.10±1.9

0.082

7.70±0.4

3.00±0.8

0.000

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1

5.20±1.2

0.340

< 23

DM (%)

38.3±2.6

9.20±0.6

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once or less

≥ 25 Metabolic syndromic waist circumference (%)3 Metabolic syndrome (%)

29.9±0.8

0.021

Tooth brushing (times per day)

23≤

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23.9±0.8 2

Exercise (yes)

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High-risk drinker means drinking > 60 g pure alcohol per drinking day for men and > 40 g per drinking day for women; Lower income means < 25% of the total equivalized income; 3 Metabolic syndromic waist circumstance means ≥ 90 cm in men and ≥ 80 cm in women *: p< 0.05 2

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Table 2. Adjusted OR (95% CI) of TMD in Multivariate Logistic Regression Model Male Female OR (95% CI)

p

OR (95% CI)

0.8038

1.159 (0.808 to 1.661)

p

Model 1 BMI level 23≤

1.120 (0.779 to 1.61) < 25

1.026 (0.674 to 1.563)

≥ 25

1.477 (1.117 to 1.953)

1

1

0.5568

Model 2 BMI level 23≤

1.052 (0.707 to 1.564) < 25

0.928 (0.592 to 1.453)

≥ 25

1

Waist circumference Non-metabolic

0.984 (0.668 to 1.448)

Metabolic

1

BMI level < 23 23≤

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Model 3

≥ 25 Waist circumference

0.8495

0.9337

0.996 (0.672 to 1.477)

Metabolic

1

1.176 (0.810 to 1.707)

0.0375*

1

1.359 (1.047 to 1.764) 1

0.0211*

1.446 (1.085 to 1.926) 0.7836

1

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Non-metabolic

0.919 (0.586 to 1.439)

0.0252*

1.438 (1.080 to 1.916)

1.071 (0.717 to 1.601)

< 25

1

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< 23

1.341 (1.037 to 1.735)

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1.115 (0.776 to 1.603)

Metabolic

0.0173*

1

Waist circumference Non-metabolic

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< 23

1.199 (0.828 to 1.738)

0.0368*

1

0.9844

1.350 (1.042 to 1.748) 1

0.0229*

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Model 1 was adjusted for age Model 2 was adjusted for age, smoke, drink, exercise, income, and education Model 3 was adjusted for age, smoke, drink, exercise, income, education, mental stress, tooth brushing times per day, and professional oral examination within 1 year. * : p< 0.05

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Highlights

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Relationship between temporomandibular disorder (TMD) and body mass index (BMI) was assessed.

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Women with TMD had lower BMI, lower waist circumference, and lower prevalence of metabolic syndrome.

TMD was associated with decreased BMI and abdominal obesity in women.

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