Abstract

Objective:

To assess the association between long sleep duration and periodontal disease among men and women using nationally representative data.

Methods:

In this study, we performed a cross-sectional analysis and used multivariable logistic regression analysis models. We analysed data from 2012 through 2014 from the Korean National Health and Nutrition Examination Survey. The analysis in this study was confined to a total of 14,675 respondents over 19 years of age. We used a community periodontal index code greater than or equal to 3 to define periodontitis.

Results:

The tendency of periodontitis increased with longer sleep duration in women. Compared with women who slept 5hours or less, women with a sleep duration of 6 to 8hours and 9hours or more had higher odds of periodontitis at 1.29 (95% confidence interval [95%CI]: 1.06-1.56) and 1.45 (95%CI: 1.07-1.96), respectively, after adjustment for age, smoking, drinking, exercise, frequency of tooth brushing, self-reported oral status, body mass index, diabetes mellitus, hypertension, white blood cell count, income, and education. A significant relationship between sleep duration and periodontitis was not found in men.

Conclusion:

Our findings suggest that long sleep duration was associated with periodontitis, after adjusting for potential confounding factors, among Korean women, especially in premenopausal women.

Keywords:
Epidemiology; Health surveys; Oral health; Periodontitis; Sleep

Resumen

Objetivo:

Evaluar la asociación entre la larga duración del sueño y la enfermedad periodontal en hombres y mujeres utilizando datos nacionales representativos.

Método:

Se realizó un análisis transversal y se utilizaron modelos de análisis de regresión logística multivariable. Se analizaron los datos de 2012 a 2014 de la Encuesta Nacional de Salud y Nutrición de Corea. El análisis se limitó a 14.675 encuestados mayores de 19 años. Se utilizó un índice periodontal comunitario ≥3 para definir la periodontitis.

Resultados:

La tendencia a la periodontitis aumentó con una mayor duración del sueño en las mujeres adultas. En comparación con las mujeres que dormían 5 horas o menos, aquellas con una duración del sueño de 6 a 8 horas y 9 horas o más tenían probabilidades más altas de periodontitis: 1,29 (intervalo de confianza del 95% [IC95%]: 1,06-1,56) y 1,45 (IC95%: 1,07-1,96), respectivamente, después de ajustar por edad, hábito de fumar, consumo de alcohol, ejercicio, frecuencia de cepillado de dientes, estado oral informado, índice de masa corporal, diabetes mellitus, hipertensión, recuento de glóbulos blancos, ingresos y educación.

Conclusión:

Nuestros hallazgos sugieren que la larga duración del sueño se asoció con periodontitis, después de ajustar por los posibles factores de confusión, en las mujeres coreanas adultas, en especial en las premenopáusicas.

Palabras clave:
Epidemiología; Encuestas de salud; Salud bucal; Periodontitis; Dormir

Introduction

Epidemiologic data show that sleep duration impacts human physical health.¹1. V. Grover,R. Malhotra,H. Kaur. Exploring association between sleep deprivation and chronic periodontitis: a pilot study. J Indian Soc Periodontol., 19 (2015), pp. 304-307 http://dx.doi.org/10.4103/0972-124X.154173.
https://doi.org/10.4103/0972-124X.154173... Both short and long durations of sleep were reported to be predictors, or markers, of cardiovascular outcomes.²2. F.P. Cappuccio,D. Cooper,L. D'Elia. Sleep duration predicts cardiovascular outcomes: a systematic review and meta-analysis of prospective studies. Eur Heart J., 32 (2011), pp. 1484-1492 http://dx.doi.org/10.1093/eurheartj/ehr007.
https://doi.org/10.1093/eurheartj/ehr007... Short and long sleep durations were associated with poor self-rated health, and the association persisted in subgroup analysis of gender.³3. J.H. Kim,K.R. Kim,K.H. Cho. The association between sleep duration and self-rated health in the Korean general population. JCSM., 9 (2013), pp. 1057-1064 http://dx.doi.org/10.5664/jcsm.3082.
https://doi.org/10.5664/jcsm.3082... In a large representative sample of the general adult population, compared with a sleep duration of 7 hours, it was found a positive association between short and long sleep durations and poor self-rated health in Korean adults.³3. J.H. Kim,K.R. Kim,K.H. Cho. The association between sleep duration and self-rated health in the Korean general population. JCSM., 9 (2013), pp. 1057-1064 http://dx.doi.org/10.5664/jcsm.3082.
https://doi.org/10.5664/jcsm.3082... The relationship between quantity of sleep and incidence of type 2 diabetes mellitus was evaluated in a previous study, and it was shown that higher relative risk of type 2 diabetes mellitus was noted both for short duration of sleep (≤5-6hours/night) and long duration of sleep (>8-9hours/night).⁴4. F.P. Cappuccio, L. D'Elia ,P. Strazzullo. Quantity and quality of sleep and incidence of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care., 33 (2010), pp. 414-420 http://dx.doi.org/10.2337/dc09-1124.
https://doi.org/10.2337/dc09-1124... Another meta-analysis of prospective studies showed that both short and long durations of sleep are significant predictors of death in prospective population studies.⁵5. F.P. Cappuccio, L. D'Elia, P. Strazzullo . Sleep duration and all-cause mortality: a systematic review and meta-analysis of prospective studies. Sleep., 33 (2010), pp. 585-592. Sleep disturbances, including insomnia, independently contribute to the risk of inflammatory disorders and major depressive disorder.⁶6. M.R. Irwin,M.R. Opp. Sleep-health: reciprocal regulation of sleep and innate immunity. Neuropsychopharmacology., 42 (2017), pp. 129-155 http://dx.doi.org/10.1038/npp.2016.148.
https://doi.org/10.1038/npp.2016.148... Sleep loss induces a functional alteration of the monocyte proinflammatory cytokine response, resulting in alteration of immune cell physiologic characteristics.⁷7. M.R. Irwin ,M. Wang,C.O. Campomayor. Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch Intern Med., 166 (2006), pp. 1756-1762 http://dx.doi.org/10.1001/archinte.166.16.1756.
https://doi.org/10.1001/archinte.166.16.... ⁸8. D.J. Frey,M. Fleshner,K.P. Wright Jr.. The effects of 40hours of total sleep deprivation on inflammatory markers in healthy young adults. Brain Behav Immun., 21 (2007), pp. 1050-1057 http://dx.doi.org/10.1016/j.bbi.2007.04.003.
https://doi.org/10.1016/j.bbi.2007.04.00... Chronic sleep deprivation markedly affects bone health by decreasing bone mineral density and 25-hydroxyvitamin D, deteriorating the bone microarchitecture and decreasing bone formation and bone resorption markers.⁹9. X. Xu,L. Wang,L. Chen. Effects of chronic sleep deprivation on bone mass and bone metabolism in rats. J Orthop Surg Res., 11 (2016), pp. 87 http://dx.doi.org/10.1186/s13018-016-0418-6.
https://doi.org/10.1186/s13018-016-0418-... Moreover, it was shown that gender differences in sleep become apparent after the onset of puberty.¹⁰10. V. Krishnan,N.A. Collop. Gender differences in sleep disorders. Curr Opin Pulm Med., 12 (2006), pp. 383-389 http://dx.doi.org/10.1097/01.mcp.0000245705.69440.6a.
https://doi.org/10.1097/01.mcp.000024570...

Previous reports showed that non-apnea sleep disorder increased the risk of periodontal disease.¹¹11. C.F. Lee,M.C. Lin,C.L. Lin. Non-apnea sleep disorder increases the risk of periodontal disease: a retrospective population-based cohort study. J Periodontol., 85 (2014), pp. e65-e71 http://dx.doi.org/10.1902/jop.2013.130284.
https://doi.org/10.1902/jop.2013.130284... Sleep disordered breathing is defined as the number of apnea plus hypopnea events associated with ≥3% desaturation of oxygen per hour of estimated sleep and was shown to be associated with periodontitis, which was most pronounced in young adults.¹²12. A.E. Sanders,G.K. Essick,J.D. Beck. Periodontitis and sleep disordered breathing in the Hispanic community health study/Study of Latinos. Sleep., 38 (2015), pp. 1195-1203 http://dx.doi.org/10.5665/sleep.4890.
https://doi.org/10.5665/sleep.4890... Similarly, higher Pittsburgh Sleep Quality Index scores, representing worse sleep quality, were associated with severity of periodontal disease.¹1. V. Grover,R. Malhotra,H. Kaur. Exploring association between sleep deprivation and chronic periodontitis: a pilot study. J Indian Soc Periodontol., 19 (2015), pp. 304-307 http://dx.doi.org/10.4103/0972-124X.154173.
https://doi.org/10.4103/0972-124X.154173... Previous reports also evaluated the relationship of routine inadequate sleep duration and periodontitis in a nationally representative sample.¹³13. R.C. Wiener. Relationship of routine inadequate sleep duration and periodontitis in a nationally representative sample. Sleep Dis., 2016 (2016), pp. 9158-195 However, limited information is available regarding the relationship between long sleep duration and periodontal disease. It was hypothesized that there is no significant association between long sleep duration and periodontitis. Thus, this study was performed to assess the association between long sleep duration and periodontitis among men and women using nationally representative data.

Methods

Survey and subjects

This study used data from the Korean National Health and Nutrition Examination Survey (KNHANES), which was conducted between 2012 and 2014. The data were obtained by the Division of Chronic Disease Surveillance under the Korean Ministry of Health and Welfare.¹⁴14. S.G. Lim,K. Han,H.A. Kim. Association between insulin resistance and periodontitis in Korean adults. J Clin Periodontol., 41 (2014), pp. 121-130 http://dx.doi.org/10.1111/jcpe.12196.
https://doi.org/10.1111/jcpe.12196... ¹⁵15. S.H. Ko,H.S. Kwon,D.J. Kim. Higher prevalence and awareness, but lower control rate of hypertension in patients with diabetes than general population: the fifth Korean National Health and Nutrition Examination Survey in 2011. Diabetes Metab J., 38 (2014), pp. 51-57 http://dx.doi.org/10.4093/dmj.2014.38.1.51.
https://doi.org/10.4093/dmj.2014.38.1.51... The sampling units of KNHANES were based on the population and housing consensus from the National Census Registry in the Republic of Korea. Sample weights with complex survey design and poststratification were applied in KNHANES.

Initially, a total of 23,626 individuals were candidates in the KNHANES survey. The analysis in this study was confined to a total of 18,382 respondents over 19 years of age. Finally, 14,675 individuals -without missing values for the outcome variables- were analyzed for the analysis. Informed consent was obtained from all participants of KNHANES, and this survey was approved by the Institutional Review Board of the Korean Centers for Disease Control and Prevention.

Sociodemographic and health behaviors variables

All participants were asked about sociodemographic and health behaviors variables by trained interviewers. Smoking status was categorized into two groups: current smoker or non-current smoker. Participants were also categorized into two groups according to alcohol consumption within one month from the interview: current drinker or noncurrent drinker.¹⁶16. D.P. Agarwal. Cardioprotective effects of light-moderate consumption of alcohol: a review of putative mechanisms. Alcohol Alcohol., 37 (2002), pp. 409-415. Individuals were regarded as a regular exerciser if they performed walking at least five times per week for over 30minutes per session. Sleep duration was self-reported. In this study, “short sleep” was considered 5hours or less, and “long sleep” was defined as 9hours; the reference category was 6 to 8hours.¹⁷17. S.R. Patel,N.T. Ayas, M. R. Malhotra . A prospective study of sleep duration and mortality risk in women. Sleep., 27 (2004), pp. 440-444.

Anthropometric and biochemical measurements

Trained staff members performed the anthropometric measurements. Body weight was measured to the nearest 0.1kg, and height was measured to nearest 1mm. Body mass index (kg/m²) was defined as body weight (kg) divided by the square of the height (m²). Waist circumference was measured at the narrowest point between the lowest rib and the iliac crest. Cut-offs for defining general and abdominal obesity were applied to be suitable for the Asian population: a body mass index ≥25kg/m² was defined as general obesity,¹⁸18. Y.M. Park,J. Liu. Obesity in East Asia. In: Rexford S. Ahima Metabolic syndrome: a comprehensive textbook. Switzerland: Springer, Cham, 2016, pp. 87-100 and abdominal obesity was defined as a waist circumference ≥90cm in men or ≥80cm in women.¹⁹19. K.G. Alberti,P. Zimmet,J. Shaw. The metabolic syndrome - a new worldwide definition. Lancet., 366 (2005), pp. 1059-1062 http://dx.doi.org/10.1016/S0140-6736(05)67402-8.
https://doi.org/10.1016/S0140-6736(05)67...

Systolic and diastolic blood pressure was measured twice using a standard mercury sphygmomanometer (Baumanometer; W.A. Baum Co., Inc., Copiague, NY, USA) at intervals of 5minutes, and the average was used for the analysis.

A blood sample was obtained from the antecubital vein of each participant after fasting for more than 8hours to measure white blood cell count and the total concentration of cholesterol, triglycerides, serum fasting plasma glucose, and high-density lipoprotein-cholesterol with Automatic Analyzer 7600 (Hitachi, Tokyo, Japan) using the kits (Daiichi, Tokyo, Japan).²⁰20. T.M. Wallace,J.C. Levy,D.R. Matthews. Use and abuse of HOMA modeling. Diabetes Care ., 27 (2004), pp. 1487-1495.

If three or more of the following criteria were fulfilled, the participants were considered to have metabolic syndrome²¹21. K.G. Alberti, R.H. Eckel,S.M. Grundy. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation., 120 (2009), pp. 1640-1645 http://dx.doi.org/10.1161/CIRCULATIONAHA.109.192644.
https://doi.org/10.1161/CIRCULATIONAHA.1... waist circumference of 90cm or greater in men and 80cm or greater in women, fasting triglycerides 150mg/dL or greater or use of lipid-lowering medication, high-density lipoprotein-cholesterol lower than 40mg/dL in men and lower than 50mg/dL in women or use of medication, blood pressure of 130/85mm Hg or greater or use of antihypertensive medication in a patient with a history of hypertension, and fasting blood glucose of 100mg/dL or greater or current use of antidiabetic medication. Participants were considered to have diabetes when fasting plasma sugar was 126mg/dL or greater and/or hemoglobin A1c was 6.5% or greater or when they were currently using antidiabetic medications or had physician-diagnosed diabetes.²²22. J.Y. Jeon, S.H. Ko, H.S. Kwon . Prevalence of diabetes and prediabetes according to fasting plasma glucose and HbA1c. Diabetes Metab J., 37 (2013), pp. 349-357 http://dx.doi.org/10.4093/dmj.2013.37.5.349.
https://doi.org/10.4093/dmj.2013.37.5.34... Hypertension was defined as a systolic blood pressure of 140mmHg or greater, a diastolic blood pressure of 90mmHg or greater, or the current use of antihypertensive medication.²³23. C. Lenfant,A.V. Chobanian,D.W. Jones. Seventh report of the Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High Blood Pressure (JNC 7): resetting the hypertension sails. Hypertension., 41 (2003), pp. 1178-1179 http://dx.doi.org/10.1161/01.HYP.0000075790.33892.AE.
https://doi.org/10.1161/01.HYP.000007579...

Oral health behaviors, periodontitis, and number of natural teeth

The time of day when participants brushed their teeth and used secondary oral products was recorded as oral health behaviors.²⁴24. Y.H. Kim,D.H. Kim,K.S. Lim. Oral health behaviors and metabolic syndrome: the 2008-2010 Korean National Health and Nutrition Examination Survey. Clin Oral Investig, 18 (2014), pp. 1517-1524 http://dx.doi.org/10.1007/s00784-013-1112-2.
https://doi.org/10.1007/s00784-013-1112-... We calculated the frequency of daily tooth brushing by the total number of times the teeth were brushed per day. Secondary oral products included the following: dental floss, mouthwash, interdental brushes, electric toothbrushes, irrigation devices, tongue cleaners, end-tufted brushes, and any special device for dentures. Self-reported oral state was categorized into favorable, average, and problematic.

The presence of periodontal disease was evaluated using the World Health Organization community periodontal index (CPI). Periodontitis was defined if the CPI score was ≥3. When more than one site had a >3.5mm pocket in the index teeth, which are 11, 16, 17, 26, 27, 31, 36, 37, 46, and 47, according to the Federation Dentaire Internationale system, it indicated a CPI score of code 3.²⁵25. J.B. Park, K. Han,Y.G. Park. Association between alcohol consumption and periodontal disease: the 2008 to 2010 Korea National Health and Nutrition Examination Survey. J Periodontol., 85 (2014), pp. 1521-1528 http://dx.doi.org/10.1902/jop.2014.130782.
https://doi.org/10.1902/jop.2014.130782... The mouth was divided into sextants and a CPI probe (PWHO, Osung MND, Seoul, Korea) with a 0.5mm ball tip was used. An average probing force was approximately 20g.²⁵25. J.B. Park, K. Han,Y.G. Park. Association between alcohol consumption and periodontal disease: the 2008 to 2010 Korea National Health and Nutrition Examination Survey. J Periodontol., 85 (2014), pp. 1521-1528 http://dx.doi.org/10.1902/jop.2014.130782.
https://doi.org/10.1902/jop.2014.130782...

Trained and calibrated dentists examined the periodontal status of the participants. Training was provided to minimize the errors in the measurement of periodontal pocket depth by each examiner during the examination, as a part of quality control. In 2012 KNHANES, 29 and 27 dentists performed the evaluation in the first and second half, respectively. Twenty-nine dentist and 27 dentists performed the evaluation in the first and second half of 2013, respectively. In 2014 KNHANES, 26 dentists examined the periodontal status.

Statistical analyses

We used the appropriate survey procedures to take into account the complex sampling design used in KNHANES. All data are presented as mean±standard error or percentage (standard error). We performed logarithmic transformation to achieve normal distribution when necessary. We performed a Rao-Scott chi-square test for categorical variables or an independent t-test for continuous variables to assess the differences in characteristics according to the presence of periodontitis. Interactions between sex and sleep and interactions between menopause and sleep were evaluated and the p-interaction values were calculated. In addition, subgroup analyses were performed. We used multivariable logistic regression analyses to evaluate the risk of periodontitis in relation to sleep duration and calculated odds ratios (OR) and 95% confidence intervals (95%CI) after adjusting for potential confounders. Model 1 was unadjusted, and model 2 was adjusted for age. In model 3, adjustments were made for the variables in model 2, plus smoking, drinking, exercise, frequency of tooth brushing, and self-reported oral status. In model 4, adjustments were made for the variables in model 3, plus white blood cell count. model 5 was adjusted for the variables in model 4, plus income and education.

Results

Table 1 describes the sex-specific baseline characteristics of the study population by presence of periodontitis. Significant differences were noted between men and women in the mean age, body mass index, waist circumference, sleep duration, smoking, drinking, and exercise. The number of individuals who brushed their teeth three times or more per day, used floss, and used interdental brushes was higher in women (p <0.05). The interactions between sex and sleep, and the interactions between menopause and sleep were evaluated, and the p-interaction values were 0.02 and 0.14, respectively.

Figure 1A displays the prevalence of periodontitis in men according to the sleep duration after adjusting for potential confounders (p >0.05). The prevalence of periodontitis in women, according to sleep duration, is shown in Figure 1B. Increase in the prevalence of periodontitis was noted with longer sleep duration after adjusting the covariates (p <0.05).

Table 2 shows the subgroup analysis regarding the sleep duration, categorized by sex, using health behaviors variables and oral health behaviors. Women with long sleep durations of 9hours or more showed a higher prevalence of smoking and drinking. These trends were not seen in men with long sleep durations. Women with long sleep durations showed lower prevalence of tooth brushing three times a day or more, lower use of floss, and lower use of interdental brushes (p <0.05). However, statistically significant differences were not seen in men.

Table 3 shows the adjusted OR and their 95%CI from multivariable logistic regression analyses for individuals with periodontitis, according to sleep duration. Adjusted OR and their 95%CI of men with periodontitis were 1, 0.99 (0.78-1.25), and 0.83 (0.57-1.22) after adjustment for age, smoking, drinking, exercise, frequency of tooth brushing, self-reported oral status, body mass index, diabetes mellitus, hypertension, and white blood cell count for sleep durations of 5hours or less, 6 to 8hours, and 9hours or more, respectively (p >0.05). Adjusted OR and their 95%CI of women with periodontitis were 1, 1.29 (1.06-1.56), and 1.45 (1.07-1.96) after adjustment for sleep durations of 5hours or less, 6 to 8hours, and 9hours or more, respectively (p <0.05).

Figure 2A Displays the prevalence of periodontitis according to sleep duration, categorized by general obesity, after adjusting the covariates. Statistically significant association was only noted in women (p <0.05).Figure 2B displays the prevalence of periodontitis according to sleep duration, categorized by abdominal obesity. Statistically significant association was only noted in women (p <0.05).

Table 4 shows the adjusted OR and their 95%CI from multivariate logistic regression analyses for individuals with periodontitis, according to sleep duration, categorized by premenopause and postmenopause. Adjusted OR and their 95%CI of periodontitis in premenopause women were 1, 1.25 (1.04-1.51), and 1.58 (1.13-2.21) after adjustment for sleep durations of 5hours or less, 6 to 8hours, and 9hours or more, respectively (p <0.05). Adjusted OR and their 95%CI of periodontitis in postmenopause women were 1, 1.17 (0.79-1.73), and 1.52 (0.86-2.68) after adjustment for sleep durations of 5hours or less, 6 to 8hours, and 9hours or more, respectively (p >0.05).

Discussion

This study aimed to identify associations between periodontitis and long sleep duration among men and women. The results showed that an increased risk of periodontitis was statistically significantly associated with longer sleep duration in women, especially in premenopause women.

The following issues should be considered when interpreting the results. Because of this study's cross-sectional design, the causal direction of the associations between sleep duration and periodontitis cannot be ascertained.²⁶26. K. Han,E. Hwang, J.B. Park . Excessive consumption of green tea as a risk factor for periodontal disease among Korean adults. Nutrients, 8 (2016), http://dx.doi.org/10.3390/nu8040194.
https://doi.org/10.3390/nu8040194... It is therefore possible that long duration of sleep might be a consequence of, rather than a causative risk factor for, periodontal disease.²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337... Another limitation of this study is that individuals’ sleep habits were obtained via recall and that they may not have recalled their habits correctly.²⁸28. K. Han ,Y. Ko, Y.G. Park. Associations between the number of natural teeth in postmenopausal women and duration of lactation: the 2010-2012 Korea National Health and Nutrition Examination Survey. Maturitas., 85 (2016), pp. 73-78 http://dx.doi.org/10.1016/j.maturitas.2015.12.010.
https://doi.org/10.1016/j.maturitas.2015... Also, long sleep duration may be part of an unhealthy health behaviors, which in turn may impair oral health.²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337... This study used partial mouth recording protocols of CPI because it was not feasible to conduct the traditional full-mouth examination in nationally performed health survey due to limited resources including manpower, funds, number of examiners and time.²⁹29. A. Kingman,C. Susin,J.M. Albandar. Effect of partial recording protocols on severity estimates of periodontal disease. J Clin Periodontol., 35 (2008), pp. 659-667 http://dx.doi.org/10.1111/j.1600-051X.2008.01243.x.
https://doi.org/10.1111/j.1600-051X.2008... However, the limitations of CPI are its inability to provide an adequate assessment of prevalence of periodontal disease and partial mouth recording protocols may underestimate the prevalence of periodontitis with the amount of underestimation varies depending on the number and type of sites examined.³⁰30. J.M. Albandar Underestimation of periodontitis in NHANES surveys. J Periodontol ., 82 (2011), pp. 337-341 http://dx.doi.org/10.1902/jop.2011.100638.
https://doi.org/10.1902/jop.2011.100638... ³¹31. P.I. Eke,G.O. Thornton-Evans,L. Wei. Accuracy of NHANES periodontal examination protocols. J Dental Res., 89 (2010), pp. 1208-1213 ³²32. P.I. Eke ,B.A. Dye, L. Wei . Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol ., 86 (2015), pp. 611-622 http://dx.doi.org/10.1902/jop.2015.140520.
https://doi.org/10.1902/jop.2015.140520... Additionally, sleep duration is reported to be associated with depressive symptoms and the use of antidepressants,³³33. L. Zhai,H. Zhang,D. Zhang. Sleep duration and depression among adults: a meta-analysis of prospective studies. Depress Anxiety., 32 (2015), pp. 664-670 http://dx.doi.org/10.1002/da.22386.
https://doi.org/10.1002/da.22386... but the information was not available for this study. However, the data used in this study were a nationally representative sample based on the National Census Registry, and a multistage clustered probability design was applied for the recruitment of the participants.³⁴34. K. Han, Y. Ko, Y.G. Park . Associations between the periodontal disease in women before menopause and menstrual cycle irregularity: the 2010-2012 Korea National Health and Nutrition Examination Survey. Medicine., 95 (2016), pp. e2791 http://dx.doi.org/10.1097/MD.0000000000002791.
https://doi.org/10.1097/MD.0000000000002... Selection bias was overcome by applying survey sample weights adjusted for participation rate and response rate.³⁵35. K.D. Han, Y.G. Park . Comments on statistical issues in January 2016. Korean J Fam Med., 37 (2016), pp. 75-76 http://dx.doi.org/10.4082/kjfm.2016.37.1.75.
https://doi.org/10.4082/kjfm.2016.37.1.7... The association between the sleep duration and periodontitis was evaluated using multiple logistic regression analyses after adjusting for confounding factors.²⁶26. K. Han,E. Hwang, J.B. Park . Excessive consumption of green tea as a risk factor for periodontal disease among Korean adults. Nutrients, 8 (2016), http://dx.doi.org/10.3390/nu8040194.
https://doi.org/10.3390/nu8040194... Collectively, this study can be considered representative and reliable.

The definitions of short and long sleep duration vary among different studies. In this study, short sleep was considered 5hours or less, long sleep was defined as 9hours, and the reference category was 6 to 8hours. Other studies have defined short sleep as ≤4hours,³⁶36. K.L. Knutson,Turek F.W. The. U-shaped association between sleep and health: the 2 peaks do not mean the same thing. Sleep., 29 (2006), pp. 878-879. ≤5hours,¹⁷17. S.R. Patel,N.T. Ayas, M. R. Malhotra . A prospective study of sleep duration and mortality risk in women. Sleep., 27 (2004), pp. 440-444. ≤6hours,³⁷37. L. Mallon,J.E. Broman,J. Hetta. Sleep complaints predict coronary artery disease mortality in males: a 12-year follow-up study of a middle-aged Swedish population. J Int Med., 251 (2002), pp. 207-216 and <7hours,³⁸38. T.Y. Lan,T.H. Lan,C.P. Wen. Nighttime sleep, Chinese afternoon nap, and mortality in the elderly. Sleep., 30 (2007), pp. 1105-1110. and long sleep as >8hours,³⁷37. L. Mallon,J.E. Broman,J. Hetta. Sleep complaints predict coronary artery disease mortality in males: a 12-year follow-up study of a middle-aged Swedish population. J Int Med., 251 (2002), pp. 207-216 ≥9hours,¹⁷17. S.R. Patel,N.T. Ayas, M. R. Malhotra . A prospective study of sleep duration and mortality risk in women. Sleep., 27 (2004), pp. 440-444. 10hours,³⁸38. T.Y. Lan,T.H. Lan,C.P. Wen. Nighttime sleep, Chinese afternoon nap, and mortality in the elderly. Sleep., 30 (2007), pp. 1105-1110. and 12hours,³⁹39. C. Gale,C. Martyn. Larks and owls and health, wealth, and wisdom. BMJ., 317 (1998), pp. 1675-1677. while the reference category has been defined as 7hours,³⁷37. L. Mallon,J.E. Broman,J. Hetta. Sleep complaints predict coronary artery disease mortality in males: a 12-year follow-up study of a middle-aged Swedish population. J Int Med., 251 (2002), pp. 207-216 7 to 8hours,⁴⁰40. C. Hublin,M. Partinen,M. Koskenvuo. Sleep and mortality: a population-based 22-year follow-up study. Sleep., 30 (2007), pp. 1245-1253. 7 to 9hours,⁴¹41. M. Kojima,K. Wakai,T. Kawamura. Sleep patterns and total mortality: a 12-year follow-up study in Japan. J Epidemiol., 10 (2000), pp. 87-93. 6 to 8hours,⁴²42. K.L. Stone,S.K. Ewing,S. Ancoli-Israel. Self-reported sleep and nap habits and risk of mortality in a large cohort of older women. J Am Geriatr Soc., 57 (2009), pp. 604-611 http://dx.doi.org/10.1111/j.1532-5415.2008.02171.x.
https://doi.org/10.1111/j.1532-5415.2008... and 9hours.³⁹39. C. Gale,C. Martyn. Larks and owls and health, wealth, and wisdom. BMJ., 317 (1998), pp. 1675-1677.

Several researches have been performed to evaluate the association between sleep duration and health outcomes.¹³13. R.C. Wiener. Relationship of routine inadequate sleep duration and periodontitis in a nationally representative sample. Sleep Dis., 2016 (2016), pp. 9158-195 ²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337... ³⁶36. K.L. Knutson,Turek F.W. The. U-shaped association between sleep and health: the 2 peaks do not mean the same thing. Sleep., 29 (2006), pp. 878-879. Previous observational epidemiologic studies suggest that both short and long durations of sleep may be associated with an increased risk of adverse health outcomes, including total mortality, cardiovascular disease, type 2 diabetes mellitus, obesity, respiratory disorders, and poor general health.²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337... ³⁶36. K.L. Knutson,Turek F.W. The. U-shaped association between sleep and health: the 2 peaks do not mean the same thing. Sleep., 29 (2006), pp. 878-879. However, other population-based data suggest that only short sleep duration was associated with adverse health issues.⁴³43. M. Singh,C.L. Drake,T. Roehrs. The association between obesity and short sleep duration: a population-based study. JCSM ., 1 (2005), pp. 357-363. In a previous study using a nationally representative sample, no statistically significant relationship between inadequate sleep duration and periodontitis was found.¹³13. R.C. Wiener. Relationship of routine inadequate sleep duration and periodontitis in a nationally representative sample. Sleep Dis., 2016 (2016), pp. 9158-195 The different results may be due to the design of the studies and characteristics of the study population, including culture.²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337...

The association between long sleep duration and periodontitis may be explained by the following. Sleep habits in the general population are reported to be the result of a complex interaction between different kinds of factors, including social, behavioral, psychological, and comorbid conditions.²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337... One study found significant consistent associations of long sleep duration with age and poorer physical health status.²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337... Low socioeconomic status, unemployment, poor general health, undiagnosed health condition, and depression may also be associated with long sleep duration.⁴4. F.P. Cappuccio, L. D'Elia ,P. Strazzullo. Quantity and quality of sleep and incidence of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care., 33 (2010), pp. 414-420 http://dx.doi.org/10.2337/dc09-1124.
https://doi.org/10.2337/dc09-1124... ⁴⁴44. S.R. Patel ,A. Malhotra,D.J. Gottlieb. Correlates of long sleep duration. Sleep., 29 (2006), pp. 881-889. Moreover, this study clearly showed that health behaviors variables and oral health behaviors were associated with long sleep duration, and this may have produced a higher prevalence of periodontitis in individuals with longer sleep duration. However, there is possibility that both, sleeping time and periodontitis, are cross-sectionally associated because both are consequences of the same group of risk factors (life style and health behavior).

Previous reports have shown sex differences in the risk associated with duration of sleep. This study clearly showed association only in women. Biological conditions unique to women, including menstrual cycles, pregnancy, and menopause, may alter sleep pattern.¹⁰10. V. Krishnan,N.A. Collop. Gender differences in sleep disorders. Curr Opin Pulm Med., 12 (2006), pp. 383-389 http://dx.doi.org/10.1097/01.mcp.0000245705.69440.6a.
https://doi.org/10.1097/01.mcp.000024570... ⁴⁵45. N.A. Collop ,D. Adkins,B.A. Phillips. Gender differences in sleep and sleep-disordered breathing. Clin Chest Med., 25 (2004), pp. 257-268 http://dx.doi.org/10.1016/j.ccm.2004.01.002.
https://doi.org/10.1016/j.ccm.2004.01.00... Similarly, modest associations between sleep and incident myocardial infarction were seen in middle-aged women but not men from the general population.⁴⁶46. C. Meisinger,M. Heier,H. Lowel. Sleep duration and sleep complaints and risk of myocardial infarction in middle-aged men and women from the general population: the MONICA/KORA Augsburg cohort study. Sleep., 30 (2007), pp. 1121-1127. The association between sleep duration and the prevalence of hypertension was only noted in women and not in men.⁴⁷47. F.P. Cappuccio , S. Stranges, N.B. Kandala. Gender-specific associations of short sleep duration with prevalent and incident hypertension: the Whitehall II Study. Hypertension ., 50 (2007), pp. 693-700 http://dx.doi.org/10.1161/HYPERTENSIONAHA.107.095471.
https://doi.org/10.1161/HYPERTENSIONAHA.... The effect was stronger among premenopausal women than among postmenopausal women.⁴⁸48. S. Stranges, J.M. Dorn, F.P. Cappuccio. A population-based study of reduced sleep duration and hypertension: the strongest association may be in premenopausal women. J Hypertens., 28 (2010), pp. 896-902 http://dx.doi.org/10.1097/HJH.0b013e328335d076.
https://doi.org/10.1097/HJH.0b013e328335... However, another report showed that long sleep duration was associated with age, especially among men.²⁷27. S. Stranges,J.M. Dorn,M.J. Shipley. Correlates of short and long sleep duration: a cross-cultural comparison between the United Kingdom and the United States: the Whitehall II Study and the Western New York Health Study. Am J Epidemiol., 168 (2008), pp. 1353-1364 http://dx.doi.org/10.1093/aje/kwn337.
https://doi.org/10.1093/aje/kwn337... Female hormones, including estrogen and progesterone, are suggested to be related to sleep patterns.⁴⁹49. B.K. Rasmussen. Migraine and tension-type headache in a general population: precipitating factors, female hormones, sleep pattern and relation to lifestyle. Pain., 53 (1993), pp. 65-72. ⁵⁰50. M. Branchey,L. Branchey,R.D. Nadler. Effects of estrogen and progesterone on sleep patterns of female rats. Physiol Behav., 6 (1971), pp. 743-746. It should also be considered that there may be sex differences in stress and reaction and there may be differences in genetics that may affect sleep.⁴⁶46. C. Meisinger,M. Heier,H. Lowel. Sleep duration and sleep complaints and risk of myocardial infarction in middle-aged men and women from the general population: the MONICA/KORA Augsburg cohort study. Sleep., 30 (2007), pp. 1121-1127.

Conclusion

Conclusively, the association between long sleep duration and periodontitis was proven by multiple logistic regression analyses after adjusting for confounding factors among Korean women, especially in premenopausal women. Long sleep duration may be considered an independent risk indicator of periodontal disease among Korean women.

Acknowledgements

The authors thank the Korea Centers for Disease Control and Prevention for providing the data.

References

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