J Clin Periodontol 2014; 41: 121–130 doi: 10.1111/jcpe.12196
Association between insulin resistance and periodontitis in Korean adults Lim SG, Han K, Kim H-A, Pyo SW, Cho Y-S, Kim K-S, Yim HW, Lee W-C, Park YG, Park Y-M. Association between insulin resistance and periodontitis in Korean adults. J Clin Periodontol 2014; 41: 121–130. doi: 10.1111/jcpe.12196.
Abstract Objective: Recent studies have proposed an association between periodontitis and metabolic abnormalities. We investigated the association between insulin resistance and periodontitis among Korean adults. Methods: A cross-sectional analysis was conducted using the Korea National Health and Nutrition Examination Survey 2008–2010. A total of 16,720 nondiabetic subjects over 18 years old were evaluated (7060 men and 9660 women). Periodontal status was assessed by the Community Periodontal Index. Insulin resistance was measured using the homeostasis model assessment of insulin resistance (HOMA-IR). Participants in the highest and lowest quartile of HOMA-IR were defined as insulin-resistant and insulin-sensitive respectively. Results: The prevalence of periodontitis increased significantly with higher HOMA-IR quartiles in post-menopausal women (p for linear association = 0.019). Among post-menopausal women, participants in the highest quartile of HOMA-IR were significantly more likely to have periodontitis compared to those in the lowest quartile [adjusted odds ratio (OR), 1.47; 95% confidence interval (CI), 1.07–2.01]. Moreover, obese post-menopausal women showed an increased association between insulin resistance and periodontitis (adjusted OR, 1.92; 95% CI,1.29–2.87). However, this association was not found in men or premenopausal women. Conclusions: Our results suggest that insulin resistance may be associated with periodontitis, especially when combined with obesity, among post-menopausal women in Korea.
Metabolic syndrome (MetS), a complex collection of impaired glucose metabolism, dyslipidemia, hypertension and central obesity, is known to Conflict of interest and source of funding statement The authors declare that there are no conflicts of interest. This study was funded by research grants from the Catholic Medical Center Research Foundation in 2011.
be associated with double the risk of future cardiovascular diseases and type 2 diabetes mellitus (Gami et al. 2007, Lorenzo et al. 2007). Although various definitions exist for MetS, insulin resistance is regarded as the key feature leading to this syndrome (Reaven 1988). Insulin resistance stimulates systemic low-grade inflammation, which may increase the risk of other inflammatory diseases (Pickup 2004). In this context, it was proposed that insulin resistance plays
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Sang Gyu Lim1,2, Kyungdo Han3,4, Hyun-Ah Kim5, Sung Woon Pyo2, Young-Sik Cho6, Kyung-Soo Kim7, Hyeon Woo Yim1,4, Won-Chul Lee1,4, Yong Gyu Park3 and Yong-Moon Park1,4,8 1
Graduate School of Public Health, The Catholic University of Korea, Seoul, Korea; 2 Department of Dentistry, College of Medicine, The Catholic University of Korea, Seoul, Korea; 3Departmentof Biostatistics, College of Medicine, The Catholic University of Korea, Seoul, Korea; 4Department of Preventive Medicine, College of Medicine, The Catholic University of Korea, Seoul, Korea; 5Catholic Medical Center, The Catholic University of Korea, Seoul, Korea; 6 Department of Dental Hygiene, Namseoul University, Cheonan, Korea; 7Department of Family Medicine, College of Medicine, The Catholic University of Korea, Seoul, Korea; 8 Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia, SC, USA
Key words: Insulin resistance; periodontitis; menopause Accepted for publication 5 November 2013
a role in the pathogenesis of periodontal infection (Genco et al. 2005). Periodontitis is a common chronic disease of the adult population, characterized by an exaggerated gingival inflammatory response against the pathogenic bacterial microflora, leading to the loss of alveolar bone and tooth (Williams 1990). Other studies have suggested that periodontitis is associated with obesity (Linden et al. 2013), low-grade inflammation (Slade
121
122
Lim et al.
et al. 2000, 2003), dyslipidemia (Katz et al. 2002), diabetes (Borgnakke et al. 2013, Engebretson & Kocher 2013, Taylor et al. 2013) and dysmetabolic status (Saito & Shimazaki 2007). Although many recent studies have proposed a potential association between MetS and periodontitis (D’Aiuto et al. 2008, Li et al. 2009, Morita et al. 2010, Kwon et al. 2011, Han et al. 2012a,b), only a few studies have examined the relationship between periodontitis and insulin resistance (Genco et al. 2005, Benguigui et al. 2010, Timonen et al. 2011, Demmer et al. 2012). Although ethnic differences in body composition and fat distribution may contribute to the differential risk for metabolic or cardiovascular disease according to different ethnicity (Wang et al. 1994, Chambers et al. 2001), even a few existing studies regarding an association between insulin resistance and periodontitis have been conducted in Western countries, and none of these have focused on the Asian population. Therefore, the aim of this study was to explore the association between insulin resistance and periodontitis among Korean adults, using the homeostasis model assessment (HOMA) to assess insulin resistance. Methods Study population
This study used the data from the Korea National Health and Nutrition Examination Survey (KNHANES) 2008–2010. KNHANES is a cross-sectional, nationally representative sample of the Korean noninstitutionalized civilian population and employs a rolling sampling design that uses a complex, stratified, multistage probability sample design. It is comprised of a health interview survey, a health examination survey, and a nutrition survey, which are carried out by specially trained interviewers and examiners. Survey participants included 74.8% of the selected sample of 12,528 subjects in 2008, 79.2% of the selected sample of 12,722 subjects in 2009 and 77.5% of the selected sample of 10,938 subjects in 2010. All participants signed an informed consent
form, and this study was approved by the Institutional Review Board of the Catholic University of Korea. The study population for this analysis included adults aged 19 years and over who participated in all three parts of the survey, including the periodontal examination. Subjects with diabetes mellitus, or who were missing data on fasting plasma glucose or serum insulin, were excluded. Diabetes mellitus was defined as having a fasting plasma glucose ≥126 mg/dl, taking insulin or antidiabetic medication, or having a physician diagnosis of diabetes mellitus. The final study population was comprised of 16,720 participants (7060 men and 9660 women). Measurements
Socioeconomic and lifestyle variables During the health interview survey, trained examiners recorded information about patient demographic status and health-related characteristics: including age, education, and household income. In addition, data about lifestyle characteristics, including smoking, drinking alcohol, and exercise, were recorded through self-reported questionnaires. Patient education level was divided into four groups by highest education achieved: elementary school, middle school, high school and university. Household income was calculated as the family income, adjusting for the number of family members, and divided into quartiles. 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 cigarettes or more in their lifetime) and exsmokers (i.e., those who had smoked in the past but ceased smoking). The amount of alcohol consumed in grams (g) per day was calculated using the average number of standard alcohol servings consumed and the frequency of alcohol consumption. Alcohol consumption status was classified into three groups: nondrinker, mild-to-moderate drinker (
Association between insulin resistance and periodontitis in Korean adults Lim SG, Han K, Kim H-A, Pyo SW, Cho Y-S, Kim K-S, Yim HW, Lee W-C, Park YG, Park Y-M. Association between insulin resistance and periodontitis in Korean adults. J Clin Periodontol 2014; 41: 121–130. doi: 10.1111/jcpe.12196.
Abstract Objective: Recent studies have proposed an association between periodontitis and metabolic abnormalities. We investigated the association between insulin resistance and periodontitis among Korean adults. Methods: A cross-sectional analysis was conducted using the Korea National Health and Nutrition Examination Survey 2008–2010. A total of 16,720 nondiabetic subjects over 18 years old were evaluated (7060 men and 9660 women). Periodontal status was assessed by the Community Periodontal Index. Insulin resistance was measured using the homeostasis model assessment of insulin resistance (HOMA-IR). Participants in the highest and lowest quartile of HOMA-IR were defined as insulin-resistant and insulin-sensitive respectively. Results: The prevalence of periodontitis increased significantly with higher HOMA-IR quartiles in post-menopausal women (p for linear association = 0.019). Among post-menopausal women, participants in the highest quartile of HOMA-IR were significantly more likely to have periodontitis compared to those in the lowest quartile [adjusted odds ratio (OR), 1.47; 95% confidence interval (CI), 1.07–2.01]. Moreover, obese post-menopausal women showed an increased association between insulin resistance and periodontitis (adjusted OR, 1.92; 95% CI,1.29–2.87). However, this association was not found in men or premenopausal women. Conclusions: Our results suggest that insulin resistance may be associated with periodontitis, especially when combined with obesity, among post-menopausal women in Korea.
Metabolic syndrome (MetS), a complex collection of impaired glucose metabolism, dyslipidemia, hypertension and central obesity, is known to Conflict of interest and source of funding statement The authors declare that there are no conflicts of interest. This study was funded by research grants from the Catholic Medical Center Research Foundation in 2011.
be associated with double the risk of future cardiovascular diseases and type 2 diabetes mellitus (Gami et al. 2007, Lorenzo et al. 2007). Although various definitions exist for MetS, insulin resistance is regarded as the key feature leading to this syndrome (Reaven 1988). Insulin resistance stimulates systemic low-grade inflammation, which may increase the risk of other inflammatory diseases (Pickup 2004). In this context, it was proposed that insulin resistance plays
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Sang Gyu Lim1,2, Kyungdo Han3,4, Hyun-Ah Kim5, Sung Woon Pyo2, Young-Sik Cho6, Kyung-Soo Kim7, Hyeon Woo Yim1,4, Won-Chul Lee1,4, Yong Gyu Park3 and Yong-Moon Park1,4,8 1
Graduate School of Public Health, The Catholic University of Korea, Seoul, Korea; 2 Department of Dentistry, College of Medicine, The Catholic University of Korea, Seoul, Korea; 3Departmentof Biostatistics, College of Medicine, The Catholic University of Korea, Seoul, Korea; 4Department of Preventive Medicine, College of Medicine, The Catholic University of Korea, Seoul, Korea; 5Catholic Medical Center, The Catholic University of Korea, Seoul, Korea; 6 Department of Dental Hygiene, Namseoul University, Cheonan, Korea; 7Department of Family Medicine, College of Medicine, The Catholic University of Korea, Seoul, Korea; 8 Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia, SC, USA
Key words: Insulin resistance; periodontitis; menopause Accepted for publication 5 November 2013
a role in the pathogenesis of periodontal infection (Genco et al. 2005). Periodontitis is a common chronic disease of the adult population, characterized by an exaggerated gingival inflammatory response against the pathogenic bacterial microflora, leading to the loss of alveolar bone and tooth (Williams 1990). Other studies have suggested that periodontitis is associated with obesity (Linden et al. 2013), low-grade inflammation (Slade
121
122
Lim et al.
et al. 2000, 2003), dyslipidemia (Katz et al. 2002), diabetes (Borgnakke et al. 2013, Engebretson & Kocher 2013, Taylor et al. 2013) and dysmetabolic status (Saito & Shimazaki 2007). Although many recent studies have proposed a potential association between MetS and periodontitis (D’Aiuto et al. 2008, Li et al. 2009, Morita et al. 2010, Kwon et al. 2011, Han et al. 2012a,b), only a few studies have examined the relationship between periodontitis and insulin resistance (Genco et al. 2005, Benguigui et al. 2010, Timonen et al. 2011, Demmer et al. 2012). Although ethnic differences in body composition and fat distribution may contribute to the differential risk for metabolic or cardiovascular disease according to different ethnicity (Wang et al. 1994, Chambers et al. 2001), even a few existing studies regarding an association between insulin resistance and periodontitis have been conducted in Western countries, and none of these have focused on the Asian population. Therefore, the aim of this study was to explore the association between insulin resistance and periodontitis among Korean adults, using the homeostasis model assessment (HOMA) to assess insulin resistance. Methods Study population
This study used the data from the Korea National Health and Nutrition Examination Survey (KNHANES) 2008–2010. KNHANES is a cross-sectional, nationally representative sample of the Korean noninstitutionalized civilian population and employs a rolling sampling design that uses a complex, stratified, multistage probability sample design. It is comprised of a health interview survey, a health examination survey, and a nutrition survey, which are carried out by specially trained interviewers and examiners. Survey participants included 74.8% of the selected sample of 12,528 subjects in 2008, 79.2% of the selected sample of 12,722 subjects in 2009 and 77.5% of the selected sample of 10,938 subjects in 2010. All participants signed an informed consent
form, and this study was approved by the Institutional Review Board of the Catholic University of Korea. The study population for this analysis included adults aged 19 years and over who participated in all three parts of the survey, including the periodontal examination. Subjects with diabetes mellitus, or who were missing data on fasting plasma glucose or serum insulin, were excluded. Diabetes mellitus was defined as having a fasting plasma glucose ≥126 mg/dl, taking insulin or antidiabetic medication, or having a physician diagnosis of diabetes mellitus. The final study population was comprised of 16,720 participants (7060 men and 9660 women). Measurements
Socioeconomic and lifestyle variables During the health interview survey, trained examiners recorded information about patient demographic status and health-related characteristics: including age, education, and household income. In addition, data about lifestyle characteristics, including smoking, drinking alcohol, and exercise, were recorded through self-reported questionnaires. Patient education level was divided into four groups by highest education achieved: elementary school, middle school, high school and university. Household income was calculated as the family income, adjusting for the number of family members, and divided into quartiles. 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 cigarettes or more in their lifetime) and exsmokers (i.e., those who had smoked in the past but ceased smoking). The amount of alcohol consumed in grams (g) per day was calculated using the average number of standard alcohol servings consumed and the frequency of alcohol consumption. Alcohol consumption status was classified into three groups: nondrinker, mild-to-moderate drinker (
