Dong-Hun Han,*â Sinye Lim,â¡ and Jin-Bom Kim§. Background: Smoking and diabetes are well-known risk factors for periodontitis. The aims of this study are to ...
J Periodontol • November 2012
The Association of Smoking and Diabetes With Periodontitis in a Korean Population Dong-Hun Han,*† Sinye Lim,‡ and Jin-Bom Kim§
Background: Smoking and diabetes are well-known risk factors for periodontitis. The aims of this study are to examine whether these factors are associated with periodontitis in representative samples of Koreans and to estimate the interaction impact of smoking and diabetes on periodontitis in this population. Methods: The Korean National Oral Health Survey (KNOHS) 2006 collected nationally representative samples of oral epidemiologic data. A community periodontal index (CPI) of 3 to 4 and a CPI value of 0 to 2 were classified as periodontitis and non-periodontitis, respectively. A total of 4,118 participants from KNOHS 2006 were interviewed on smoking and diabetes. Periodontitis was the outcome variable. Smoking and diabetes were the major explanatory variables. The confounders consisted of age, sex, education, occupation, monthly income, and residential area. Logistic regression analyses were used to evaluate the associations of smoking and diabetes with periodontitis after adjustment for confounders. Results: The overall prevalence of periodontitis, current smoking, and self-reported diabetes in Korean adults was 10.1%, 25.9%, and 4.5%, respectively. Associations of smoking and diabetes with periodontitis were : current smokers, odds ratio (OR) = 1.40, 95% confidence interval (CI) = 1.02 to 1.90; and diabetes, OR = 1.21, 95% CI = 0.82 to 1.77. The association between diabetes and periodontitis was not significant and there were no synergistic interactions of smoking and diabetes on periodontitis. Conclusions: The results suggest that smoking has a significant impact on the periodontal health of Korean adults, but the combined effect of smoking and diabetes had no significant impact. J Periodontol 2012;83: 1397-1406. KEY WORDS Diabetes mellitus; epidemiology; periodontitis; risk factors; smoking. * Department of Preventive and Social Dentistry, School of Dentistry, Seoul National University, Seoul, Korea. † Dental Research Institute, School of Dentistry, Seoul National University. ‡ Department of Occupational and Environmental Medicine, Kyung Hee University Hospital, Seoul, Korea. § Department of Preventive and Community Dentistry, School of Dentistry, Pusan National University, Yangsan, Korea.
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eriodontal disease is recognized as one of the major and most prevalent oral pathologies throughout the world. 1 Periodontal disease results from a complex interplay between chronic bacterial infection and the inflammatory host response, and genetic and environmental factors are also influences.2 The effects of smoking as a risk factor on the prevalence, extent, and severity of periodontitis have been the topics of numerous epidemiologic studies.3-13 In Korea, the prevalence of periodontitis ranges from 10.3%14 to 32.9%.15 A recent systematic review16 on periodontal disease and smoking, based on the appraisal of 21 cohort studies, 70 cross-sectional studies, and 14 casecontrol studies, concluded that evidence in support of a negative impact of smoking on periodontal health is strong. Thirteen of 14 cross-sectional studies and four of five cohort studies published after this review concluded that there is an association between smoking and periodontal disease.17 The association between cigarette smoking and periodontitis has been examined in nationally representative samples in Korea,14 the United States,11 and Japan.9 Diabetes and periodontal health status have long been considered to be biologically linked. Advanced chronic periodontitis (CP) often coexists with poorly controlled diabetes, such that diabetes is considered to be a risk factor
doi: 10.1902/jop.2012.110686
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Smoking, Diabetes, and Periodontitis in Koreans
for severe CP.18 An epidemiologic review19 of four studies conducted among adults reported a significant positive correlation between diabetes (types 1 and 2) and periodontal disease. A recent cross-sectional study showed poorer periodontal health in patients with type 1 diabetes than in controls.20 Numerous epidemiologic studies21-23 that evaluated this relationship hypothesized that diabetes increases the risk of developing CP after controlling for related confounders. At the same time, there is evidence that the presence of CP may increase the risk of diabetes. 24 Oxidative stress may also act as a potential common link to explain relationships between diabetes and periodontitis.25 Studies have investigated the association of periodontitis with various risk factors, including smoking and diabetes, in national Korean samples.14,15 However, no study has evaluated the dose–response relationship between smoking and periodontitis in Koreans. Moreover, no study has assessed the impact of the interaction of smoking and diabetes on periodontitis in Koreans. Therefore, this study investigates the association among periodontitis, smoking, and diabetes in a large representative sample of Korean adults to add evidence of the association of these major risk factors to periodontitis. MATERIALS AND METHODS Study Population The Korean National Oral Health Survey (KNOHS) 2006,26 the fifth national oral health survey conducted by the Korean Ministry of Health and Welfare, was performed from September 2006 to December 2006 using a stratified cluster sampling procedure. The sampling frame was derived from the 150 stratified enumeration districts maintained by the Department of Statistics in Korea and was stratified according to size of region, defined as urban, semi-urban, and rural areas. Sixty households from each enumeration district were contacted and the survey procedure explained. Households refusing to complete the survey were excluded. Two or three individuals were examined per household for a total for a total of 15,777 Koreans. The number of Korean individuals ‡18 years of age for whom all records were available was 4,546. To assess the exact periodontal status, the final dataset was composed of individuals who had ‡6 teeth (n = 4,118). Data Collection The survey was performed by eight survey teams using a questionnaire and a dental examination. Each team was composed of a dentist and an interviewer, trained to perform standard dental examination and to conduct the interview procedure, and subsequently calibrated with various oral health status indicators. Demographic information (age and sex), socioeco1398
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nomic status (education, monthly household income, occupation, and residence), smoking status, and diabetes status were obtained from the questionnaire. The questionnaire and periodontal examination were performed at a single home visit. The Korean Oral Health Act of 2000 specifies that the Minister of Health and Welfare should investigate the oral health status of the people on a regular basis. The data analyzed in our study are from the Korean National Oral Health Survey 2006; therefore, the research for this study is exempt from ethical approval since the database includes no personally identifiable information. Assessment of periodontitis. Eight experienced public health dentists (J.H. Han, J.W. Im, S.K. Jun, S.M. Kang, D.Y. Kim, W.J. Roh, W.S. Sul, G.H. Yeo, Korean Ministry of Health and Welfare, Seoul, Korea) examined the oral health status of each of the participants. Periodontal condition was assessed using the community periodontal index (CPI)27 because it is used widely in surveys of large populations. The five CPI scores used to evaluate the periodontal health status were as follows: 1) normal (CPI 0); 2) gingival bleeding (CPI 1); 3) calculus (CPI 2); 4) shallow periodontal pocket of 3.5 to 5.5 mm (CPI 3); and 5) deep periodontal pocket of ‡5.5 mm (CPI 4). The measurements were made using a CPI probe at six sites (mesio-buccal, mid-buccal, disto-buccal, disto-lingual, mid-lingual, and mesio-lingual) per tooth. Ten teeth were selected for the periodontal examination: the two molars in each posterior sextant and the upper right and lower left central incisors. If no index teeth were present in the qualifying sextant, the adjacent remaining teeth in that sextant were examined. The highest resulting score was recorded as the CPI score for each individual. Groups were categorized according to periodontal status: non-periodontitis (CPI 0 to CPI 2) or periodontitis (CPI 3 or CPI 4). The number of sextants with CPI 3 or CPI 4 was also counted as the extent of periodontitis. Before the survey, the eight public health dentists underwent a calibration training procedure for CPI measurements. After achieving a k value >0.70 between the gold standard (D.Y. Park, GangneungWonju National University, Gangneung, Korea) and eight examiners, the main survey began. The intraexaminer k value was also >0.70. Assessment of smoking and diabetes. Individuals were classified as current or non-smokers. Current smokers were asked the number of cigarettes smoked per day and duration of smoking. Individuals selfreporting a diagnosis of diabetes by a doctor (‘‘Has the doctor ever told you that you have diabetes?’’) were included in the group with diabetes. Assessment of covariates. Sociodemographic variables related to periodontal disease were selected as covariates and included age and sex were selected to control the demographic confounding effects;
J Periodontol • November 2012
education level, occupation, area of residence, and monthly household income were used to indicate socioeconomic status. Behavioral factors, such as frequency of daily toothbrushing and recent dental visit, were also used as covariates. The frequency of daily toothbrushing and recent dental visit were the proxy measures of personal and professional dental care received. Education was divided into five groups: 1)no schooling (0 years); 2) 12 years. Occupation was categorized as: 1) non-manual, including management, professional, administrative, and service; 2) manual, including mechanics, farming, and armed forces; and 3) other. Recent dental visit was categorized as: 1) £6 months; 2) £2 years; 3) >2 years; and 4) never. Area of residence was classified as: 1) urban; 2) semi-urban; and 3) rural. Monthly household income was: 1) 1,000,000 KRW and 2,000,000 KRW and 3,000,000 KRW. 1,000 KRW was 1.05 US Dollars. An average Korean monthly household income was 2,950,000 KRW in 2006. Age and frequency of daily toothbrushing were obtained as continuous variables. Statistical Analyses Individual weighted factors were used and a complex sampling design of the survey was considered to obtain variances. The dependent variable was periodontitis. Independent variables included smoking and diabetes. The confounders were sociodemographic factors(age, sex, education, occupation, area of residence, and monthly household income) and behavioral factors(frequency of daily toothbrushing and recent dental visit). The characteristic variables of the individuals were described using frequency distributions for the categorical variables. A x2 test was used to assess differences in categorical variables. Continuous variables were presented with means and standard deviations. Independent t tests were used to determine differences between periodontal status, smoking status, and diabetes status. The independent variables were divided for the application of binary logistic regression into current smoker, yes/no and diabetes, yes/no. Current smoking was categorized into four groups (pack-year was calculated by multiplying of the number of packs per day by the duration of smoking): 1) 0 pack-year; 2) 660 pack-year in a lifetime. Multivariate logistic regression analysis was used to evaluate the adjusted odds ratio (AOR) estimates between the periodontitis (category, no versus yes) and bivariate independent variables (smoking and diabetes, no versus yes) to test the association adjusting for
Han, Lim, Kim
confounders, including age, sex, education level, occupation, frequency of daily toothbrushing, recent dental visit, area of residence, and monthly household income. To determine the strength of the association, the dose–effect relationship between the severity of smoking and periodontitis was evaluated. Finally, the interaction of smoking and diabetes was also assessed. RESULTS Among the total sample, 10.1% (95% confidence interval [CI] = 9.1% to 11.2%) had periodontitis (CPI ‡ 3); 25.9% (95% CI = 24.2% to 27.6%); were smokers and 4.5% (95% CI = 3.9% to 5.2%) of the respondents had diabetes. There were significant differences in the distribution of periodontitis with regard to all sociodemographic and behavioral (Table 1). The distribution of current smokers was significantly different from these variables (Table 2). The distribution of self-reporting with diabetes was significantly different from the above factors, except for sex and recent dental visit (Table 3). Table 4 shows the crude odds ratio (OR) and AOR values of periodontitis for smoking and diabetes. Current smokers showed significantly higher OR and AOR (1.58 and 1.40) values than non-smokers. A dose– response relationship, according to smoking packyears, was clearly detected, and the linear trends for the effects of smoking on periodontitis were statistically significant (trend P = 0.003). In the case of diabetes, there was a crude association between diabetes and periodontitis (OR = 2.31, P
