Longitudinal Associations of Toothbrushing With Obesity and Hyperglycemia

Background Toothbrushing is a health-related lifestyle habit and has been reported to contribute not only to oral health but also to some parameters of general health; however, little research has been conducted to understand the association of the frequency and timing of toothbrushing with the development of comprehensive metabolic abnormalities, with consideration of oral health condition. In this study, using longitudinal data, we examined this association in Japanese adults, adjusting for periodontal condition. Methods A 5-year longitudinal study was performed with 4,537 participants between 35 and 64 years old who underwent an annual dental examination in both 2003 and 2008. Data about toothbrushing habits and metabolic abnormalities, such as obesity, hyperglycemia, diabetes, hypertension, hypertriglyceridemia, and low levels of high-density lipoprotein-cholesterol, were analyzed using Poisson regression analysis. Results The percentage of participants with a toothbrushing frequency ≤1 time/day was 29.4%, and that for those not brushing their teeth at night was 21.4%. The incidences of obesity and hyperglycemia after 5 years were 5.5% and 28.4%, respectively. A toothbrushing frequency ≤1 time/day was associated with development of obesity (prevalence rate ratio [PRR] 1.77; 95% confidence interval [CI], 1.12–2.80), after adjusting for periodontal condition and potential risk factors. A significant association between not brushing teeth at night and hyperglycemia (PRR 1.30; 95% CI, 1.02–1.66) was observed in participants with toothbrushing frequency of 1 time/day. No association was found between toothbrushing habits and other metabolic abnormalities. Conclusions This study suggests that toothbrushing habits are associated with the development of obesity and hyperglycemia.


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In modern affluent societies, unhealthy lifestyle factors are responsible for a large 51 proportion of morbidities and mortalities. For example, smoking, unhealthy dietary 52 habits, lack of regular physical activity, high alcohol consumption, and not maintaining 53 an appropriate body weight have been shown to have an unfavorable influence on 54 cardiovascular disease 1, 2 as well as diabetes mellitus 3 and hypertension 4 . Additionally, 55 metabolic syndrome, a precursor of cardiovascular disease and diabetes mellitus 5 , is 56 affected by lifestyle factors, including smoking, diet, physical activity, and alcohol 57 consumption habits 6 . 58 These lifestyle factors have been shown to be connected to oral health 59 behaviors, such as toothbrushing, as it has been reported that lower toothbrushing 60 frequency correlates with smoking, unhealthier dietary habits, lower physical activity, 61 and higher consumption of alcohol 7,8 .Recent studies have shown that low toothbrushing 62 frequency is associated with obesity 9 , metabolic syndrome 10 , diabetes mellitus 11,12 , and 63 cardiovascular disease 13 . Furthermore, it has been found that not brushing teeth at night 64 is related to mortality 14 . These previous studies suggest both the clinical and public 65 health importance of toothbrushing, as toothbrushing leads not only to the prevention of 66 oral disease, but also to a reduced risk of health deterioration. Toothbrushing may be an 67 easily applicable preventive method for overall health deterioration. Additionally, 68 toothbrushing may have the hidden potential to become another factor of improving 69 health deterioration when general lifestyle modification has not been effective. 70 However, these studies [10][11][12][13][14] did not simultaneously address oral health 71 condition. Metabolic abnormalities, including obesity, hyperglycemia, dyslipidemia, and 72 high blood pressure, is associated with poor oral health condition, especially periodontal 73 disease 15 . The association between toothbrushing and metabolic abnormalities may be 74 A c c e p t e d V e r s i o n 4 influenced not only by lifestyle but also by periodontal condition 16 . We previously 75 reported that low toothbrushing frequency was associated with the onset of metabolic 76 syndrome, defined by ≥3 components of metabolic syndrome, after adjusting for 77 lifestyle factors and periodontal condition 17 . The previous study suggests the possibility 78 that toothbrushing is an independent related factor for the development of metabolic 79 syndrome. However, it remained unclear as to which specific metabolic abnormalities 80 were associated with toothbrushing habits and whether this association differed based 81 on the timing of toothbrushing. 82 In the present study, we examined whether toothbrushing habits (toothbrushing 83 frequency and toothbrushing at night) was longitudinally associated with the 84 development of metabolic abnormalities in addition to diabetes and hypertension, 85 considering oral health condition in Japanese adults. We hypothesized that 86 toothbrushing was an independent risk factor for developing metabolic abnormalities.  'two times, in the morning and at night'; 'two times, in the morning and the afternoon'; 110 'two times, in the afternoon and at night'; 'three times'; and 'four and more times'.

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Then, the 'once in the morning', 'once in the afternoon', and 'two times in the morning 112 and afternoon' were combined to create a dichotomous variable to identify the no 113 toothbrushing at night group. Toothbrushing time was also recorded.

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Number of teeth, periodontal condition, and oral hygiene status were recorded 115 as indicators of oral health condition at the baseline examination. A periodontal 116 examination was performed on all teeth except the third molars at two sites 117 (mesiobuccal and mid-buccal), following the National Health and Nutrition 118 Examination Survey III method; probing pocket depth (PPD) and clinical attachment 119 level (CAL) were assessed. The percentage of teeth that bled upon probing (%BOP) was 120 also examined. The periodontal examination was described previously in more detail 18 .

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Oral hygiene status was recorded using the Oral Hygiene Index-Simplified 19 .      The percentage of participants with a toothbrushing frequency of ≤1 time/day and who 198 did not brushing their teeth at night was 29.4% and 21.4%, respectively. The association between toothbrushing frequency and brushing teeth at night is shown in Table 2 Table 3). The association of not brushing teeth at night with 208 oral condition and lifestyle factors was similar to that of toothbrushing frequency.   (Table 7). A significant association between brushing at night 234 and obesity was not found (Table 7). Regarding periodontal condition, mean CAL, PPD, 235 calculus, and %BOP were higher in participants who had a toothbrushing frequency of 1 236 time/day and were not brushing at night than in those who brushed at night 237 (Supplemental Table 1). In participants with toothbrushing frequency of 1 time/day, not  Table 2). We found that a low frequency of toothbrushing was associated with the development of 243 obesity after adjusting for covariates and, furthermore, that not brushing teeth at night in 244 participants with toothbrushing frequency of 1 time/day was associated with 245 hyperglycemia. This longitudinal study reinforced the results of a previous cross-246 sectional study 9 , which showed the association between a low frequency of 247 toothbrushing and obesity. Moreover, the current study extends the findings of prior 248 longitudinal studies 10,12,17 in regard to toothbrushing frequency and health conditions 249 by specifying the link between the time of day of toothbrushing and metabolic 250 abnormalities.

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The association between toothbrushing habits and obesity was found, even 252 though periodontal condition and several lifestyle factors were adjusted for in 253 multivariate models, suggesting that this association is explained by other related factors.  9 . In this study, PRR for obesity with ≤1 time/day toothbrushing 258 was 1.77, indicating a relatively stronger association than that in the Park et al. study 9 .

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This might be related to unobserved confounders such as diet quality, including total 260 energy intake, and vegetable and fruit intake.  suggesting that gingival inflammation may play a role in mediating this association. hyperglycemia. In this context, this study showed a lack of a significant association 299 between toothbrushing habits and diabetes, which was probably due to the low 300 incidence of diabetes (2.3%). A longer follow-up study is necessary to confirm this 301 association.

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Although we were not able to clearly explain the direct link between 303 toothbrushing and metabolic abnormalities, one potential pathway may be that the  Low frequency of toothbrushing and not brushing teeth at night was inversely 323 associated with eating habits, such as eating snacks between meals and eating more 324 sweet foods (Table 2). This finding may be partly because participants are prone to 325 brushing their teeth after eating a snack or a sweet food to prevent dental caries and 326 maintain oral hygiene. Regarding metabolic abnormalities, participants who ate snacks 327 between meals were less likely to have hyperglycemia, hypertriglyceridemia, and 328 hypertension based on the cross-sectional data (data not shown). It has been reported 329 that individuals who eat snacks more frequently eat more fruits, vegetables, milk, and 330 dairy products and less fried food than those with a lower eating frequency 35 . The 331 inverse association between eating snacks and metabolic abnormalities may be 332 explained by diet quality.

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This study had several limitations. First, diet quality, such as total energy intake 334 and vegetable and fruit intake, was not investigated, although eating habits were 335 included in our study. It has been reported that toothbrushing frequency is positively 336 associated with intake of vegetables and fruits, 36 which contributes to the prevention of 337 metabolic abnormalities 37 . We also did not investigate inflammatory parameters, such as 338 high-sensitivity C-reactive protein, which is considered to be responsible for the link 339 between gingival and systemic inflammation. These unmeasured potential confounders 340 may have biased our estimates of the association between toothbrushing habits and 341 metabolic abnormalities owing to using the data of health check-ups, these variables 342 that might have been important were not recorded and could not be included in the 343 model. Future studies are needed to assess these factors. Second, we did not obtain 344 glucose tolerance test data, which defines diabetes more accurately, since a glucose 345 tolerance test is more time consuming in the health examination setting and a fasting 346 blood examination was more practical. Third, we used a partial mouth assessment for 347 periodontal condition, which did not include an examination of lingual or palatal sites.         ) Poisson regression models with robust standard error; each metabolic abnormality was the dependent variable and toothbrushing frequency was the independent variable. The crude model included one independent variable and one dependent variable. a Model 1 adjusted for age, sex, number of teeth, BMI, eating snacks between meals, preferring salty dishes, skipping breakfast, eating meat and oily food, eating sweet food, seldomly eating home-cooked meals, smoking, alcohol consumption, physical activity, sleeping hours, job, and baseline value of each metabolic abnormality, and Model 2 additionally included mean CAL. CAL, clinical attachment level; ACC/AHA, American College of Cardiology/American Heart Association; JNC7, Seventh Report of the Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High Blood Pressure; HDL, high-density lipoprotein; PRR, prevalence rate ratio; CI, confidence interval. smoking, alcohol consumption, physical activity, sleeping hours, job, and baseline value of each metabolic abnormality, and Model 2 additionally included mean CAL. CAL, clinical attachment level; ACC/AHA, American College of Cardiology/American Heart Association; JNC7, Seventh Report of the Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High Blood Pressure; HDL, high-density lipoprotein; PRR, prevalence rate ratio; CI, confidence interval.