The current study adopted data from the 2008-2009 KNHANES. KNHANES is a nationwide population survey conducted by the Korean Center for Disease Control and Prevention. This study included 2322 Korean subjects (959 men, 1363 women) over the age of 65. To include a representative sample of the population, a clustered, multistage, and stratified probability approach was applied. This study consisted of a nutritional examination, a general health interview, a health assessment and an oral examination. All participants provided written informed consent after approval from the Institutional Review Board of the Korean Center of Disease Control and Prevention. The ethical approval of this study protocol was exempted by the Institutional Review Board of Tertiary University Hospital (AJIRB-MED-EXP-21–307). Data from eligible participants over 65 years of age were included and participants with missing data in the health assessments, questionnaires, BMD measurement and oral examination were excluded (Fig. 1).
Qualified personnel measured the weight (kg) and height (cm) of all participants. Body Mass Index (BMI) was calculated by dividing weight by height squared31.
Total body dual-energy X-ray absorptiometry (DXA) was applied using a QDR Discovery fan beam densitometer (Hologic, Bedford, MA, USA). The areal BMDs (aBMDs) of the total hip, femoral neck, and lumbar spine and body lean mass were assessed using DXA32. Data from DXA was analyzed using the standard techniques of the Korean Society of Osteoporosis and Hologic Discovery software (version 13.1).
Sociodemographic parameters, parental history of osteoporosis and individual history of fractures and falls
The data on socio-demographics and health behaviors such as cigarette smoking, alcohol consumption, level of physical activity were determined by a self-administered KNHANES survey. Monthly household income and number of household members were collected for each participant and participants were then divided into the following four different categories: < 25% (the lowest quartile group), 25-49%, 50-74%, and 75-100 % (the highest quartile group). Educational attainment was also classified into four groups based on the Korean education system: under elementary school (≤ 6 years of institutionalized education), middle school (7-9 years of institutionalized education), high school (10-13 years of institutionalized education), and college or higher education (≥ 14 years of institutionalized education).Cigarette smoking behavior was categorized into the following three groups: non-smokers, smokers who currently smoke and have smoked less than five packs in their lifetime, and smokers who currently smoke and have smoked more than five packs in their lifetime. Alcohol consumption was divided into the following two groups: no or light drinkers (0-3 days/month) and moderate to heavy drinkers (≥ 4 days/month). Physical activity level was measured using the Korean version of the short form of the International Physical Activity Questionnaire (IPAQ).33. Respondents were grouped as those who performed high/moderate intensity physical activity for more than 30 minutes or more than 5 times per week, respectively.
Data were collected on parental history of osteoporosis and individual history of fractures of the spine, hip, or distal radius. Data on individual falls experiences in the past year are also included.
Diagnosis of the metabolic syndrome was made based on the criteria proposed in previous reports34.35. Metabolic syndrome was diagnosed if participants met at least three of the following five criteria: 1) a clinical diagnosis of diabetes treated with oral hypoglycemic medication or insulin or a fasting serum glucose level of 110 mL/dL or higher; 2) arterial blood pressure of 130/85 mm Hg or higher or current use of antihypertensive drugs; 3) plasma triglyceride level of 150 mg/dL or higher; 4) high-density lipoprotein cholesterol level of ≤ 50 mg/dL for women or ≤ 40 mg/dL for men; or 5) a waist measurement of more than 80 cm for women or 90 cm for men.
Assessment of oral health status
Oral examinations were performed by trained dentists. Periodontal health status was determined using the Community Periodontal Index (CPI) based on WHO criteria36. CPI scores were categorized as follows: 0, healthy gums; 1, gum bleeding; 2, presence of calculus; 3, pocket depth of 3.5-5.5mm; and 4, pocket depth of 5.5 mm or more. The ten point teeth were #11, 16, 17, 26, 27, 31, 36, 37, 46, and 47. If no point tooth was present in a sextant eligible for study, the adjacent remaining tooth in that sextant was selected . The Decayed, Missing, and Filled permanent Teeth (DMFT) index and the number of teeth present were also measured37. Tooth patterns, including samples with more than 20 teeth, teeth with more than 0 but less than 20, and edentulous were also determined.
Fracture probability calculations
The 10-year probabilities of major fractures and hip fractures were calculated using the FRAX tool (version 3.7, South Korean model), which calculated the probability based on age, sex, aBMD of the femoral neck, individual fracture history, parental history of hip fractures, current tobacco use, rheumatoid arthritis, alcohol use (more than three units per day), secondary osteoporosis, and long-term use of glucocorticoids29. Data on individual history of fractures, current tobacco use, rheumatoid arthritis, alcohol use and secondary osteoporosis were collected from the health surveys. Since the 2008-2009 KNHANES did not include data on long-term glucocorticoid use or parental history of hip fractures, negative responses were entered into the FRAX tool as in previous reports38,39,40.
Statistical analyzes were performed based on a complex design including stratification, clustering and weighting. Sample weights were constructed for the sample participants to represent the Korean population by taking into account non-response, complex survey design, and stratification (by age, gender, and geographic area).
All analyzes were performed separately for males and females due to the different amounts of skeletal muscle mass and background bone metabolism between the sexes. The participants were divided into three groups based on the 10-year probable risk of major fracture41. Those participants whose FRAX scores were less than 10% were classified as a low-risk group (10% > FRAX score), whose FRAX scores were between 10 and 20% as a moderate-risk group (20 > FRAX score ≥ 10%), and whose FRAX scores above 20% belonged to the high-risk group (FRAX score ≥ 20%). Independent t-tests and Rao-Scott chi-square tests were applied to compare the differences in the sociodemographic, anthropometric, and behavioral factors, number of teeth, DMFT, CPI, 10-year probabilities of major and hip fractures, fat-free mass, and skeletal BMD for continuous and categorical variables. Multivariate linear regression analysis was applied to analyze the associations between the 10-year probabilities of major or hip fractures and factors related to oral health, adjusted for the possible confounding factors such as lean body mass, presence of metabolic syndrome, parental history of osteoporosis, and recent experience with falls. Each anthropometric and sociodemographic variable with a significant association with FRAX scores in the univariate analysis was integrated into the multivariate linear regression analysis to identify interdependent contributions. The variables included in the calculation of the FRAX score, such as age, aBMD of the femoral neck, individual fracture history, current smoking and alcohol consumption, were excluded in multivariate analysis. Finally, the independent variables were the total number of teeth, DMFT, CPI, lean body mass, incidence of metabolic syndrome, fall history and parental osteoporotic history and the outcome variables were the probability of major fracture and the probability of hip fracture.
Ethical approval and informed to consent
Written informed consents were obtained from all participants after approval from the Institutional Review Board of the Korean Center for Disease Control and Prevention. The ethical approval of this study protocol was exempt by the University Hospital Institutional Review Board (AJIRB-MED-EXP-21–307).