J Bone Miner Metab DOI 10.1007/s00774-015-0669-z
ORIGINAL ARTICLE
Oral health behaviors and bone mineral density in South Korea: the 2008–2010 Korean National Health and Nutrition Examination Survey Hyun‑Jin Kim1 · Yang‑Hyun Kim1 · Kyung‑Hwan Cho1 · Byoung‑Duck Han1 · Seon‑Mee Kim1 · Youn‑Seon Choi1 · Do‑Hoon Kim1 · Kyung‑ Do Han2 · Yong‑Joo Lee3 · Chul‑Min Kim3
Received: 28 October 2014 / Accepted: 19 March 2015 © The Japanese Society for Bone and Mineral Research and Springer Japan 2015
Abstract The purpose of this study was to examine the association between oral health behaviors and bone mineral density (BMD) by using data from the Korean National Health and Nutrition Examination Survey conducted in 2008–2010. We included 6,620 subjects (3,140 men aged more than 50 years and 3,480 postmenopausal women). BMD was measured at three sites—namely, the lumbar spine, total femur, and femur neck. Oral health behaviors were assessed by use of a self-administered questionnaire in the Korean National Health and Nutrition Examination Survey. After adjustment for all covariates, BMD of the lumbar spine and femur neck tended to increase as the frequency of tooth brushing increased in men (ptrend = 0.020 and ptrend = 0.028, respectively). Women using secondary oral products had increased lumbar spine BMD compared with women who did not use secondary oral products. However, after adjustment for all covariates, no significant relationship was observed between BMD and the use of secondary oral products. As the frequency of tooth brushing Hyun-Jin Kim and Yang-Hyun Kim contributed equally to this work. Electronic supplementary material The online version of this article (doi:10.1007/s00774-015-0669-z) contains supplementary material, which is available to authorized users. * Chul‑Min Kim [email protected] 1
Department of Family Medicine, Korea University College of Medicine, Seoul, South Korea
2
Department of Medical Statistics, Catholic University College of Medicine, Seoul, South Korea
3
Department of Family Medicine, Catholic University College of Medicine, 222 Banpo‑daero, Seocho‑Gu, Seoul, Korea 137‑701, South Korea
and the number of secondary oral products used increased, the prevalence of osteoporosis decreased. The frequency of tooth brushing is associated with increased lumbar spine and femur neck BMD in South Korean men. Keywords Bone mineral density · Osteoporosis · Oral health behavior · Tooth brushing · Korea National Health and Nutrition Examination Survey
Introduction Oral health behaviors such as frequent tooth brushing and the use of secondary oral products are known to be related to general health behaviors [1]. In Asian studies, healthy oral health behaviors are also related to decreased cardiovascular risk factors [2] as well as metabolic syndrome [3, 4], which is a precondition of cardiovascular diseases [5]. In contrast, healthy oral health behaviors are inversely associated with the prevalence of periodontitis, which is an inflammatory state of periodontal structures, including alveolar bone damage [6]. Osteoporosis is a bone disease characterized by a low bone mass and deterioration of bone microarchitecture. Both increased bone resorption and decreased bone formation lead to osteoporosis [7]. The risk factors for the development of osteoporosis are old age, postmenopausal women, low calcium intake, low vitamin D level, and health behaviors such as smoking, alcohol intake, and physical activities [8–10]. Cardiometabolic abnormalities including dyslipidemia and metabolic syndrome are also known to be associated with the prevalence of osteoporosis [11–16]. Some studies have shown the relationship between periodontitis and osteoporosis [17, 18]; however, there has been no study on the relationship between oral health behaviors
13
and bone mineral density (BMD). Therefore, we analyzed the relationship by using representative data of Korean adults from the Korean National Health and Nutrition Examination Survey (KNHANES) conducted in 2008–2010.
J Bone Miner Metab
defined as those who exercised for more than 30 min per session or those who exercised more than three times per week at an intense level for more than 20 min per session. Anthropometric measurements
Materials and methods Survey overview We used data from the 2008–2010 KNHANES. The KNHANES was performed from 1998 by the Division of Chronic Disease Surveillance of the Korea Centers for Disease Control and Prevention as a nationwide survey. The KNHANES evaluates health and nutrition at the national level, and it consists of a physical examination, a nutritional survey, and a health interview [19]. To obtain a representative sample of the noninstitutionalized civilians of both sexes from all the geographic regions of South Korea, the subjects from the KNHANES were stratified into multiple stages, selected using a cluster sampling design, and prorated by age from the 2005 National Census Registry. Trained interviewers performed face-to-face interviews. Subjects A total of 21,811 subjects (12,417 men and 13,487 women) aged 19 years or older were included in the KNHANES. First, we included only men aged more than 50 years and postmenopausal women. We excluded those who had been treated for osteoporosis and periodontitis. Finally, 6,620 subjects (3,140 men and 3,480 women) were included in this study. The study protocol was approved by the Korean Ministry of Health and Welfare, and the study was conducted according to the Ethical Principles for Medical Research Involving Human Subjects, as defined by the Helsinki Declaration. Written informed consent was obtained from all the subjects. Sociodemographic factors and general health behaviors The subjects were surveyed about sociodemographic factors and completed a self-administered questionnaire about age, sex, family income, and education level. Household income was adjusted for the number of family members and divided into quartiles. Education level was categorized as either high school graduate or not high school graduate. General health behaviors were also reported by the subjects. Current smokers were defined as those who smoked currently and had smoked 100 cigarettes in their whole life. Heavy drinkers were those who drank 30 g or more per day. Physical activity was defined using the International Physical Activity Questionnaire [20]. The regular exercise group was
13
The subjects wore light clothes without shoes, and then a trained examiner measured weight (kg), height (cm), and waist circumference (cm) to the nearest 0.1 kg, 0.1 cm, and 0.1 cm, respectively. After normal expiration, waist circumference was measured on a horizontal plane at the midpoint level between the costal margin and the iliac crest. Body mass index was calculated by dividing weight (kg) by the square of the height (m2). Blood pressure was measured three times using a mercury sphygmomanometer (Baumanometer; W.A. Baum, Copiague, NY, USA), and average systolic blood pressure and diastolic blood pressure were used for statistical analysis. Biochemical measurements After the subjects had fasted for more than 8 h, serum blood samples were collected. Triglyceride, high-density lipoprotein cholesterol, fasting blood glucose, alkaline phosphatase, and parathyroid hormone levels were measured enzymatically using a model 7600 automatic analyzer (Hitachi, Tokyo, Japan), and the serum 25-hydroxyvitamin D level was analyzed with use of a 25-hydroxyvitamin D 125I radioimmunosssay kit (DiaSorin, Stillwater, MN, USA) and a gamma counter (1470 Wizard; PerkinElmer, Turku, Finland) after the samples had been transported to the Central Testing Institute in Seoul, South Korea. BMD measurement Whole-body dual-energy X-ray absorptiometry was performed with a QDR Discovery fan beam densitometer (Hologic, Bedford, MA, USA), following the procedures recommended by the manufacturer. All subjects wore light clothes and removed all jewelry and other items that could interfere with the BMD measurement. BMD was measured at the lumbar spine (LS), total femur (TF), and femur neck (FN). The dual-energy X-ray absorptiometry results were analyzed using the standard techniques of the Korean Society of Osteoporosis and Hologic Discovery software (version 13.1). Definition of metabolic syndrome We defined metabolic syndrome according to the American Heart Association/National Heart, Lung, and Blood Institute scientific statement criteria for Asians [21]. Metabolic syndrome was diagnosed when three or more of the following criteria were met: waist circumference 90 cm or greater
J Bone Miner Metab
in men and 80 cm or greater in women; blood pressure 130/85 mmHg or greater or use of antihypertensive medication; fasting blood glucose level 100 mg/dL or greater or use of antidiabetic medication; fasting triglyceride level 150 mg/dL or greater or use of antidyslipidemic medication; high-density lipoprotein cholesterol level below 40 mg/dL in men and below 50 mg/dL in women or use of antidyslipidemic medication. Oral health behaviors We checked the time of day when tooth brushing occurred and the use of secondary oral products. Secondary oral products included mouthwash, dental floss, an interdental brush, and an electric toothbrush. The time of day was categorized as before or after breakfast, lunch, or dinner; after snacks; or before bedtime. The frequency of daily tooth brushing was calculated as the number of tooth brushing sessions per day. Remaining teeth and periodontitis The subjects were asked whether they had lost their natural teeth, and we counted the number of remaining teeth. The World Health Organization community periodontal index was used to define periodontitis. We defined periodontitis when the community periodontal index was “code 3” or greater, which means that at least one site had a pocket. larger than 3.5 mm. The tooth index numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46, and 47. An appropriate community periodontal index probe was used in accordance with the World Health Organization guidelines [22]. We divided the mouth into sextants, and used an approximately 20-g force for probing. The mean kappa value for the interexaminer reliability was 0.89 (0.55–1.00) [23]. Osteopenia and osteoporosis The diagnosis of osteopenia and osteoporosis was based on the measurement of BMD using the dual-energy X-ray absorptiometry results for the LS, TF, and FN according to the World Health Organization diagnostic classification [24]. Osteopenia was defined as a BMD of 1.0 standard deviation below the peak bone mass of a young, healthy, sex- and race-matched reference population, and osteoporosis was defined as a BMD of 2.5 standard deviations as follows [25]: (1) normal bone mass, −1.0
ORIGINAL ARTICLE
Oral health behaviors and bone mineral density in South Korea: the 2008–2010 Korean National Health and Nutrition Examination Survey Hyun‑Jin Kim1 · Yang‑Hyun Kim1 · Kyung‑Hwan Cho1 · Byoung‑Duck Han1 · Seon‑Mee Kim1 · Youn‑Seon Choi1 · Do‑Hoon Kim1 · Kyung‑ Do Han2 · Yong‑Joo Lee3 · Chul‑Min Kim3
Received: 28 October 2014 / Accepted: 19 March 2015 © The Japanese Society for Bone and Mineral Research and Springer Japan 2015
Abstract The purpose of this study was to examine the association between oral health behaviors and bone mineral density (BMD) by using data from the Korean National Health and Nutrition Examination Survey conducted in 2008–2010. We included 6,620 subjects (3,140 men aged more than 50 years and 3,480 postmenopausal women). BMD was measured at three sites—namely, the lumbar spine, total femur, and femur neck. Oral health behaviors were assessed by use of a self-administered questionnaire in the Korean National Health and Nutrition Examination Survey. After adjustment for all covariates, BMD of the lumbar spine and femur neck tended to increase as the frequency of tooth brushing increased in men (ptrend = 0.020 and ptrend = 0.028, respectively). Women using secondary oral products had increased lumbar spine BMD compared with women who did not use secondary oral products. However, after adjustment for all covariates, no significant relationship was observed between BMD and the use of secondary oral products. As the frequency of tooth brushing Hyun-Jin Kim and Yang-Hyun Kim contributed equally to this work. Electronic supplementary material The online version of this article (doi:10.1007/s00774-015-0669-z) contains supplementary material, which is available to authorized users. * Chul‑Min Kim [email protected] 1
Department of Family Medicine, Korea University College of Medicine, Seoul, South Korea
2
Department of Medical Statistics, Catholic University College of Medicine, Seoul, South Korea
3
Department of Family Medicine, Catholic University College of Medicine, 222 Banpo‑daero, Seocho‑Gu, Seoul, Korea 137‑701, South Korea
and the number of secondary oral products used increased, the prevalence of osteoporosis decreased. The frequency of tooth brushing is associated with increased lumbar spine and femur neck BMD in South Korean men. Keywords Bone mineral density · Osteoporosis · Oral health behavior · Tooth brushing · Korea National Health and Nutrition Examination Survey
Introduction Oral health behaviors such as frequent tooth brushing and the use of secondary oral products are known to be related to general health behaviors [1]. In Asian studies, healthy oral health behaviors are also related to decreased cardiovascular risk factors [2] as well as metabolic syndrome [3, 4], which is a precondition of cardiovascular diseases [5]. In contrast, healthy oral health behaviors are inversely associated with the prevalence of periodontitis, which is an inflammatory state of periodontal structures, including alveolar bone damage [6]. Osteoporosis is a bone disease characterized by a low bone mass and deterioration of bone microarchitecture. Both increased bone resorption and decreased bone formation lead to osteoporosis [7]. The risk factors for the development of osteoporosis are old age, postmenopausal women, low calcium intake, low vitamin D level, and health behaviors such as smoking, alcohol intake, and physical activities [8–10]. Cardiometabolic abnormalities including dyslipidemia and metabolic syndrome are also known to be associated with the prevalence of osteoporosis [11–16]. Some studies have shown the relationship between periodontitis and osteoporosis [17, 18]; however, there has been no study on the relationship between oral health behaviors
13
and bone mineral density (BMD). Therefore, we analyzed the relationship by using representative data of Korean adults from the Korean National Health and Nutrition Examination Survey (KNHANES) conducted in 2008–2010.
J Bone Miner Metab
defined as those who exercised for more than 30 min per session or those who exercised more than three times per week at an intense level for more than 20 min per session. Anthropometric measurements
Materials and methods Survey overview We used data from the 2008–2010 KNHANES. The KNHANES was performed from 1998 by the Division of Chronic Disease Surveillance of the Korea Centers for Disease Control and Prevention as a nationwide survey. The KNHANES evaluates health and nutrition at the national level, and it consists of a physical examination, a nutritional survey, and a health interview [19]. To obtain a representative sample of the noninstitutionalized civilians of both sexes from all the geographic regions of South Korea, the subjects from the KNHANES were stratified into multiple stages, selected using a cluster sampling design, and prorated by age from the 2005 National Census Registry. Trained interviewers performed face-to-face interviews. Subjects A total of 21,811 subjects (12,417 men and 13,487 women) aged 19 years or older were included in the KNHANES. First, we included only men aged more than 50 years and postmenopausal women. We excluded those who had been treated for osteoporosis and periodontitis. Finally, 6,620 subjects (3,140 men and 3,480 women) were included in this study. The study protocol was approved by the Korean Ministry of Health and Welfare, and the study was conducted according to the Ethical Principles for Medical Research Involving Human Subjects, as defined by the Helsinki Declaration. Written informed consent was obtained from all the subjects. Sociodemographic factors and general health behaviors The subjects were surveyed about sociodemographic factors and completed a self-administered questionnaire about age, sex, family income, and education level. Household income was adjusted for the number of family members and divided into quartiles. Education level was categorized as either high school graduate or not high school graduate. General health behaviors were also reported by the subjects. Current smokers were defined as those who smoked currently and had smoked 100 cigarettes in their whole life. Heavy drinkers were those who drank 30 g or more per day. Physical activity was defined using the International Physical Activity Questionnaire [20]. The regular exercise group was
13
The subjects wore light clothes without shoes, and then a trained examiner measured weight (kg), height (cm), and waist circumference (cm) to the nearest 0.1 kg, 0.1 cm, and 0.1 cm, respectively. After normal expiration, waist circumference was measured on a horizontal plane at the midpoint level between the costal margin and the iliac crest. Body mass index was calculated by dividing weight (kg) by the square of the height (m2). Blood pressure was measured three times using a mercury sphygmomanometer (Baumanometer; W.A. Baum, Copiague, NY, USA), and average systolic blood pressure and diastolic blood pressure were used for statistical analysis. Biochemical measurements After the subjects had fasted for more than 8 h, serum blood samples were collected. Triglyceride, high-density lipoprotein cholesterol, fasting blood glucose, alkaline phosphatase, and parathyroid hormone levels were measured enzymatically using a model 7600 automatic analyzer (Hitachi, Tokyo, Japan), and the serum 25-hydroxyvitamin D level was analyzed with use of a 25-hydroxyvitamin D 125I radioimmunosssay kit (DiaSorin, Stillwater, MN, USA) and a gamma counter (1470 Wizard; PerkinElmer, Turku, Finland) after the samples had been transported to the Central Testing Institute in Seoul, South Korea. BMD measurement Whole-body dual-energy X-ray absorptiometry was performed with a QDR Discovery fan beam densitometer (Hologic, Bedford, MA, USA), following the procedures recommended by the manufacturer. All subjects wore light clothes and removed all jewelry and other items that could interfere with the BMD measurement. BMD was measured at the lumbar spine (LS), total femur (TF), and femur neck (FN). The dual-energy X-ray absorptiometry results were analyzed using the standard techniques of the Korean Society of Osteoporosis and Hologic Discovery software (version 13.1). Definition of metabolic syndrome We defined metabolic syndrome according to the American Heart Association/National Heart, Lung, and Blood Institute scientific statement criteria for Asians [21]. Metabolic syndrome was diagnosed when three or more of the following criteria were met: waist circumference 90 cm or greater
J Bone Miner Metab
in men and 80 cm or greater in women; blood pressure 130/85 mmHg or greater or use of antihypertensive medication; fasting blood glucose level 100 mg/dL or greater or use of antidiabetic medication; fasting triglyceride level 150 mg/dL or greater or use of antidyslipidemic medication; high-density lipoprotein cholesterol level below 40 mg/dL in men and below 50 mg/dL in women or use of antidyslipidemic medication. Oral health behaviors We checked the time of day when tooth brushing occurred and the use of secondary oral products. Secondary oral products included mouthwash, dental floss, an interdental brush, and an electric toothbrush. The time of day was categorized as before or after breakfast, lunch, or dinner; after snacks; or before bedtime. The frequency of daily tooth brushing was calculated as the number of tooth brushing sessions per day. Remaining teeth and periodontitis The subjects were asked whether they had lost their natural teeth, and we counted the number of remaining teeth. The World Health Organization community periodontal index was used to define periodontitis. We defined periodontitis when the community periodontal index was “code 3” or greater, which means that at least one site had a pocket. larger than 3.5 mm. The tooth index numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46, and 47. An appropriate community periodontal index probe was used in accordance with the World Health Organization guidelines [22]. We divided the mouth into sextants, and used an approximately 20-g force for probing. The mean kappa value for the interexaminer reliability was 0.89 (0.55–1.00) [23]. Osteopenia and osteoporosis The diagnosis of osteopenia and osteoporosis was based on the measurement of BMD using the dual-energy X-ray absorptiometry results for the LS, TF, and FN according to the World Health Organization diagnostic classification [24]. Osteopenia was defined as a BMD of 1.0 standard deviation below the peak bone mass of a young, healthy, sex- and race-matched reference population, and osteoporosis was defined as a BMD of 2.5 standard deviations as follows [25]: (1) normal bone mass, −1.0
